Exceso de Peso en Adolescentes

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Exceso de peso en adolescentes: inﬂuencia del estrés social en el rendimiento

neuropsicológico y efecto de la visualización de imágenes de alimentos en la
activación cerebral y to...
Thesis · October 2018
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UNIVERSIDAD DE JAÉN
FACULTAD DE HUMANIDADES Y CIENCIAS DE LA
EDUCACIÓN
DEPARTAMENTO DE PSICOLOGÍA
TESIS DOCTORAL
Exceso de peso en adolescentes: influencia del
estrés social en el rendimiento neuropsicológico
y efecto de la visualización de imágenes de
alimentos en la activación cerebral y toma de
riesgos.
PRESENTADA POR:
MARÍA MORENO PADILLA
DIRIGIDA POR:
Dr. Gustavo. A Reyes del Paso

Dra. María Josefa Fernández Serrano
Dr. Antonio Verdejo García
JAÉN, 5 JULIO DE 2018

1
“Soy de las que piensan que la ciencia
tiene una gran belleza. Un científico en su
laboratorio no es sólo un técnico:
también es un niño colocado ante
fenómenos naturales que lo impresionan
como un cuento de hadas”
(Marie Curie)
2
3
ÍNDICE
Datos identificativos...................................................................................................................... 6
Autorización .................................................................................................................................. 7
Agradecimientos ........................................................................................................................... 8
Resumen ...................................................................................................................................... 14
I. INTRODUCCIÓN .......................................................................................................... 20
Capítulo 1. Obesidad ............................................................................................................... 22
1. Definición y datos epidemiológicos ............................................................................ 24
2. Factores predisponentes y relevancia clínica del problema ........................................ 25
Capítulo 2. Rendimiento neuropsicológico, toma de riesgos e impulsividad en la obesidad.. 30
1. Rendimiento neuropsicológico .................................................................................... 32
2. Toma de riesgos e impulsividad .................................................................................. 36
Capítulo 3. Estrés social y obesidad ........................................................................................ 42
1. Estrés social en adolescentes con exceso de peso ....................................................... 44
2. Influencia del estrés social sobre la conducta alimentaria........................................... 46
3. Reactividad psicofisiológica al estrés.......................................................................... 49
Capítulo 4. Cerebro y obesidad ............................................................................................... 54
1. Singularidades psicobiológicas del neurodesarrollo de la adolescencia ..................... 56
2. Sistemas cerebrales asociados al comportamiento alimenticio ................................... 58
3. La “adicción” a la comida ........................................................................................... 61
4. Estudios de activación cerebral relacionados con la motivación por la comida ......... 65
II. JUSTIFICACIÓN, OBJETIVOS E HIPÓTESIS ............................................................ 68
Capítulo 5. Justificación, objetivos e hipótesis de la tesis....................................................... 70
1. Justificación y objetivo principal ................................................................................ 72
2. Objetivos específicos................................................................................................... 73
3. Hipótesis ...................................................................................................................... 75
III. MEMORIA DE TRABAJOS .......................................................................................... 78
Capítulo 6. Social stress increases cortisol and hampers attention in adolescents with excess
weight ...................................................................................................................................... 80
1. Introduction ................................................................................................................. 82
2. Methods ....................................................................................................................... 83
3. Results ......................................................................................................................... 88
4. Discussion ................................................................................................................... 93
5. References ................................................................................................................... 97
4
Capítulo 7. Negative social evaluation impairs executive functions in adolescents with excess
weight: associations with autonomic responses. ................................................................... 106
1. Introduction ............................................................................................................... 108
2. Method ...................................................................................................................... 110
3. Results ....................................................................................................................... 114
4. Discussion ................................................................................................................. 118
5. References ................................................................................................................. 125
Capítulo 8. Risky decision-making after exposure to a food-choice task in excess weight
adolescents: relationships with high-calorie food preferences and hunger ........................... 132
1. Introduction ............................................................................................................... 134
2. Methods ..................................................................................................................... 137
3. Results ....................................................................................................................... 141
4. Discussion ................................................................................................................. 146
5. References ................................................................................................................. 152
Capítulo 9. Increased food choice-evoked brain activation in adolescents with excess weight:
relationship with subjective craving...................................................................................... 160
1. Introduction ............................................................................................................... 162
2. Methods ..................................................................................................................... 165
3. Results ....................................................................................................................... 170
4. Discussion ................................................................................................................. 174
5. References ................................................................................................................. 181
IV. DISCUSIÓN, CONCLUSIONES Y PERSPECTIVAS FUTURAS............................. 190
Capítulo 10. Discusión .......................................................................................................... 192
1. Implicaciones teóricas ............................................................................................... 196
2. Implicaciones clínicas ............................................................................................... 201
3. Fortalezas y limitaciones ........................................................................................... 205
Capítulo 11. Conclusiones..................................................................................................... 206
Capítulo 12. Perspectivas futuras .......................................................................................... 210
V. DOCTORADO INTERNACIONAL ............................................................................ 214
1. Summary ................................................................................................................... 216
2. Conclusions ............................................................................................................... 219
3. Future perspectives.................................................................................................... 220
VI. REFERENCIAS BIBLIOGRÁFICAS .......................................................................... 222
VII. ANEXOS....................................................................................................................... 250
5
Datos identificativos
María Moreno Padilla

D.N.I 77359772-P
Licenciada en Psicología
Máster en Intervención Psicológica en ámbitos clínicos y de la salud
Universidad de Jaén
Departamento de Psicología
Área de Personalidad, Evaluación y Tratamiento Psicológico
6
Autorización
Gustavo A. Reyes del Paso, Catedrático de Personalidad, Evaluación y Tratamiento
Psicológico de la Universidad de Jaén (España), María José Fernández Serrano,
Profesora de Metodología de las Ciencias del Comportamiento de la Universidad de
Jaén (España) y Antonio Verdejo García, Profesor en School of Psychological Sciences
en la Universidad de Monash (Australia)
Garantizan que:
La Tesis Doctoral titulada: “Exceso de peso en adolescentes: influencia del estrés social
en el rendimiento neuropsicológico y efecto de la visualización de imágenes de
alimentos en la activación cerebral y toma de riesgos.”, realizada por la doctoranda
María Moreno Padilla, ha sido elaborada bajo nuestra dirección y reúne las condiciones
de calidad, originalidad y rigor científico necesarias para que se proceda a su defensa
pública de acuerdo con la legislación vigente.
Fdo. Gustavo. A Reyes del Paso
Fdo. María José Fernández Serrano
Fdo. Antonio Verdejo García
Jaén, a 5 de Julio de 2018.
7
Agradecimientos
Caminante, son tus huellas

el camino y nada más;
Caminante, no hay camino,
se hace camino al andar.
Al andar se hace el camino,
y al volver la vista atrás
se ve la senda que nunca
se ha de volver a pisar.
Caminante no hay camino
sino estelas en la mar
Decía Machado que solo se hace camino al andar, y así es. Yo, hace cuatro años, decidí
escoger y caminar este sendero y, mirando atrás, contemplo mis huellas y pienso en lo
mucho que se aprende, al andar, sobre los pasos que volverás y los que no volverás a
dar. Porque al final el aprendizaje es precisamente eso, equivocarte, volver un poco
atrás en el camino, aprender y seguir adelante. Al final, como decía Machado, son
nuestras decisiones las que van construyendo nuestro propio sendero.
Y el camino que conlleva la realización de una tesis doctoral no es fácil, pero en este
sendero no estás tú solo, siempre hay personas con las que te cruzas y te alegran el
camino, personas que agradeces todos los días que realicen el camino a tu lado,
personas que están apeadas en la acera y que sabes que cuándo las necesites acudirán a
tu llamada para ofrecerte agua, alimento o cualquier cosa que esté en sus manos para
que sigas caminando.
Este apartado de mi tesis doctoral se trata de eso, de dar las gracias a todas las personas
que hicieron más fácil recorrer este camino.
8
Agradecimientos
En primer lugar, quería agradecer a mis directores de tesis el brindarme la oportunidad
de aprender de ellos y realizar este trabajo bajo su tutela. A Gustavo, porque no he
conocido nunca a una persona más tenaz, inteligente y dedicado a su trabajo. Gracias
por darme esta oportunidad, por dedicarme parte de tu tiempo y ayudarme siempre que
lo he necesitado. Te estaré siempre agradecida por todo lo que me has enseñado. A
Antonio, por permitirme adentrarme en un mundo desconocido como era para mí el
tema de la neuroimagen. Y, por último, a María José, gracias por todo, por ser un
referente para mí, por pensar en mi futuro cuando esto acabe, por sus palabras de apoyo
y ánimo que siempre me consuelan en los momentos de bajón, por querer siempre lo
mejor para mí y por demostrarme que, aunque el camino pueda llegar a ser muy
complicado en algún momento, hay que seguir caminando. Y a María, por ser su luz en
su propio camino.
Deseo también expresar mi agradecimiento a la Universidad de Jaén por haber facilitado
los medios suficientes para llevar a cabo el desarrollo de las diferentes investigaciones
que componen este trabajo.
Gracias también a mi supervisor de Estancia Pre-doctoral Robert Whelan, por darme la
oportunidad de visitarles y acogerme durante 3 meses en el Instituto de Neurociencias
del Trinity College de Dublín (Irlanda). Y a Marga, Chris y la pequeña Arianna por
acogerme en su casa durante esos tres meses y hacerme sentir como parte de su familia.
También quiero agradecer a Juan Verdejo, por enseñarme todo lo que sé sobre
neuroimagen y por acogerme siempre con una sonrisa en mis primeros años de tesis
doctoral durante mis viajes a Granada. Las cosas hubieran sido mucho más difíciles sin
ti.
9
Agradecimientos
No puedo olvidarme de mis compañeros de despacho y amigos, esos que en cuatro años
han hecho que los días se pasaran más rápido y que siempre estaban ahí cuando
necesitaba apoyo. Gracias a Pablo, José Andrés, Pedro, Gabi, Rocío Donaire, Sonia,
Loida, Carmen, Teresa y Rocío Linares. En especial quiero agradecer a Pablo por estar
conmigo desde el principio del camino, por ayudarme siempre, por pensar siempre en el
bien del otro y porque tus logros me alegran y sé que los míos también te alegran a ti.
No sé dónde nos llevaran nuestros caminos, solo espero que no se separen. A Rocío
Linares por convertirse en una amiga de esas que llegan tarde en el camino pero que ya
se quedan para siempre. Gracias por ser una amiga en la que apoyarse y confiar, por
poder contante mis éxitos y fracasos, por ser una de las personas más buenas que
conozco, además de trabajadora como nadie, te quiero amiga. A Teresa, por su risa que
ilumina el despacho, por sus preguntas “tecnológicas” que siempre me hacen sentir útil
y por hacerme sentir afortunada de tener su amistad.
Por supuesto, agradecer también a todos los participantes de los estudios, sin ellos no
hubiera sido posible. Y a mis alumnos del grado de Psicología, espero que ellos hayan
aprendido de mis clases al igual que yo lo he hecho de la experiencia tan gratificante
que es la enseñanza.
También le tengo que agradecer a este trabajo el haberme encontrado con María del
Mar. La conocí en mi primer congreso, en Cádiz, y desde ahí compartimos experiencias
y recuerdos. Gracias por escucharme, entenderme y apoyarme siempre. Este trabajo nos
ha unido, pero ya caminemos siempre juntas.
También quiero agradecer a mis amigas de toda la vida, Isabel, Rocío, os quiero y
aunque este trabajo me ha quitado de muchos momentos con vosotras sabéis que
siempre estaremos juntas. También, dar las gracias a Lucía, porque en la carrera se
10
Agradecimientos
conocen personas maravillosas y algunas tienes la suerte de que se quedan contigo para
siempre. Todavía nos quedan muchas aventuras por vivir amiga.
Por supuesto quiero agradecer a toda mi familia por acompañarme y entenderme todos
estos años. Pero, en especial, quiero dar unas gracias inmensas, tan grandes que no
tendría suficiente espacio en este apartado para hacerlo, a mis padres y hermana. Ellos
son el motor que me ha dado fuerzas para seguir siempre adelante, cuando he flaqueado
me han infundido ánimos, cuando he tropezado con alguna piedra me han ayudado a
levantarme, siempre me han querido de manera incondicional y eso, en un mundo en el
que el miedo al fracaso pulula por cada rincón, es fundamental. Sin ellos, que están
conmigo desde el origen del camino, no hubiera sido posible. Os quiero.
Por último, quiero dar las gracias a mi marido. A Juan Antonio, por apoyarme siempre y
aguantar mis malos ratos, por transmitirme su eterna positividad y hacer que un día
malo se convierta en bueno, por todos estos años de felicidad a tu lado, por ser mi luz en
el camino, GRACIAS. Te quiero.
¡Gracias a todos/as!
11
A mis padres Eduardo y Mercedes
A mi marido Juan Antonio
A mis profesores que me inculcaron su amor por la enseñanza
12
13
Resumen
14
15
Resumen
El aumento en la prevalencia de la obesidad se ha convertido en las últimas décadas,
según la Organización Mundial de la Salud, en uno de los principales problemas de
salud pública a nivel mundial. La obesidad es una condición compleja en la que
intervienen multitud de factores.
En la antigüedad, las personas regulaban su ingesta según sus estados metabólicos de
hambre y saciedad, sin embargo, en las sociedades occidentales actuales qué y cuánto
comer se ha convertido en una cuestión de toma de decisiones. Estudios recientes
apuntan a que el cambio en el estilo de vida actual, basado en el sedentarismo y hábitos
alimenticios no saludables, es el responsable del drástico aumento de la prevalencia de
la obesidad.
El exceso de peso y la obesidad también han aumentado exponencialmente en la
infancia y la adolescencia, etapas críticas en el desarrollo del individuo. La adolescencia
es una etapa en la que el individuo es especialmente vulnerable debido a sus
peculiaridades comportamentales. En esta etapa son frecuentes los comportamientos
dirigidos a la búsqueda de recompensa y propensión al riesgo, así como una
disminución del control ejecutivo y la capacidad de regulación efectiva del
comportamiento. En este sentido, distintos estudios confirman la existencia de
alteraciones en el funcionamiento ejecutivo en adolescentes con exceso de peso
comparados con adolescentes con peso saludable. Las funciones ejecutivas permiten
una mejor regulación del comportamiento, y específicamente, del comportamiento
alimenticio.
Por otro lado, el exceso de peso en la adolescencia no solo provoca consecuencias
negativas a nivel de salud (diabetes tipo II, mayor probabilidad de desarrollar obesidad
en la edad adulta y sus perjudiciales consecuencias médicas, etc.) sino que también está
16
Resumen
asociado a un incremento del estrés social debido fundamentalmente a las frecuentes
burlas que reciben por parte de sus iguales referidas a su imagen corporal y que, incluso,
pueden llevar a la marginalización y exclusión social. Por tanto, los adolescentes con
exceso de peso sufren mayor estrés social en su día a día. Numerosos estudios señalan
el efecto perjudicial que produce el estrés en el rendimiento cognitivo. Así mismo, el
estrés también puede alterar los patrones de alimentación a través de diversos
mecanismos.
Como hemos comentado anteriormente, los mecanismos homeostáticos han quedado en
segundo lugar para explicar el comportamiento alimenticio, siendo los procesos de toma
de decisiones extremadamente importantes en esta cuestión. En concreto, el
comportamiento impulsivo puede jugar un importante papel en la obesidad durante la
infancia y la adolescencia. Distintos estudios han mostrado que la visualización de
señales relacionadas con el consumo de drogas produce un incremento en los niveles de
impulsividad e induce a una mayor toma de riesgos, incrementando como consecuencia
el riesgo de consumo en individuos adictos a sustancias. Asimismo, varios estudios
demuestran que las personas con exceso de peso tienen un sesgo atencional y mayor
reactividad hacia señales de alimentos altos en grasas y/o azúcares.
Por otra parte, en los últimos años distintas investigaciones subrayan la superposición
de las vías neurobiológicas implicadas en la adicción a sustancias y en la obesidad
derivando en la creación del concepto “adicción a la comida”. Las drogas de abuso
utilizan los mismos mecanismos neurales que modulan la motivación para consumir
alimentos, por lo tanto, existe un paralelismo entre los circuitos cerebrales implicados
en la pérdida de control y la ingesta excesiva de alimentos que caracteriza la obesidad y
el consumo compulsivo de drogas propio de la adicción. La alteración de los circuitos
cerebrales de dopamina es central en estas dos patologías. Concretamente, el sistema de
17
Resumen
recompensa cerebral es un componente central para desarrollar y monitorear
comportamientos motivados. Por lo tanto, el conocimiento de su funcionamiento es vital
para comprender mejor el problema de la obesidad. Ante la visualización de alimentos
altamente apetecibles o de gran aporte energético, las áreas del circuito de la
recompensa pueden promover una mayor liberación de dopamina debido a la gran
saliencia que tiene el estímulo y conllevar así a una mayor predisposición a la
sobreingesta, al igual que sucede en estudios con poblaciones adictas a sustancias. En
general, los resultados de los estudios de neuroimagen realizados hasta ahora señalan
una respuesta incrementada en áreas del circuito de la recompensa, tanto en adultos
como en adolescentes con exceso de peso, al procesar imágenes de comida,
especialmente aquellas con un alto contenido en grasas y azúcares.
Tomando en consideración todo lo expuesto, los objetivos de esta tesis doctoral fueron:
1) estudiar la influencia del estrés social sobre el rendimiento neuropsicológico, en
adolescentes con exceso de peso y adolescentes con normopeso, 2) analizar la influencia
de la visualización de alimentos en una tarea de toma de decisiones de riesgo y su
relación con la impulsividad, en adolescentes con exceso de peso comparados con
adolescentes con normopeso, y 3) analizar el procesamiento cerebral durante las
elecciones alimenticias y su relación con el craving subjetivo, en adolescentes con
exceso de peso y adolescentes con normopeso.
Para abordar estos objetivos se llevaron a cabo 4 estudios. Los resultados obtenidos
mostraron: 1) el estrés social se asocia con un peor rendimiento atencional y ejecutivo
en adolescentes con exceso de peso, experimentando estos mayor reactividad
autonómica ante ese estrés, con respecto a los adolescentes con normopeso (estudio 1 y
2); 2) los adolescentes con exceso de peso toman decisiones más arriesgadas tras la
visualización de señales de alimentos y presentan mayores niveles de impulsividad que
18
Resumen
los adolescentes con normopeso (estudio 3); y 3) se produce mayor activación de áreas
cerebrales relacionadas con el circuito de la recompensa en el grupo de adolescentes con
exceso de peso y observamos una asociación de la activación en estas áreas con el
craving informado por los participantes hacia los alimentos presentados en la tarea
(estudio 4).
Estos resultados podrían resultar de enorme utilidad tanto a nivel teórico, contribuyendo
al avance del conocimiento de los factores que están predisponiendo al aumento de peso
en la adolescencia, como a nivel clínico, impulsando nuevos tratamientos que tengan en
cuenta variables neuropsicológicas y emocionales que contribuyan a mejorar las
intervenciones pediátricas dirigidas a reducir los problemas de exceso de peso.
19
I. INTRODUCCIÓN
20
21
Capítulo 1
Obesidad
22
23
Capítulo 1. Obesidad
1. Definición y datos epidemiológicos
La Organización Mundial de la Salud (OMS) define la obesidad como una acumulación
anormal y excesiva de grasa que puede ser perjudicial para la salud del individuo que lo
padece. Tradicionalmente, instituciones como la OMS o la WOF (“World Obesity
Federation” [anteriormente, International Obesity Task Force, (IOTF)], recomiendan
utilizar el Índice de Masa Corporal (IMC) como medida de estimación del sobrepeso y
la obesidad en los estudios de población (Pérez-Rodrigo, Bartrina, Majem, Moreno y
Rubio, 2006). Este índice se calcula dividiendo el peso, en kilogramos, entre el
cuadrado de la altura, en metros (kg/m2). Para adultos, la OMS definió los umbrales
indicando que un IMC mayor a 25 kg/m2 está asociado a sobrepeso, y un IMC superior
a 30 kg/m2 a obesidad. En la edad adulta, estos puntos de corte están bien establecidos
ya que, parece ser, que en esta etapa el IMC tiene una alta asociación con la grasa
corporal o adiposidad, y también con las complicaciones clínicas derivadas de ésta
(Flegal y Ogden, 2011). Sin embargo, en el caso de niños y adolescentes la
determinación del IMC es más complicada ya que está asociado de forma más indirecta
con el grado de adiposidad (Rolland-Cachera, 2011). La clasificación de la obesidad en
la niñez y adolescencia se realiza siguiendo las indicaciones del IOTF (Cole, Bellizzi,
Flegal y Dietz, 2000), las cuáles sugieren utilizar valores de IMC ajustados por edad (2-
18 años) y sexo. Según esta clasificación, valores de percentil mayores de 85 se asocian
a sobrepeso, mientras que se considera obesidad si estos valores superan el percentil 95.
Según la OMS, el aumento de la prevalencia de la obesidad se ha convertido en las
últimas décadas en uno de los principales problemas de salud pública a nivel mundial.
La prevalencia mundial de la obesidad casi se duplicó en el período comprendido entre
1980 y 2008, afectando en 2008 a quinientos millones de hombres y mujeres mayores
24
de 20 años, siendo más frecuente en las mujeres que en los hombres. Según este
organismo, en 2014, más de 1900 millones de adultos de 18 ó más años tenían
sobrepeso, de los cuales, más de 600 millones eran obesos, mientras que 41 millones de
niños menores de cinco años tenían sobrepeso o eran obesos (OMS).
Por su parte, la WOF informa que si se mantiene la tendencia actual se calcula que en
2025 cerca de 2.700 millones de adultos tendrán sobrepeso, más de 1.000 millones
tendrán obesidad y 177 millones de adultos sufrirán gravemente las consecuencias de
ésta. La última evaluación del Instituto Médico Europeo de la Obesidad en 2014 indicó
que, para esa fecha, el 21,1% de los niños españoles presentaban sobrepeso y el 8,2%
presentaban obesidad, con lo que casi uno de cada tres niños de entre 3 y 12 años tenía
exceso de peso. Datos del Centro Nacional de Investigaciones Cardiológicas indican
que el porcentaje de la obesidad infantil ha aumentado un 35% en la última década. En
esta misma línea, el informe de la Organización para la Cooperación y el Desarrollo
Económicos (OCDE), en Estados Unidos y Gran Bretaña, indica que el 40% de la
población infantil padece de obesidad. España es el segundo país de la Unión Europea,
detrás de Gran Bretaña, con mayor porcentaje de niños obesos o con sobrepeso entre los
7 y los 11 años. De este modo, la obesidad se ha convertido en una epidemia que afecta
cada año a 400.000 niños en todo el mundo (WOF, 2018).
2. Factores predisponentes y relevancia clínica del problema
Dada la alta prevalencia del sobrepeso y la obesidad en la adolescencia y el aumento de
la severidad de esta, resulta de vital importancia conocer cuáles son los factores
específicos que están causando o manteniendo dicha situación y qué consecuencias
conlleva el exceso de peso en esta etapa.
25
La obesidad es una condición compleja en la que no solo influyen procesos metabólicos
como el ingreso y gasto calórico. Los factores que pueden desencadenar la obesidad,
son numerosos y de diversa índole, incluyendo factores genéticos, endocrinos,
psicológicos y socioculturales. En cuanto al factor genético, aunque la ciencia ha
demostrado que los genes pueden predisponer al sobrepeso (Locke y cols., 2015), este
solo se produce cuando se combinan con otros factores, como los hábitos alimenticios y
el estilo de vida (Martínez-Gómez y cols., 2011). De hecho, la genética por sí sola no
puede explicar el rápido aumento de la obesidad en distintos países del mundo. Por otro
lado, existen algunas alteraciones de la función endocrina que pueden provocar la
obesidad, como el síndrome de Cushing (una enfermedad provocada por el aumento de
la hormona cortisol), alteraciones en la tiroides, o el hipogonadismo (Wierman, 2003).
En cuanto a los factores socioculturales, el aumento del sedentarismo, el cambio en los
patrones de sueño, así como la total disponibilidad que tenemos de alimentos altamente
calóricos a precios asequibles en las sociedades occidentales actuales (Sahoo y cols.,
2015; Ellulu, Abed, Rahmat, Ranneh y Ali, 2014), son variables a tener en cuenta a la
hora de abordar el problema del aumento de prevalencia de la obesidad. El sedentarismo
afecta a adultos (mayor uso de transportes, ascensores, escaleras mecánicas, tiempo
dedicado a la televisión, etc.), pero también a niños y adolescentes, los cuales pasan
mucho tiempo sentados, ya sea mirando televisión o utilizando dispositivos
electrónicos, como las consolas de videojuegos, los ordenadores portátiles o los
smartphones. Esto provoca que el gasto energético sea bajo y que resulte difícil
deshacerse de las calorías consumidas. Por otro lado, el sueño deficiente es cada vez
más común en los niños y las asociaciones entre la corta duración del sueño en la
primera infancia y la obesidad se encuentran consistentemente a través de la literatura
(Hasler y cols., 2004; Cappuccio y cols., 2008; Miller, Lumeng & LeBourgeois, 2015).
26
Los factores psicológicos también son de vital importancia a la hora de entender la
obesidad. En ocasiones, las personas recurren a la comida cuando se encuentran bajo
estados emocionales negativos (estrés, tristeza, enfado, frustración, soledad, etc.) como
una forma de liberar su ansiedad (Faith, Allison & Geliebter, 1997).
Todos los factores anteriormente mencionados confluyen a la hora de crear una
determinada predisposición a desarrollar obesidad. Además, algunos estudios indican
que los drásticos cambios producidos en el entorno y el estilo de vida han modificado la
forma en la que percibimos los alimentos y regulamos su ingesta (Zheng, Lenard, Shin
y Berthoud, 2009). Nuestros antepasados comían para asegurar la supervivencia, ellos
se guiaban solamente por sus sistemas de regulación metabólica (hambre y saciedad).
Sin embargo, actualmente, qué y cuánto comer se ha convertido en una cuestión de
toma de decisiones, otorgamos a la comida un valor hedónico similar al que otorgamos
a otras actividades reforzantes (Zheng y cols., 2009). Además, diversos estudios han
encontrado que los alimentos altamente apetitosos (altos en grasas y/o azúcares) activan
regiones del área de recompensa cerebral, al igual que hacen las drogas de abuso, lo que
conlleva que este tipo de alimentos tengan un valor hedónico y reforzante similar,
pudiendo llegar a convertirse en un comportamiento abusivo y compulsivo (Volkow,
Wang, Fawler y Telang, 2008; Volow, Wang, Fowler, Tomasi, Baler, 2011; Volkow,
Wang, Tomasi y Baler, 2013).
En cuanto a las consecuencias del exceso de peso en la adolescencia, la obesidad se
relaciona con un mayor número de complicaciones médicas directas (tolerancia a la
glucosa, diabetes tipo 2) e indirectas (absentismo escolar, visitas al médico), además de
mayor riesgo cardiovascular en la edad adulta y los costes sociales que no pueden ser
directamente estimados (Lobstein, Baur y Uauy, 2004; Baker, Olsen, Sorensen, 2007;
DeBoer, 2013; Goran, Ball y Cruz, 2003).
27
En concreto, la diabetes tipo 2, conocida hasta hace poco tiempo como diabetes del
adulto, ya que prácticamente sólo aparecía en la edad adulta, ha aumentado de forma
significativa entre niños y adolescentes de todo el mundo en los últimos 15 años. La
diabetes está estrechamente relacionada con el exceso de peso, por lo tanto, la causa de
este aumento parece ser el incesante crecimiento de la obesidad infantil (DeBoer, 2013;
Goran y cols., 2003). El aumento de peso, los hábitos alimenticios no saludables y la
falta de actividad física provocan un mal funcionamiento de la insulina causando una
alteración denominada “resistencia a la insulina”. Al principio, el cuerpo compensa este
déficit aumentando la producción de insulina. Sin embargo, con el tiempo y debido a
que cada vez se consumen más alimentos ricos en azúcares y harinas refinadas, la
capacidad del páncreas para incrementar la producción no se mantiene y el
azúcar/glucosa en sangre empieza a aumentar, provocando finalmente una diabetes tipo
2.
También, existe evidencia de que el exceso de peso es un factor de riesgo para
desarrollar problemas de ajuste social en la adolescencia (Puhl y Heuer, 2009), así como
problemas de baja autoestima, estigmatización y síntomas depresivos (Chaiton y cols.,
2009). Por tanto, los adolescentes con exceso de peso sufren de más estrés social que
sus compañeros con normopeso. De este modo, la evaluación de los posibles efectos
que el estrés social pueda estar causando en el procesamiento cognitivo y la toma de
decisiones de los adolescentes con exceso de peso son de vital importancia a la hora de
tener un conocimiento más certero acerca de las causas que puedan estar desarrollando
y manteniendo el problema de la obesidad. Este es un tema que desarrollaremos más
profundamente en el capítulo 3.
Por otro lado, diversos estudios y revisiones recientes confirman que el exceso de peso
en la infancia y adolescencia es un fuerte factor predisponente para el desarrollo de la
28
obesidad en la edad adulta (Guo, Wu, Chumlea y Roche, 2002; Singh, Mulder, Twisk,
Van Mechelen y Chinapaw, 2008). Según la OMS, un IMC elevado en la edad adulta es
un importante factor de riesgo para desarrollar enfermedades cardiovasculares (que
fueron la principal causa de muerte en 2012), diabetes, trastornos del aparato locomotor
(en especial, osteoartritis) y algunos tipos de cánceres. Los costes médicos asociados a
la obesidad en la edad adulta parecen superar a los provocados por el consumo de
tabaco o alcohol (Sturm, 2002).
En resumen, padecer obesidad predispone al desarrollo de múltiples problemas de salud
y de ajuste social en el individuo. Estos problemas resultan aún más significativos si la
obesidad ocurre en la adolescencia.
29
Capítulo 2
Rendimiento neuropsicológico, toma de riesgos e
impulsividad en la obesidad
30
31
Capítulo 2. Rendimiento neuropsicológico, toma de riesgos e impulsividad en la obesidad
1. Rendimiento neuropsicológico
En los últimos años distintas investigaciones subrayan la superposición de las vías
neurobiológicas implicadas en la adicción a sustancias y en la obesidad, derivando en la
creación del concepto “adicción a la comida” (Volkow, Wang, Fawler y Telang, 2008;
Volow, Wang, Fowler, Tomasi, Baler, 2011; Volkow, Wang, Tomasi y Baler, 2013). En
ambas condiciones, la evaluación de la motivación por el estímulo elegido (drogas o
alimentos apetecibles) está exageradamente exaltada, mientras que el sistema de control
“top-down” que normalmente regula las respuestas guiadas por las recompensas está
alterado (Acosta, Manubay y Levin, 2008). Esta interacción anormal entre la regulación
de la motivación homeostática y el control del comportamiento ha sido relacionada con
alteraciones en las funciones ejecutivas (Berthoud, 2007).
Las funciones ejecutivas son un conjunto de habilidades implicadas en la generación, la
supervisión, la regulación, la ejecución y el reajuste de conductas adecuadas para
alcanzar objetivos complejos, especialmente aquellos que requieren un abordaje
novedoso y creativo (Gilbert y Burgess, 2008; Verdejo-García y Bechara, 2010). Se
trata de habilidades esenciales para nuestro día a día ya que se ponen en marcha en una
amplísima variedad de situaciones y su correcta competencia es vital para un
funcionamiento óptimo y socialmente adaptado. Las funciones ejecutivas se componen
tanto de recursos atencionales como de recursos mnésicos, pero su función es la de
proporcionar un espacio operativo y un contexto de integración de estos procesos con
objeto de optimizar la ejecución en función del contexto actual (externo, interoceptivo y
metacognitivo) y de la previsión de nuestros objetivos futuros (Verdejo-Barcía y
Bechara, 2010). Estas funciones, muestran importantes deterioros en pacientes con
lesiones que afectan a la corteza frontal (Stuss y Levine, 2002), lo que ha llevado a
32
considerar esta región como el principal sustrato neuroanatómico de estas habilidades,
razón por la cual en la adolescencia estas funciones están más limitadas que en la edad
adulta ya que el córtex prefrontal (PFC) no ha completado su maduración a esta edad.
Las funciones ejecutivas se dividen en cuatro componentes (Verdejo-García y Pérez-
García, 2007): actualización (formado a su vez por memoria de trabajo, razonamiento y
fluidez), control inhibitorio, flexibilidad cognitiva y toma de decisiones. El componente
de actualización implica la monitorización, actualización y manipulación de la
información “on line” en la memoria operativa. El control inhibitorio se refiere a la
capacidad para cancelar respuestas automatizadas, impulsivas o guiadas por la
recompensa que son inapropiadas para las demandas actuales. Se trata de un constructo
multidimensional asociado con distintos procesos neuropsicológicos con bases
cerebrales relativamente independientes: inhibición de respuestas, autorregulación, entre
otros. La flexibilidad cognitiva o “shifting” es la capacidad de reestructurar el propio
conocimiento de forma espontánea para dar una respuesta adaptada a las exigencias
cambiantes del ambiente. Por último, la toma de decisiones es la habilidad para
seleccionar de entre un conjunto de posibles alternativas existentes aquella que resulta
más adaptativa para el individuo (Verdejo-García y Bechara, 2010).
La alteración en las funciones ejecutivas puede ser mayor en la adolescencia, ya que se
trata de un periodo caracterizado por la inmadurez relativa de los sistemas de control
prefrontales, a su vez unido con la madurez de los sistemas subcorticales responsables
de la motivación y el procesamiento de la recompensa (Chambers, Taylor y Potenza,
2003). Por un lado, estudios con resonancia magnética funcional (fMRI) han señalado
que los adolescentes, comparados con los adultos, muestran mayor activación del
estriado ventral y de la ínsula anterior durante la anticipación de la recompensa y su
consecución (Van Leijenhorst y cols., 2009; Ernst y cols., 2005). Por otro lado, los
33
resultados de estudios cognitivos que han empleado fMRI, han mostrado que las
habilidades de control ejecutivo y sus sustratos neurales (p.ej. PFC) están todavía
mejorando su competencia durante la adolescencia temprana y tardía (Bunge y Wright,
2007; Waber y cols., 2007; Crone, Bullens, van der Plas, Kijkuit y Zelazo, 2008). Este
desequilibrio hace que la adolescencia sea un período durante el cual la actividad del
sistema de recompensa prevalece sobre la de los sistemas que gobiernan la evitación de
daños y el autocontrol (Chambers y cols., 2003). Por lo tanto, los sistemas encargados
del funcionamiento ejecutivo son sumamente importantes en esta etapa.
Respecto a la obesidad y el funcionamiento ejecutivo, distintos estudios confirman la
existencia de alteraciones en este funcionamiento en adolescentes con exceso de peso
comparados con adolescentes con peso saludable. Varios estudios (Kamijo, Khan y
cols., 2012; Kamijo, Pontifex, y cols., 2012) han mostrado una correlación negativa del
IMC con el rendimiento en control cognitivo en un grupo de pre-adolescentes con
obesidad. Respecto al componente de inhibición, un estudio de Anzman y Birch (2009)
señaló que los participantes con bajo control inhibitorio a los 7 años tendían a tener un
IMC mayor a los 15 años. Riggs, Huh, Chou, Spruijt-Metz y Pentz (2012) y Riggs,
Spruijt-Metz, Chou y Petz (2012) señalaron que los niños altamente sedentarios que no
eran conscientes de su peso y consumían alimentos altos en grasas y/o azúcares
mostraban menor control inhibitorio que los niños activos que consumían frutas y
verduras. Asimismo, distintos estudios han señalado que los adolescentes con obesidad
muestran peor control inhibitorio y, por lo tanto, peor rendimiento en tareas go/no go y
de retraso de la recompensa (tareas “delay-discounting”) que el grupo con peso
saludable (Pauli-Pott, Albayrak, Hebebrand y Pott, 2010; Bruce, Martin y Savage,
2011). Respecto a la memoria de trabajo (el componente de actualización más
estudiado), Riggs, Huh y cols (2012) y Riggs, Spruijt-Metz y cols (2012) también
34
señalaron una correlación negativa entre el sedentarismo y el consumo de alimentos
altos en grasas y/o azúcares y el rendimiento en este componente. Por otro lado,
Maayan, Hoogendoorn, Sweat y Convit (2011) también encontraron que los
adolescentes con obesidad rendían peor en tareas de memoria de trabajo [Wide Range
Assessment of Learning and Memory (WRAML)] que los adolescentes con peso
saludable. En lo relacionado con la flexibilidad cognitiva, hay estudios que muestran
que los adolescentes con exceso de peso muestran peor rendimiento en este componente
en una variedad de tareas utilizadas (Trail Making Test, Test de Cartas de Wisconsin,
condición de cambio en el Test de los Cinco Dígitos, etc.) (Verdejo-García y cols.,
2010; Lokken, Boeka, Austin, Gunstad y Harmon, 2009; Cserjési, Molnár, Luminet y
Lénárd, 2007; Delgado-Rico, Río-Valle, González-Jiménez, Campoy y Verdejo-García,
2012). Por último, Verdejo-García y cols. (2010) utilizaron la Iowa Gambling Task
(IGT) para evaluar toma de decisiones y observaron que los adolescentes con sobrepeso
presentaban un rendimiento significativamente menor que los adolescentes con
normopeso.
En resumen, la evidencia científica existente revela de forma consistente una asociación
inversa entre la obesidad y las funciones ejecutivas en niños y adolescentes. Sin
embargo, es imperativo determinar la dirección de esta asociación, así como unificar el
método de evaluación de las funciones ejecutivas. En concreto, aún se desconoce si los
déficits cognitivos son anteriores al desarrollo de la obesidad (y, por tanto, pudieran
actuar como factor de vulnerabilidad) o si es una consecuencia de esta condición. Así
mismo, la variedad de instrumentos y procedimientos utilizados a través de los estudios
hacen difícil la generalización de resultados.
35
2. Toma de riesgos e impulsividad
Identificar estilos de comportamiento específicos asociados con la obesidad representa
un paso importante para mejorar potencialmente los métodos de prevención y
tratamiento. En nuestra sociedad actual, llena de alimentos altos en grasas y/o azúcares
totalmente disponibles, el autocontrol es necesario para evitar la sobre ingesta. Por lo
tanto, los mecanismos homeostáticos han quedado en segundo lugar para explicar el
comportamiento alimenticio, siendo los procesos de toma de decisiones
extremadamente importantes en esta cuestión. En concreto, el comportamiento
impulsivo puede jugar un importante papel en la obesidad durante la infancia y la
adolescencia.
La impulsividad describe la tendencia a actuar con menos previsión, y predispone a un
individuo a reacciones precipitadas, no planificadas, sin tener en cuenta las
consecuencias negativas y obviando las elecciones racionales a largo plazo. La
impulsividad es considerada un conjunto multidimensional que engloba múltiples
características. Uno de los instrumentos de autoinforme más utilizados para evaluar
impulsividad es el cuestionario UPPS-P (Verdejo-García, Lozano, Moya, Alcázar,
Pérez-García, 2010). El modelo que sigue este cuestionario identifica cuatro vías
diferentes que conducen al comportamiento impulsivo: urgencia (positiva y negativa),
falta de premeditación, falta de perseverancia y búsqueda de sensaciones. La urgencia
positiva se refiere a la tendencia a experimentar fuertes impulsos y falta de control
inhibitorio cuando la persona se encuentra bajo estados de ánimos positivos; mientras
que la urgencia negativa implica el aumento de la impulsividad y la falta de inhibición
bajo condiciones de afecto negativo. La falta de premeditación se refiere a la tendencia
a pensar y reflexionar sobre las consecuencias de un acto antes de participar en ese acto
o tomar una decisión. La falta de perseverancia se refiere a la capacidad de permanecer
36
enfocado en una tarea que puede ser larga, aburrida o difícil. Finalmente, la búsqueda de
sensaciones abarca dos aspectos: (a) la tendencia a disfrutar y llevar a cabo actividades
emocionantes y (b) una apertura a probar nuevas experiencias que pueden o no ser
peligrosas. La puntuación en búsqueda de sensaciones se correlaciona positivamente
con sensibilidad a la recompensa porque ambas dimensiones se relacionan con el inicio
del comportamiento de aproximación asociado con la novedad o con la perspectiva de
recompensa (Verdejo-García y cols., 2010).
La impulsividad se ha relacionado tradicionalmente con varias conductas de alto riesgo
en los jóvenes, como el consumo de sustancias (p. ej. cigarrillos, alcohol), el juego, la
agresión y el comportamiento sexual de alto riesgo (Steinberg, 2004; Miller, Naimi,
Brewer y Jones, 2007). Además, la impulsividad hace que sea más difícil resistir la
tentación de comer alimentos apetecibles normalmente altos en calorías y, por lo tanto,
puede contribuir al exceso de peso. Existe cierta evidencia de que las personas con
obesidad son más propensas a ceder ante las tentaciones y son menos efectivas para
inhibir sus impulsos. Estudios con medidas de autoinforme muestran que las personas
con obesidad son más impulsivas que las personas con normopeso y muestran
comorbilidad con otras conductas impulsivas, como el abuso de sustancias (Rydén y
cols., 2003). Además, se ha encontrado que los niños obesos son menos capaces de
retrasar la gratificación y, más a menudo, eligen una recompensa inmediata sobre una
recompensa retrasada más grande, siendo este un índice de poco auto-control (Bonato y
Boland, 1983; Best et al., 2012). Investigaciones recientes también han demostrado que
los niños y adolescentes con obesidad son menos efectivos en la inhibición de respuesta
en una tarea “stop-signal”, son más sensibles a la recompensa y toman más riesgos en
una variedad de tareas de toma de decisiones, asociándose un mayor peso a un
37
comportamiento más impulsivo (Nederkoorn, Braet, Van Eijs, Tanghe y Jansen, 2006;
Thamotharan, Lange, Zale, Huffhines y Fields, 2013; Davis, Patte, Curtis y Reid, 2010).
Las habilidades de toma de decisiones son particularmente relevantes en el caso de los
adolescentes, en quienes las transiciones cerebrales del desarrollo parecen estar
programadas para maximizar la recompensa a expensas del riesgo. Relacionado con
esto, aparece el concepto de toma de riesgos, asociado a características impulsivas y de
toma de decisiones y que ha sido ampliamente estudiado en comportamientos adictivos.
La toma de riesgos describe la tendencia a participar en un comportamiento que tiene
una probabilidad relativamente alta de un resultado negativo y está asociado con el
abuso de sustancias (Lejuez, Bornovalova, Daughters y Curtin, 2005), desórdenes
alimenticios (Boeka y Lokken, 2006), y comportamientos sexuales de riesgo (Lawyer,
2013). El exceso de peso también se asocia con la toma de riesgos ya que los
participantes con obesidad muestran patrones de toma de decisiones más arriesgadas en
la tarea IGT (Bechara, 2007), una medida usual de toma de riesgos (Boeka y Lokken,
2006; Brogan, Hevey y Pignatti, 2010). Estudios de neuroimagen también han
demostrado que los adolescentes con exceso de peso tienen una respuesta estriatal
hipersensible (Cohen y cols., 2010; Galvan y cols., 2006) y una activación aumentada
en regiones cerebrales envueltas en el fomento de la toma de riesgos [córtex
orbitofrontal (OFC)] durante la toma de decisiones (Van Leijenhorst y cols., 2009).
Una tarea ampliamente utilizada para evaluar toma de riesgos es la Balloon Analogue
Risk Task (BART) (Lejuez y cols., 2002). En esta tarea, los participantes acumulan
dinero en un banco temporal presionando un botón que infla un globo simulado. Cada
globo tiene un punto de explosión (desconocido por el participante) que, si se alcanza,
da como resultado la pérdida de todo el dinero en el banco temporal. Antes de la
38
explosión de cada globo, los participantes tienen la opción de presionar un botón de
guardar que transferirá su dinero a un banco permanente. Hay un número determinado
de globos, e independientemente de si el globo explota o se si se guarda el dinero
acumulado, el participante pasa al siguiente globo. Por lo tanto, el participante debe
equilibrar la ganancia potencial de acumular más dinero con el riesgo potencial de
perder todo el dinero acumulado en ese globo. A diferencia de la tarea IGT, tarea muy
utilizada para la evaluación de la toma de decisiones, en la que cada prueba implica una
elección entre una alternativa de riesgo y otra segura (mediante selección de cartas), la
BART implica un número variable de elecciones en un contexto de riesgo creciente (es
decir, la cantidad de dinero acumulado y la probabilidad de perder ese dinero aumenta
cada vez que se infla el globo). El riesgo en esta tarea está asociado con la ocurrencia de
conductas de riesgo en el mundo real (Lejuez, Aklin, Zvolensky y Pedulla, 2003). En
concreto, la puntuación en la BART se considera una medida de las diferencias
individuales en la propensión a tomar decisiones arriesgadas, y se ha encontrado que las
puntuaciones altas en BART se relacionan con la asunción de riesgos en la adolescencia
(Lejuez, Aklin, Zvolensky y cols., 2003), el tabaquismo (Lejuez, Aklin, Jones y cols.,
2003) y el abuso de drogas (Hopko y cols., 2006).
Por otra parte, la literatura muestra que distintos contextos o elementos como, por
ejemplo, la visualización de señales relacionadas con el comportamiento abusivo,
pueden exacerbar la tendencia impulsiva del individuo. En concreto, distintos estudios
han mostrado que la visualización de señales relacionadas con el consumo de drogas
produce un incremento en los niveles de impulsividad e induce a una mayor toma de
riesgos, incrementando como consecuencia el riesgo de consumo en estos individuos
(Field y Eastwood, 2005; Fox y cols., 2005). Asimismo, varios estudios demuestran que
las personas con exceso de peso tienen un sesgo atencional hacia señales de alimentos
39
altos en grasas y/o azúcares (Hou y cols., 2011; Castellanos y cols., 2009). Por lo que
parece razonable esperar que, del mismo modo que en los individuos adictos a
sustancias, los adolescentes con exceso de peso asuman mayores riesgos al encontrarse
en un contexto que favorezca la visualización de alimentos muy apetitosos.
40
41
Capítulo 3
Estrés social y obesidad
42
43
Capítulo 3. Estrés y obesidad
1. Estrés social en adolescentes con exceso de peso
El sobrepeso durante la adolescencia no solo tiene consecuencias a nivel de salud, sino
que también tiene efectos nocivos en el ámbito social y psicológico. Padecer sobrepeso
u obesidad en la niñez y adolescencia tiene unas consecuencias perjudiciales muy
significativas en el desarrollo emocional y en el bienestar general del niño y adolescente
(Strauss y Pollack, 2003). Numerosos estudios han encontrado que los adolescentes con
exceso de peso tienen mayor probabilidad de desarrollar síntomas depresivos y además
poseen menores niveles de autoestima que sus iguales con peso saludable. En este
sentido, los estudios desarrollados por Richardson, Goodman, Hastorf y Dornbusch
(1961) ya en la década de 1960 indicaban que los niños con sobrepeso eran
considerados por los otros niños como los amigos menos deseables.
La amistad es un vehículo esencial para el ajuste psicológico y social de los
adolescentes. Dadas las normas estrictas de apariencia entre los adolescentes en cuanto
a imagen corporal, el sobrepeso puede tener importantes consecuencias sobre el
desarrollo del niño y el bienestar del adolescente. En un estudio de Strauss y Pollack
(2003) se comprobó que los adolescentes con exceso de peso sufrían mayor
marginalización social y estigmatización, y este aislamiento agravaba las consecuencias
sociales y emocionales del sobrepeso en este grupo de edad. Distintos estudios
confirman que los estereotipos negativos hacia el sobrepeso empiezan en la infancia
temprana (Cramer y Steinwert, 1998; Rich y cols., 2008), y la victimización de los
adolescentes basada en su sobrepeso es muy común (Haines, Neumark-Sztainer,
Hannan, van den Berg y Eisenberg, 2008). Es más probable que los adolescentes con
exceso de peso y obesidad se conviertan en objeto de burlas y bullying que sus
compañeros con normopeso (Janssen, Craig, Boyce y Pickett, 2004; Hayden-Wade y
cols., 2005; Pearce, Boergers y Prinstein, 2002). La probabilidad de victimización
44
verbal, social y física entre los adolescentes aumenta con el IMC (Janssen y cols.,
2004), además estudios longitudinales demuestran que el peso corporal predice
significativamente la victimización futura (Griffiths, Wolke, Page, Horwood y Team,
2006), siendo los adolescentes con mayor nivel de obesidad especialmente vulnerables a
la estigmatización y presión social. La literatura sugiere que un tercio de las chicas y un
cuarto de los chicos reportan burlas basadas en el peso por sus compañeros, pero esta
prevalencia aumenta hasta aproximadamente el 60% entre los estudiantes con mayor
nivel de obesidad (Neumark-Sztainer y cols., 2002). En un estudio de Puhl, Luedicke y
Heuer (2011) en el que utilizaron las valoraciones de los estudiantes con peso saludable,
los resultados mostraron que los participantes percibían que el sobrepeso y la obesidad
era la primera razón de sufrir acoso y estigmatización en la escuela.
Las personas con sobrepeso y obesas son altamente estigmatizadas en nuestra sociedad,
y los estereotipos basados en el peso siguen siendo generalizados, incluyendo la
percepción de que las personas obesas son perezosas, desmotivadas, incompetentes,
descuidadas, carentes de autodisciplina y carentes de voluntad (Puhl y Brownell, 2001;
Puhl y Heuer, 2009). Para los jóvenes que presentan sobrepeso u obesidad, la
estigmatización del peso se traduce en victimización generalizada, burlas e
intimidación. Estas experiencias pueden ser explícitas (p. ej. burlas verbales, insultos,
violencia física), o pueden tomar formas más sutiles, como victimización relacional (p.
ej. exclusión social, evitación, ser objeto de rumores).
En resumen, los niños con sobrepeso u obesidad son con frecuencia víctimas de burlas,
acoso, discriminación y otras formas de marginación social. Por lo tanto, los
adolescentes con exceso soportan un estrés social elevado.
45
Hay evidencia de las consecuencias emocionales negativas del estrés social en
adolescentes con exceso de peso. Las burlas basadas en el peso pueden contribuir a
consecuencias emocionales negativas para niños y adolescentes ya que aumenta el
riesgo de depresión, ansiedad, baja autoestima e insatisfacción corporal (Puhl y Heuer,
2009; Eisenberg, Neumark-Sztainer y Story, 2003). La consecuencia emocional más
dramática que ocurre entre los adolescentes que sufren marginalización por su peso es el
aumento del riesgo de comportamiento suicidas (Eaton, Lowry, Brener, Galuska y
Crosby, 2005).
Además de las consecuencias a nivel social en el ámbito escolar, las consecuencias
perjudiciales a nivel académico también son frecuentes. La evidencia indica que los
adolescentes que sufren de continuas burlas y acoso sufren mayor absentismo escolar, lo
que perjudica su rendimiento académico (Puhl y Luedicke, 2012).
2. Influencia del estrés social sobre la conducta alimentaria
Muchos factores externos pueden influir en la ingesta de alimentos, entre los que se
incluyen factores ambientales (p.ej. económicos, disponibilidad de alimentos) (Popkin,
Duffey y Gordon-Larsen, 2005), factores sociales (p.ej. influencia de otros) y la
palatabilidad de los alimentos, entendida como el valor hedónico que otorgamos a la
comida y que depende de las propiedades organolépticas del alimento como, por
ejemplo, su sabor, olor o apariencia (Pliner y Mann, 2004). Además de esto, es una
creencia comúnmente sostenida que el estrés puede alterar los patrones de alimentación
(Wardle y Gibson, 2002).
La salud física, y en concreto, el comportamiento alimenticio, también puede verse
afectado por el estrés social que sufren las personas con sobrepeso y obesidad. Los
mecanismos biológicos directos que vinculan el estrés con la obesidad implican la
46
elevación prolongada del cortisol circulante, un marcador de la activación hipotalámica
del eje pituitario-adrenal, que puede aumentar el apetito y la deposición de grasa
visceral (Bjorntorp, 2001) (ver Figura 1).
Cambios biológicos:
- Elevado cortisol
- Grasa visceral
MAYOR
Mayor exposición al
RIESGO DE
estrés psicosocial OBESIDAD
Cambios comportamentales:
- Aumento de la
ingesta calórica
Figura 1. Vías a través de las cuales el estrés puede contribuir al desarrollo de la obesidad.
En humanos, la literatura muestra que el estrés influencia la conducta alimenticia de
forma bidireccional; posiblemente alrededor del 30% de los individuos disminuye la
ingesta de alimentos y pierde peso durante o después del estrés, mientras que la mayoría
de las personas aumentan su ingesta durante el estrés (Stone y Brownell, 1994; Epel y
cols., 2004). Teniendo en cuenta que las personas que viven en países occidentalizados
viven en un entorno alimenticio apetecible, con una abundancia de alimentos
calóricamente densos, tiene sentido que la mayoría de las personas refieran comer más
durante la situación estresante, en lugar de comer menos. Casi el 50% de una muestra
representativa de EE.UU. afirmó estar preocupada por la cantidad de estrés en sus vidas
al ser conscientes de la relación entre este estrés y su involucración en comportamientos
poco saludables como fumar y comer como forma de aliviarse de esas situaciones
(Stambor, 2006). El deseo -inducido por el estrés- por alimentos altamente calóricos es
alarmante teniendo en cuenta la creciente epidemia de obesidad.
47
Así mismo, se ha observado que las personas con exceso de peso presentan
frecuentemente un patrón de ingesta emocional basado en la tendencia a consumir de
manera impulsiva cuando están bajo un estado emocional negativo (ansiedad, depresión,
estrés, etc.). Como hemos comentado, el estrés agudo puede aumentar la ingesta,
especialmente cuando hay alimentos apetitosos (altos en calorías) disponibles (Oliver y
Wardle, 1999; Bjorntorp, 2001). Por ejemplo, un estudio con autoinformes señaló que el
42% de los estudiantes informaban que incrementaban su ingesta después de percibir
estrés, y el 73% de los participantes informaban incrementar el “picoteo” durante el
estrés (Oliver y Wardle, 1999). En esta misma línea, un estudio de Jääskeläinen y cols.
(2014) encontró que los adolescentes que se dejaban llevar por el estrés a la hora de
comer tenían una mayor prevalencia de obesidad que los que no lo hacían. Otro estudio
señaló que las mujeres que reportaban mayor estrés crónico también reportaban ser
“comedoras emocionales” (Tomiyama, Dallman y Epel, 2011). Hay evidencia
significativa que sugiere efectos potencialmente perjudiciales del estrés en los patrones
de alimentación (p. ej. omitir las comidas, restringir la ingesta, atracones) y las
preferencias alimentarias basadas en alimentos apetecibles altos en calorías (Torres y
Nowson, 2007). Distintas investigaciones muestran que los efectos del estrés pueden ser
diferentes en las personas con peso saludable en comparación con las personas con
obesidad (Block, He, Zaslavsky, Ding y Ayanian, 2009; Lemmens, Rutters, Born y
Westerterp-Plantenga, 2011; Jastreboff y cols., 2011). Se ha observado que la
alimentación debida al estrés se exacerba en las personas con obesidad, mientras que la
ingesta emocional parece tener un efecto inconsistente en individuos con normopeso
(Laitinen, Ek y Sovio, 2002).
Los adolescentes con exceso de peso, los cuales hemos comentado que se encuentran
bajo un estrés social recurrente, podrían utilizar la sobreingesta de alimentos altos en
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grasas y/o azúcares como estrategia de afrontamiento a esa situación. Así, las funciones
cognitivas superiores de control ejecutivo podrían estar alteradas tras estas situaciones
emocionalmente negativas, facilitándose de esta manera, la dificultad para inhibir los
impulsos ante la presencia de alimentos altamente calóricos en el ambiente (Dallman y
colsy cols., 2003; Dallman, Pecoraro y la Fleur, 2005).
Por otro lado, el modelo “Reward Based Stress Eating” (Adam y Epel, 2007) enfatiza el
papel del cortisol y los circuitos de recompensa en la motivación de la ingesta de
alimentos altamente calóricos, y señala el papel de los mediadores neuroendocrinos en
la relación entre el estrés y la alimentación. A nivel fisiológico, existe evidencia que
sostiene que la ghrelina u “hormona del hambre” aumenta en respuesta de estresores
sociales (p.ej. después de la Trier Social Stress Task, que se basa en un discurso
público) (Rouach y cols., 2007) al igual que el cortisol u “hormona del estrés” que está
asociado positivamente con la posterior ingesta de lípidos (Therrien y cols., 2007;
Bjorntorp, 2001).
3. Reactividad psicofisiológica al estrés
Está ampliamente aceptado que el estrés psicológico puede producir reactividad
fisiológica similar a la producida por desafíos de carácter físico. Existen tres sistemas
primarios que están particularmente involucrados en el establecimiento de la respuesta
al estrés, el sistema nervioso autónomo (SNA), el eje hipotálamo-hipófisis-adreno
cortical (HHCA) y el simpático-adrenomedular (SAM). La activación del eje HHCA
causa un aumento en la secreción de cortisol, un glucocorticoide liberado por la corteza
suprarrenal, conocido como “la hormona del estrés” (Sapolsky, Krey y McEwen, 1986;
Al'Absi y Arnett, 2000). La recogida de muestra de cortisol salival ha sido muy
recurrente en investigaciones sobre estrés. Las concentraciones de cortisol salival están
49
estrechamente correlacionadas con la concentración de cortisol sérico o en plasma
(Kirschbaum y Hellhammer, 1994. El cortisol salival es una herramienta de evaluación
más práctica que la recolección de sangre, ya que este método refleja una tendencia a
provocar aumentos espurios en la secreción de cortisol. Muchos informes han
demostrado que diversos tipos de estrés psicológico activan la liberación de cortisol y,
en consecuencia, inducen aumentos significativos en el nivel de cortisol salival
(Kirschbaum y Hellhammer, 1994). La toma de muestras de saliva tiene la ventaja de
que es un método no-invasivo, lo que hace que la recogida de muestras múltiple sea
fácil y libre de estrés. La medida de cortisol ha sido utilizada como medida de la
respuesta al estrés psicosocial en varias investigaciones (Kirschbaum y Hellhammer,
1994).
Por otro lado, además del cortisol, para evaluar la reactividad ante el estrés en una
situación de laboratorio se puede recurrir a otras medidas fisiológicas de la actividad del
SNA. Entre ellas, la frecuencia cardíaca (FC) y la actividad electrodermal (AED) han
sido ampliamente utilizadas, ya que reflejan el grado de reactividad fisiológica que
experimenta el sujeto al afrontar una situación estresante (Kuhmann, Boucsein, Schaefer
y Alexander, 1987; Kohlish y Schaefer, 1996). La intensidad y el patrón de las
respuestas de la FC y la AED ante situaciones de estrés dependen de las características
del estresor, de los recursos psicosociales que posea el sujeto y de los factores
biológicos y constitucionales del individuo, así como de la interacción entre estos
componentes (Steptoe, 1990; Peters y cols., 1998). La FC se considera una variable muy
sensible a los estresores (Freyschus, Hjemdahl, Juhlin-Dannfelt y Linde, 1988), aporta
información de regulación autonómica del corazón, no es invasiva y se puede registrar
de forma continua. La FC se incrementa normalmente en el laboratorio tras la
utilización de diversos estresores como la tarea "Stroop" (Goldberg y cols., 1996),
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hablar en público (Kirschbaum y cols., 1995; Carrillo, Moya-Albiol, González-Bono y
Salvador, 2000; Verdejo-García y cols., 2015), tareas aritméticas (Sloan y cols., 1997),
tareas de tiempo de reacción (Marrero, Al'Absi, Pincomb y Lovallo, 1997). La
reactividad en FC ante un estresor psicológico en una situación de laboratorio puede ser
utilizada como un indicador bastante fiable de la reactividad cardíaca en otras
situaciones semejantes de laboratorio o de la vida real, ya que las variaciones en FC son
los cambios cardiovasculares más estables en el tiempo (Swain y Suls, 1996). La AED
ha sido uno de los índices psicofisiológicos más empleado como correlato de procesos
psicológicos, ya que se ha asociado con la emoción, el arousal y la atención. La AED
depende de la activación de las glándulas sudoríparas y tiene un alto grado de
sensibilidad (Wieland y mefferd, 1970), por lo que los cambios en la AED pueden
entenderse como evidencia de variaciones en el estado cognitivo o emocional del sujeto
(Hugdahl, 1995). Los niveles basales de AED pueden variar notablemente entre
individuos e incluso en el mismo individuo en diferentes situaciones. Sin embargo, al
analizar un mismo sujeto ante una misma situación, la respuesta disminuye con la
habituación a ese estímulo para incrementarse ante la posterior aparición de un estímulo
nuevo y decrecer de nuevo gradualmente a medida que se produce la habituación del
mismo estímulo (Montagu, 1963). En situaciones de laboratorio, se produce un
aumento de la conductancia durante la ejecución de la tarea (Siddle, Lipp y Dall, 1996),
y una disminución al finalizar la misma (Köhler, Scherbaum y Ritz, 1995). Se han
realizado diversos estudios de laboratorio sobre la respuesta electrodérmica ante
estresores de tipo psicológico (Steptoe, Cropley y Joekes, 1999). En varios estudios
realizados por Lazarus (1966), se encontró un aumento de los niveles tónicos de AED
en individuos que veían escenas "estresantes" de largometrajes. Estos resultados se han
encontrado también con varones hipertensos (Köhler y cols., 1995). La AED se ha
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utilizado como indicador de estados de estrés (Clemens y Turpin, 2000) y como índice
clínico en el estudio de diversos trastornos psicofisiológicos asociados con el estrés
(Hugdahl, 1995).
En resumen, la FC y la AED reflejan hasta qué punto un estresor concreto puede
producir un incremento en la activación autonómica. Ambas medidas pueden presentar
un patrón de activación similar o diferente ante un mismo estímulo, por lo que podrían
estar aportando información de diversos aspectos de un mismo proceso como es la
respuesta al estrés (Moya y Salvador, 2001).
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53
Capítulo 4
Cerebro y obesidad
54
55
Capítulo 4. Cerebro y obesidad
1. Singularidades psicobiológicas del neurodesarrollo de la

adolescencia
Durante la adolescencia se producen importantes cambios a nivel físico (crecimiento,
cambios en la masa corporal, maduración sexual), psicológico (intensidad y labilidad
afectiva, aspiraciones románticas e idealistas, sentido de invulnerabilidad, pensamiento
abstracto) y social (distanciamiento de los adultos y niños, primacía de las relaciones
entre compañeros, participación romántica) (Ernst, Pine y Hardin, 2006). Por lo tanto, el
comportamiento en la adolescencia se ve afectado por multitud de factores. Distintos
modelos teóricos han intentado explicar la regulación comportamental en la
adolescencia. El modelo triádico de la neurobiología de la conducta motivada en la
adolescencia de Ernst y cols. (2006), indica que la adolescencia se caracteriza por una
descompensación madurativa entre los sistemas cerebrales encargados de procesar las
recompensas (sistema fronto-estriado), los cuales están totalmente maduros en esta
etapa, y los sistemas prefrontales encargados de la supervisión de la conducta, los cuales
aún permanecen en desarrollo. A esta peculiaridad se añade un sistema de evitación de
daños débil (amígdala), lo cual conlleva al adolescente a una mayor propensión a
involucrarse en conductas de riesgo, como puede ser el consumo de sustancias de abuso.
En resumen, según este modelo existe un aumento de la dominancia de las regiones
motivacionales subcorticales en comparación con las regiones prefrontales. Aplicado a
los problemas de exceso de peso, según este modelo, los adolescentes podrían
sobreestimar las propiedades reforzantes y hedónicas de los alimentos apetecibles (altos
en grasas y/o azúcares) restando importancia al equilibrio homeostático que regula el
apetito. Esta situación conllevaría a la sobre ingesta ignorando las necesidades
fisiológicas de hambre y saciedad y, a su vez, sin tener en cuenta las consecuencias
negativas que este comportamiento podría tener sobre su salud.
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Otros autores, como Chambers, y cols., 2003, se centran en las capacidades de
autorregulación y control inhibitorio del adolescente, argumentando también la falta de
maduración del PFC. La relativa maduración del sistema de recompensa conlleva una
mayor vulnerabilidad a involucrarse en nuevas experiencias relacionadas con la
recompensa. Estas actividades a su vez favorecen la maduración del PFC, pero suponen
una vulnerabilidad hacia comportamientos donde las habilidades de autorregulación y
control de impulsos son necesarias. Debido a esto, los adolescentes podrían ser más
vulnerables a la ingesta de alimentos altos en grasas y/o azúcares debido los déficits
nombrados anteriormente.
Por otro lado, Galvan, Hare, Voss, Glover y Casey (2007), además de señalar la
descompensación entre los sistemas subcorticales y prefrontales, enfatizan el papel de la
toma de riesgos en la adolescencia debido al aumento de la actividad del núcleo
accumbens (NAcc) (Galvan y cols., 2007; Spear, 2000). En relación a la obesidad,
podemos decir que los hábitos alimenticios no saludables podrían ser una conducta de
riesgo hacia la que los adolescentes serían más proclives debido al déficit en el control
de impulsos, su mayor sensibilidad a la recompensa y la mayor propensión hacia la
toma de riesgos.
Por último, desde el modelo del marcador somático de Damasio (2006), se propone que
en las personas que tienden hacia conductas de riesgo como el consumo de sustancias
podría existir una ausencia, alteración o debilitamiento de los marcadores somáticos, lo
que conduciría a tomar decisiones inadecuadas o desventajosas. Este déficit en los
marcadores somáticos afectaría a la capacidad para decidir en función de las potenciales
consecuencias futuras de la conducta, en lugar de en función de las consecuencias
inmediatas. El modelo del marcador somático podría explicar la “miopía hacia el
futuro” que presentan las personas con antecedentes de abuso de sustancias manifestada
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en la alteración de la toma de decisiones. Este modelo propone también una alteración
en el sistema fronto-estriado. Si aplicamos este modelo a la adolescencia, y tenemos en
cuenta lo comentado anteriormente, podría explicar por qué los adolescentes con exceso
de peso no son capaces de tener en cuenta las consecuencias perjudiciales que sus
hábitos alimenticios tienen sobre su salud (debido a un déficit en sus marcadores
somáticos), lo que les lleva a seguir teniendo una toma de decisiones alterada y
vinculada al consumo de alimentos no saludables.
En resumen, estos modelos tienen varios aspectos en común ya que proponen que los
adolescentes tienen mayor sensibilidad a la recompensa, mayor tendencia a
comportamientos impulsivos/compulsivos y un pobre funcionamiento ejecutivo, y todo
esto conlleva una mayor vulnerabilidad hacia conductas o comportamientos de riesgo,
como puede ser una excesiva ingesta de alimentos.
2. Sistemas cerebrales asociados al comportamiento alimenticio
El hipotálamo ha sido considerado tradicionalmente como el centro cerebral regulador
de la ingesta o el apetito (Kimet y cols., 2006). Sin embargo, a nivel cerebral, no solo el
hipotálamo es responsable del balance energético (Rolls, 2008). Las hormonas
implicadas en la modulación de la actividad del hipotálamo (p.e., leptina, ghrelina o
insulina), también modulan la actividad neuronal en regiones cerebrales cortico-
límbicas, las cuales están implicadas en la motivación, procesamiento de recompensas y
aprendizaje de hábitos, procesos muy relacionados con el comportamiento alimenticio
(Farooqi y cols., 2007).
Por otro lado, el sistema de recompensa cerebral es un componente central para
desarrollar y monitorear comportamientos motivados. Por lo tanto, el conocimiento de
su funcionamiento es vital para comprender mejor el problema de la obesidad. La
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percepción de la recompensa de los alimentos comienza con la información generada
por las células receptoras del gusto oral que posteriormente se transmite al núcleo del
tracto solitario (NTS) por fibras sensitivas aferentes. Desde el NTS, la información del
gusto se transmite a múltiples áreas del cerebro posterior (p.ej., el núcleo parabraquial),
el mesencéfalo (zona tegmental ventral o VTA) y el prosencéfalo (p.ej., NAcc, el
estriado, el tálamo y la corteza cerebral) (Kelley, Baldo, Pratt y Will, 2005), que
colectivamente perciben y discriminan entre diferentes gustos y texturas, asignándole un
determinado valor reforzante. El procesamiento más alto de la información del gusto se
realiza en la ínsula (córtex gustativo primario), mientras que el OFC integraría la
información del gusto con características olfativas, visuales y cognitivas (córtex
gustativo secundario) (Rolls, 2005). La respuesta de esta última área a los estímulos del
gusto disminuye a medida que los alimentos son ingeridos, lo que implica la capacidad
de integrar información gustativa y estados de saciedad. De acuerdo con esta hipótesis,
la disminución de la activación del córtex gustativo secundario disminuye el valor de
recompensa de los alimentos y, por lo tanto, contribuye al cese de la alimentación
mediante proyecciones al estriado y la amígdala (Kringelbach, O’Doherty, Rolls y
Adrews, 2003).
La valoración de la recompensa también implica la liberación de dopamina (DA) en las
neuronas del VTA. Éstas, a su vez, se proyectan al NAcc, estriado y otras áreas
cerebrales. La DA que actúa en estas áreas del prosencéfalo aumenta potencialmente el
impulso para obtener un estímulo gratificante (es decir, aumenta el "deseo" de un
alimento o fármaco en particular) (Kelley y cols., 2005; Kelley y Berridge, 2002).
En resumen, existe evidencia de que el procesamiento cerebral de las recompensas
depende de una red cerebral compuesta por diversas regiones, incluyendo el estriado, el
PFC, el cíngulo anterior, la ínsula o las áreas dopaminérgicas del mesencéfalo (Haber y
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Knutson, 2009). Como hemos comentado, existe cierta especialización dentro de este
sistema, por ejemplo, el estriado ventral está más enfocado a la valoración subjetiva que
se le otorga a reforzadores relevantes como la comida o el dinero (Passamonti y cols.,
2009), mientras que la ínsula anterior parece estar más relacionada con la integración de
información interoceptiva (Craig, 2009).
En nuestras sociedades occidentales actuales, en las que, como hemos mencionado,
existe total disponibilidad de comida y están repletas de señales de alimentos altos en
grasas y/o azúcares, el individuo tiene que ser capaz de controlar la cantidad de
alimento que ingiere. Así, el comportamiento alimenticio ha dejado de ser una cuestión
relacionada con la supervivencia tornándose en una actividad que adquiere un valor
hedónico y reforzante. Los sistemas implicados en el procesamiento de las recompensas
y la toma de decisiones juegan un papel muy importante, incluso a veces obviando los
sistemas de regulación metabólica. Es decir, el individuo no solo regula su
comportamiento alimenticio en función de sus estados de hambre o saciedad, sino
también en función de otras propiedades reforzantes presentes en la comida, como
apariencia, sabor, textura, olor, etc. (Zheng y Berthoud, 2007). Por lo tanto, ante la
visualización de alimentos altamente apetecibles o de gran aporte energético, las áreas
del circuito de la recompensa pueden promover una mayor liberación de DA debido a la
gran saliencia que tiene el estímulo y conllevar así a una mayor predisposición a la
sobreingesta (Stice, Figlewicz, Gosnell, Levine y Pratt, 2013).
Numerosos estudios también han relacionado la ingesta excesiva y la obesidad con la
descompensación entre los sistemas cerebrales encargados de otorgar el valor reforzante
a la comida y los sistemas encargados del control ejecutivo. Como hemos dicho, las
personas con obesidad asociarían la comida y en concreto los alimentos hipercalóricos a
un valor subjetivo mayor. A su vez se produciría una disminución de la eficacia de los
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sistemas prefrontales ejecutivos, lo que daría lugar a la impulsividad e incapacidad para
inhibir su comportamiento y finalmente conllevaría comportamientos relacionados con
la alimentación excesiva (Volkow y cols., 2008; Rolls, 2011).
En la adolescencia, la descompensación entre estos dos sistemas está más acentuada
como mencionamos con el modelo triádico de la neurobiología de la conducta motivada
en la adolescencia de Ernst y cols., 2006. Además, diferentes estudios han expuesto que
los adolescentes con exceso de peso presentan mayor impulsividad y sensibilidad a la
recompensa (Van den Bert y cols., 2011).
3. La “adicción” a la comida
Recientemente, se ha postulado un modelo teórico de adicción a la comida (“food
addiction model”) basándose en las similitudes existentes entre las alteraciones
cerebrales que presentan las personas con trastornos adictivos a sustancias y las
personas que tienen obesidad (Volkow y cols., 2013). Las drogas de abuso utilizan los
mismos mecanismos neurales que modulan la motivación para consumir alimentos, por
lo tanto, existe una superposición entre los circuitos cerebrales implicados en la pérdida
de control y la ingesta excesiva de alimentos que caracteriza la obesidad y el consumo
compulsivo de drogas propio de la adicción. La alteración de los circuitos cerebrales de
DA es central en estas dos patologías.
Las neuronas dopaminérgicas residen en los núcleos del cerebro medio (VTA, y
sustancia negra) que se proyectan al estriado (NAcc y el estriado dorsal), regiones
límbicas (amígdala e hipocampo) y regiones corticales (PFC, giro cingulado y córtex
temporal) y modulan la motivación y el esfuerzo necesario para lograr los
comportamientos de supervivencia. Para lograr sus funciones, las neuronas DA reciben
proyecciones de regiones cerebrales involucradas con respuestas autonómicas (es decir,
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hipotálamo, tronco cerebral), memoria (hipocampo), reactividad emocional (amígdala),
excitación (tálamo) y control cognitivo (PFC y córtex cingulado) a través de una vasta
matriz de neurotransmisores y péptidos. Por lo tanto, los neurotransmisores implicados
en los comportamientos de búsqueda de drogas también están implicados en la ingesta
de alimentos, y, por otro lado, los péptidos que regulan la ingesta de alimentos también
influyen en los efectos reforzantes de las drogas. Sin embargo, y a diferencia de las
drogas de abuso cuyas acciones están desencadenas por sus efectos farmacológicos
directos en las vías DA de recompensa cerebral (NAcc y núcleo pálido ventral), la
regulación de los comportamientos alimenticios está modulada por múltiples
mecanismos periféricos y centrales que directa o indirectamente transmiten información
a las vías dopaminérgicas, dónde el hipotálamo juega un papel primordial.
Ambos problemas pueden ser definidos como desordenes en los cuáles la saliencia de
un tipo específico de recompensa (comida o droga) se valora exageradamente a
expensas de otros tipos de reforzadores incrementando repentinamente la DA en los
centros cerebrales de recompensa. En individuos vulnerables, estos incrementos de DA
pueden invalidar a los mecanismos de control homeostático. Estudios de imagen
cerebral han empezado a delinear algunos de los circuitos cerebrales superpuestos cuyas
disfunciones pueden ser la base de los déficits observados. Los resultados sugieren que
tanto los individuos obesos como los adictos a sustancias de abuso sufren alteraciones
en las vías dopaminérgicas que regulan los sistemas neuronales asociados no solo con la
sensibilidad de la recompensa y la motivación de los incentivos, sino también con el
condicionamiento, el autocontrol, la reactividad del estrés y la conciencia interoceptiva
(Volkow y cols., 2013) (ver figura 2).
El modelo de adicción a la comida ha sido ampliamente estudiado en los últimos años.
Sin embargo, existen corrientes contrarias que han relacionado estos paralelismos entre
62
adicción y obesidad con patrones específicos de sobreingesta como el trastorno por
atracón o “binge eating”, más que con el concepto de obesidad en sí (Ziauddeen y
Fletcher, 2013). Esta condición se clasifica como un trastorno alimentario en el DSM-V
y se caracteriza por episodios recurrentes ("atracones") de consumo incontrolado de
gran cantidad de alimentos que se realiza de forma muy rápida, normalmente estando la
persona sola e incluso en ausencia de hambre. Esta alimentación persiste a pesar de la
incomodidad física y los atracones se asocian con marcada angustia y sentimientos de
culpa y disgusto. Los atracones pueden desencadenarse por estados de ánimo negativos
que no necesariamente mejoran por el atracón (Stein y cols., 2007). Una advertencia
importante es que, aunque el trastorno por atracón o “binge eating disorder (BED)” se
asocia con la obesidad, un número considerable de personas que muestran un
comportamiento de atracones no presentan obesidad y la mayoría de las personas obesas
no tienen este trastorno (Striegel-Moore y cols., 2001). Esta observación enfatiza la
importancia de evitar el uso simple del IMC como un marcador general para el consumo
compulsivo excesivo y comportamientos adictivos. También, recientemente ha
aparecido un modelo alternativo postulando un cambio en la denominación, cambiando
el concepto “food addiction” a “eating addiction”, el cual sugiere más bien una adicción
comportamental al acto de comer, y no tanto al alimento en sí (Hebebrand y cols.,
2014). Las personas que comen en exceso generalmente no restringen sus dietas a
nutrientes específicos; en cambio, la disponibilidad de una gama más amplia de
alimentos apetecibles (altos en grasas y/o azúcares) parece hacer que los sujetos
propensos sean vulnerables a comer en exceso. Sin lugar a dudas, la industria
alimentaria tiene que actuar de manera responsable, dado que el acceso fácil a alimentos
altamente apetecibles y con alto contenido calórico promueve la ingesta excesiva y
potencialmente el desarrollo de una "adicción a comer" (“eating addiction”) en personas
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predispuestas. Además, los autores que apoyan este cambio de concepto postulan que el
término “eating addiction” es más apropiado para evitar la connotación infundada de
que la comida puede contener sustancias químicas que pueden conducir al desarrollo de
un trastorno por consumo de sustancias, ya que el concepto de “adicción a comer” se
asociaría más a una adicción comportamental (Hebebrand y cols., 2014).
Figura 2. Mecanismos de acción de las drogas de abuso y la comida sobre las vías de
recompensa cerebrales.
En contraste con las drogas de abuso cuyas acciones son desencadenadas por sus directos
efectos farmacológicos en el sistema cerebral de recompensa mediado por la dopamina (área
tegmental ventral, núcleo accumbens y pálido ventral), la regulación del comportamiento
alimenticio y, por tanto, las respuestas a la comida están moduladas por múltiples mecanismos
centrales y periféricos que directamente o indirectamente transmiten a las vías de recompensa
cerebrales, incluidos aquellos envueltos en el placer, aversión, habituación y control cognitivo.
PYY: peptide YY; s. intestines: small intestines; SN: substantia nigra (Adaptado de Volkow y
cols., 2013b).
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4. Estudios de activación cerebral relacionados con la motivación por la

comida
En los últimos años ha aumentado exponencialmente el número de estudios que,
utilizando fMRI, han analizado el funcionamiento cerebral de personas con obesidad,
utilizando para ello distintos tipos de tareas. Los estudios de actividad cerebral se basan
en mediciones de la señal BOLD (bloodoxygen- level-dependent) obtenida durante
adquisiciones de fMRI (Ogawa y cols., 1993). De forma resumida, esta técnica se basa
en que la actividad neuronal provoca cambios en la ratio oxihemoglobina
/desoxihemoglobina, que son captados por un escáner de resonancia magnética, y
transformados en imágenes. Los estudios de fMRI permiten obtener mapas de
activación cerebral que reflejan las áreas implicadas en determinados procesos
cerebrales. Para ello la persona evaluada simplemente debe realizar una determinada
tarea dentro del escáner.
Un gran número de estudios han permitido estudiar la estructura y el funcionamiento
cerebral de personas con exceso de peso. Como hemos comentado, determinados
mecanismos neuronales tienen un papel crucial en los comportamientos alimenticios a
través de la regulación de la motivación por la comida y el control del comportamiento
(DelParigi, Pannacciulli y Tataranni, 2005). El análisis del procesamiento cerebral de
estímulos alimenticios ha sido el paradigma más utilizado dentro de los estudios de
neuroimagen con fMRI. Estos estudios en participantes sanos han mostrado que la
comida es un potente reforzador cerebral y tanto su simple observación en imágenes,
como su consumo, activan áreas del sistema de recompensa cerebral (O’Doherty,
Deichmann, Critchley y Dolan, 2002; Kringelbach, y cols., 2003).
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En cuanto a los resultados en obesidad, los estudios de fMRI indican que los individuos
con obesidad muestran una mayor activación en la ínsula, el opérculo frontal, el OFC, la
amígdala y el cuerpo estriado en respuesta a imágenes de alimentos apetecibles
(Rothemund y cols., 2007; Stoeckel y cols., 2008) y a la recepción anticipada de estos
(Stice, Spoor, Bohon, Veldhuizen y Small, 2008). Los datos sugieren que la ínsula y el
opérculo frontal están involucrados en el deseo o “craving” a estos alimentos y a su
recompensa anticipada, y además que el OFC, la amígdala y el cuerpo estriado
codifican su valor de recompensa (Gottfried, O'Doherty y Dolan, 2003; Small,
Veldhuizen, Felsted, Mak y McGlone, 2008).
En cuanto a los adolescentes, hay un menor número de estudios al respecto. Un estudio
de Bruce y cols. (2010) encontró que el grupo de adolescentes con obesidad mostraba
significativamente mayor activación que los adolescentes con un peso saludable ante las
imágenes de comida en PFC (antes de comer) y en la OFC (después de comer).
Además, el grupo con obesidad mostró menos reducción de la activación después de la
comida en el PFC, y regiones límbicas y de procesamiento de la recompensa,
incluyendo el NAcc. Asimismo, se ha observado el incremento de la activación en el
córtex dorsolateral (dlPFC) en adolescentes con obesidad debido al aumento del control
inhibitorio durante la visualización de alimentos (Davids y cols., 2010). Sin embargo,
en un estudio de Batterink, Yokum y Stice (2010) donde se utilizaba una tarea
específica go/no go de comida, los resultados mostraron que las adolescentes con
sobrepeso mostraban mayor impulsividad en la tarea y menor activación de las regiones
frontales inhibitorias. Esta variedad de resultados puede deberse a la diferencia en el
paradigma utilizado.
En otro estudio con fMRI (Stice y cols., 2008), en el que se utilizaba un alimento
apetitoso (batido de chocolate) y una solución insípida, las adolescentes con obesidad
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mostraron una mayor activación bilateral que las adolescentes con peso normal en la
corteza gustativa (ínsula anterior y media, opérculo frontal) y en las regiones
somatosensoriales (opérculo parietal y opérculo rolandiano) en respuesta a la
anticipación de la ingesta de batido de chocolate (frente a la solución insípida) y al
consumo real de batido (frente a una solución insípida); estas regiones cerebrales
codifican los aspectos sensoriales y hedónicos de los alimentos. Por otro lado, en un
estudio de Yokum, Ng y Stice (2011) con chicas adolescentes, se observó que el IMC
correlacionaba significativamente con la activación en regiones cerebrales relacionadas
con la atención y la recompensa alimenticia, incluida la ínsula anterior, opérculo frontal,
OFC, la corteza prefrontal ventrolateral (vlPFC) y el lóbulo parietal superior, durante la
orientación inicial a señales de alimentos apetitosos. El incremento de activación en
OFC durante la orientación inicial a alimentos apetitosos predijo futuros aumentos en el
IMC. Los resultados indicaron que el sobrepeso estaba asociado a un mayor sesgo
atencional a las señales de alimentos y que los adolescentes que mostraban mayor
reactividad en los circuitos de recompensan durante la exposición a alimentos apetitosos
tenían un mayor riesgo de aumento de peso.
En general, los resultados de los estudios de neuroimagen realizados hasta ahora señalan
una respuesta incrementada en áreas del circuito de la recompensa, tanto en adultos
como en adolescentes con exceso de peso, al procesar imágenes de comida,
especialmente aquellas con un alto contenido en grasas y azúcares.
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II. JUSTIFICACIÓN,
OBJETIVOS E
HIPÓTESIS
68
69
Capítulo 5
Justificación, objetivos e hipótesis de la tesis
70
71
Capítulo 5. Justificación, objetivos e hipótesis de la tesis
1. Justificación y objetivo principal
Los cambios producidos en la sociedad actual en los últimos años han modificado la
forma en la que percibimos e interpretamos el valor hedónico de los alimentos.
Actualmente, nuestro ambiente, repleto de señales de alimentos altos en calorías y/o
azúcares, hace necesario el fortalecimiento de los sistemas de control del
comportamiento para poder resistir la tentación y evitar la sobreingesta. Como hemos
dicho, no solo los mecanismos regulatorios homeostáticos son los responsables de
nuestro comportamiento alimenticio, sino que otros muchos factores están influyendo
en nuestra toma de decisiones a la hora de comer. Estas variables pueden ser la mayor
palatabilidad de la comida, la extensa variedad de alimentos, alimentos baratos de fácil
y rápido acceso, la continua presencia de señales alimentarias, la mayor densidad de
energía en los alimentos, el mayor tamaño de las porciones, etc.
El aumento de la prevalencia del sobrepeso y la obesidad en edades cada vez más
tempranas como es la niñez y la adolescencia, hace necesario investigar los mecanismos
específicos que están actuando en esta población. El sobrepeso en la adolescencia está
asociado con un mayor número de problemas y mayor severidad de estos en la edad
adulta (Whitaker, Wright, Pepe, Seidel y Dietz, 1997). Aparte de las perjudiciales
consecuencias del exceso de peso a nivel médico (p.ej., aumento de la diabetes tipo II en
niños y adolescentes), los adolescentes con exceso de peso están expuesto a un mayor
nivel de estrés social (p.ej., burlas, discriminación, bullying, etc.). Dado los efectos que
produce el estrés crónico sobre las habilidades y recursos personales, es necesario
indagar sobre las consecuencias del estrés social en adolescentes con exceso de peso.
Además, las alteraciones neurocognitivas y emocionales que parecen estar relacionadas
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con la obesidad podrían estar acentuadas en esta etapa debido a las peculiaridades en el
neurodesarrollo que acontecen en la misma (Ernst y cols., 2006).
En este contexto es donde se encuadra la realización de esta tesis doctoral.
El objetivo principal de esta tesis es estudiar los mecanismos neuropsicológicos y
cerebrales asociados al exceso de peso en adolescentes.
2. Objetivos específicos
De nuestro objetivo general se derivan tres objetivos específicos:
I. Primer objetivo: caracterizar y comparar la influencia del estrés social sobre el
rendimiento neuropsicológico en adolescentes con exceso de peso y
adolescentes con normopeso.
Este objetivo fue dividido en dos objetivos específicos:
1. Objetivos específico 1: caracterizar y comparar la influencia del estrés
social sobre las funciones cognitivas de atención y toma de decisiones y
sobre la respuesta de cortisol salival en adolescentes con exceso de peso
y adolescentes con normopeso.
2. Objetivo específico 2: caracterizar y comparar la influencia del estrés
social y el papel de la evaluación social negativa sobre tareas de función
ejecutiva y medidas de reactividad psicofisiológica en adolescentes con
exceso de peso y adolescentes con normopeso.
II. Segundo objetivo: evaluar y comparar la influencia de la visualización de
estímulos alimenticios en una tarea de elección sobre el comportamiento en una
tarea de toma de riesgos, y su relación con variables de impulsividad y niveles
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de hambre subjetiva, en adolescentes con exceso de peso y adolescentes con
normopeso.
III. Tercer objetivo: comparar los patrones de activación cerebral de un grupo de
adolescentes con exceso de peso y un grupo de adolescentes con normopeso ante
la visualización de una tarea de elección alimenticia, analizando la relación de
esta activación con el craving provocado por los alimentos de la tarea.
Nuestro primer objetivo fue estudiar la influencia del estrés social sobre el rendimiento
neuropsicológico en adolescentes con exceso de peso, ya que como hemos visto
anteriormente, el estrés social es mucho más frecuente en esta población y además hay
varias investigaciones que exponen la existencia de un menor rendimiento
neuropsicológico en personas con obesidad. Por lo tanto, derivado de los resultados que
abordan los perjudiciales efectos del estrés en la cognición, queríamos observar si la
exposición al estrés social propiciaba una ejecución más pobre en adolescentes con
exceso de peso en tareas que evaluaban distintas funciones cognitivas. Para ello
realizamos dos estudios. En el primer estudio nos centramos en las funciones de
atención y toma de decisiones y utilizamos la medida de cortisol salival como medida
objetiva del estrés. Este estudio ha sido publicado en la revista Plos One (Verdejo-
Garcia, A., Moreno-Padilla, M., Garcia-Rios, M. C., Lopez-Torrecillas, F., Delgado-
Rico, E., Schmidt-Rio-Valle, J., & Fernandez-Serrano, M. J., 2015) y se encuentra
íntegramente en el Capítulo 6 de esta tesis. En el segundo estudio evaluamos el resto de
funciones ejecutivas (memoria de trabajo, inhibición y flexibilidad) y utilizamos la
reactividad psicofisiológica (tasa cardíaca y respuesta electrodermal) como medida
objetiva del estrés. Además, también analizamos el efecto específico de la evaluación
social negativa, ya que los adolescentes con exceso de peso están expuestos con mayor
frecuencia a las evaluaciones sociales despectivas (normalmente por parte de sus
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iguales). Este estudio ha sido publicado en la revista Annals of Behavioral Medicine
(Moreno-Padilla, M., Fernández-Serrano, M. J., Verdejo-García, A., & Reyes del Paso,
G. A, 2018) y se encuentra íntegramente en el Capítulo 7 de esta tesis.
Respecto al objetivo 2, nuestro planteamiento estuvo basado en los resultados de
distintos estudios que han mostrado que la visualización de señales relacionadas con el
consumo de drogas produce un incremento en los niveles de impulsividad e induce a
una mayor toma de riesgos en individuos adictos a sustancias, incrementando como
consecuencia el riesgo de consumo. En este contexto realizamos un tercer estudio en el
que, dadas las similitudes encontradas entre los sistemas que regulan la adicción a
sustancias y la obesidad, investigamos la influencia de la visualización de imágenes de
comida sobre la toma de decisiones en adolescentes con exceso de peso. Este estudio
está bajo revisión en la revista Plos One y se encuentra íntegramente en el Capítulo 8 de
esta tesis.
En cuanto al objetivo 3, queríamos estudiar las diferencias en activación cerebral entre
los dos grupos ante una tarea de elección alimenticia y comprobar, si como aparece en
los individuos adictos a sustancias, esta activación está relacionada con el craving por
alimentos con alta saliencia (algos en grasas y/o azúcares). Para abordar este último
objetivo realizamos nuestro cuarto estudio que está bajo revisión en la revista Appetite y
se encuentra íntegramente en el Capítulo 9 de esta tesis.
3. Hipótesis
Las principales hipótesis que se derivan de estos objetivos son:
I. Los adolescentes con exceso de peso serán más sensibles a la influencia del
estrés social y presentarán peor rendimiento en las tareas de atención y toma de
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decisiones después de la situación estresante, asociándose este déficit en el
rendimiento con el mayor aumento de cortisol salival en adolescentes con
exceso de peso.
II. Los adolescentes con exceso de peso serán más sensibles a la influencia del
estrés social, y en concreto a la evaluación social negativa por parte de la
audiencia, y presentarán peor rendimiento en las tareas de función ejecutiva
después del estresor social, asociándose este déficit en el rendimiento con la
mayor reactividad psicofisiológica en adolescentes con exceso de peso.
III. Los adolescentes con exceso de peso mostrarán una mayor toma de decisiones
arriesgadas tras la exposición a una tarea de elección alimenticia, así como
mayores niveles de hambre, más elecciones de alimentos apetecibles y mayores
puntuaciones en impulsividad.
IV. Durante el procesamiento de elecciones alimenticias, los adolescentes con
exceso de peso evidenciarán mayor activación cerebral en comparación con los
adolescentes con normopeso. A su vez, esta activación estará asociado con el
craving que los participantes presenten por los diferentes alimentos.
(Ver figura 3).
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EP: exceso de peso; NP: normopeso
77
III. MEMORIA DE
TRABAJOS
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79
Capítulo 6. Social stress increases cortisol and hampers
attention in adolescents with excess weight
Verdejo-Garcia, A., Moreno-Padilla, M., Garcia-Rios, M. C., Lopez-Torrecillas, F.,

Delgado-Rico, E., Schmidt-Rio-Valle, J., & Fernandez-Serrano, M. J. (2015). Social
stress increases cortisol and hampers attention in adolescents with excess weight. PloS
one, 10(4), e0123565.
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81
Capítulo 6. Social stress increases cortisol and hampers attention in adolescents with excess weight
1. Introduction
Adolescents with excess weight suffer substantial social stress including frequent peer
bullying and social marginalization and exclusion [1,2]. Crucially, the degree of
exposure to these social stressors is the most important predictor of poor psychological
adjustment and poor academic achievement in adolescents with obesity [3]. Moreover,
neuroendocrine studies have shown that non-fasting levels of the “hunger hormone”
ghrelin increase in response to social stressors (i.e., the Trier Social Stress Task,
involving a public speak) [4] and that the awakening response of the “stress hormone”
cortisol positively associates with subsequent lipid intake [5]. Therefore, social stress is
a potent determinant of poor cognition and poor food choices in adolescents with excess
weight. This phenomenon could be explained by the harmful impact of social stress on
cognitive skills such as attention, cognitive control and decision-making, which
contribute to obesity-related behaviours in adolescents [6]. The harmful impact of
persistent social stressors on cognition in adolescents with obesity is likely to be
enduring as stress induces neuroadaptations in prefrontal and limbic regions particularly
during adolescence [7,8]. Therefore, examining whether social stress hampers cognition
in adolescents with excess weight is essential for prevention of cognitive decline and
hence progression of obesity. However, to date no studies have experimentally assessed
this notion. In this study we examined if a social stressorthe Trier public speaking stress
task- specifically increases cortisol levels and hampers cognitive performance in
adolescents with excess weight compared to adolescents with normal weight. We
specifically assessed the impact of social stress on outcome measures of attention,
cognitive inhibition and decision-making. We selected these outcomes because they
reflect the function of frontal-limbic systems [9,10] and are longitudinally associate
with weight gain in pediatric populations [11,12]. We hypothesized that adolescents
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with excess weight would show greater cortisol response to the social stressor, and
greater detrimental impact of social stress on attention and decision making
performance.
2. Methods
Participants
Eighty-four adolescents aged between 12 and 18 years old participated in the study.
They were classified in two groups (Normal weight [n = 42] and Excess weight [n =
42]) based on their age adjusted Body Mass Index (BMI) percentile [13]. Sample size
was estimated through power analysis. The existing evidence about the impact of the
Trier Social Stress Task (TSST) on selected outcome variables was correlational (i.e.,
the association between TSST-induced cortisol changes and decision-making
performance is between 0.3 and 0.4) [14,15]. Therefore, we estimated that in order to
achieve adequate power (80%) to detect a ρH1 = 0.3 association between the
independent variable (stress) and the cognitive outcomes (attention and decision-
making) 84 participants would be required. This sample size was deemed acceptable for
the mixed repeated-measures design. The classification of the two groups was
conducted in alignment with the guidelines of the International Obesity Task Force and
the Centers for Disease Control and Prevention: Normal weight participants had age
adjusted BMI percentiles in the range between the 5th and the 84th percentile, and
Excess weight participants had age adjusted BMI percentiles 85 (Table 1). Three
participants from the Excess weight group provided invalid cortisol samples, and
therefore the final study sample comprised 42 Normal weight and 39 Excess weight
participants. Participants’ socio-demographic characteristics, BMIs, percentage fat and
blood count obtained biochemical parameters are as well displayed in Table 1.
Participants also completed The Dutch Eating Behavior Questionnaire [16] which was
83
used to characterise psychological traits relevant to maladaptive eating behaviours (i.e.,
external eating, emotional eating and restraint) (Table 1). Participants were recruited
from the paediatrics and endocrinology services of the Hospital “Virgen de las Nieves”
in Granada (Spain), and from schools located in the same geographical area. The
inclusion criteria for participants were defined as follows: (i) age range between 12 and
18 years old; (ii) BMI percentiles falling within the intervals categorized as overweight
or obesity (85—Excess weight group), or normal weight (5–85—Normal weight group);
and (iii) absence of history or current evidence of neurological or psychiatric disorders,
assessed by participants and parent’s interviews and the Eating Disorder Inventory [17].
All participants had normal or corrected-to-normal vision.
Experimental procedures
Fig 1 displays a schematic representation of the experiment. In order to induce social
stress in the laboratory we utilised a previously validated Virtual Reality version of the
Trier Social Stress Task (TSST) [18]. Participants had to perform a stressing task which
consisted of delivering a speech about personal characteristics including both positive
and negative aspects of themselves in front of a simulated audience. Participants were
84
told that this audience would at- tend the speech and subsequently evaluate its quality.
However, the virtual audience was programmed to look progressively bored and
disappointed with the speech. The speech was followed by a mental calculation test
(serially subtracting 17, starting from 2013). Cortisol levels were measured via saliva
samples collected before onset of the TSST (T1), after completion of the TSST and the
calculation test (10 minutes after TSST onset—T2) and after performance on each of
the attention and decision making cognitive probes (20 and 30 minutes after TSST
onset-T3 and T4- respectively). Cognitive measures were conducted in a fixed order
before TSST onset (pre-TSST, overlapping with T1) and after completion of the TSST
and the calculation test (post-TSST, overlapping with T2). To minimize practice effects,
we utilised parallel versions of all tasks in the post-TSST administration. The original
validation study showed that this virtual reality TSST is able to induce modest but
sizeable increases in cortisol and subjective stress responses [18]. Moreover the virtual
audience tamed the ethical concerns associated with the negative impact of the social
stressor on adolescents’ participants. The Ethics Committee for Human Research of the
Universidad de Granada approved the study. Both participants and parents signed
informed consent.
Fig 1. Schematic representation of the experiment.
Cortisol measurement. Participants were told not to smoke, eat or drink coffee for at
least 30 minutes before the experiment. All the experimental sessions were conducted at
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the same time of the day (4–5 pm) based on pilot data obtained in this cohort prior to
study onset indicating that diurnal cortisol levels were stable during these hours. Saliva
was collected via a commercially available device: Salivette Cortisol (Sarstedt,
Numbrecht, Germany). This device is composed of a cotton tube (similar to dental
cotton), and two plastic tubes that fit one inside the other. Subjects were told to place
cotton salivettes inside their mouth and gently chew and/ or suck on them for 1–3 min
until they became soaked in saliva. The cotton tube was inserted inside the plastic tube,
which was then capped. Saliva samples were stored at -20°C until required for assay.
Samples were analyzed at the University Hospital, using the electrochemiluminescence
immunoassay “ECLIA” method. This method is designed for use in Roche Elecsys
1010/2010 automated analyzers and in the Elecsys MODULAR NALYTICS E170
module. We computed two different metrics from each cortisol sample
(microgram/deciliter and nanomol/liter). The correlation between both metrics at the
different time points ranged from 0.8 and 0.9.
Cognitive measures. We utilized three computerized tests: two subtests from the Cam-
bridge Neuropsychological Test Automated Battery (CANTAB) [19], Motor Screening
(MOT) and Rapid Visual Information Processing (RVP), and the Iowa Gambling Task
(IGT) [20]. Al- ternate versions of each test were used in pre-stress and post-stress
administrations.
MOT. The main objective of this test is to provide a baseline measure of the
subjects’ basic motor skills in terms of reaction times and accuracy. After a
demonstration of the correct way to point on the computer screen using the forefinger of
the dominant hand, the subjects must point to a series of stimuli (crosses) popping up in
turn. The outcome measure of this test was response latency.
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RVP. This is a test of visual sustained attention with an impulse control
component. A white box is displayed in the centre of the computer screen, inside which
digits, from 2 to 9, are displayed in a pseudo-random order, at the rate of 100 digits per
minute. The subject must detect consecutive odd or even sequences of digits (for
example, 2-4-6) and respond by pressing the touch pad. The outcome measures of this
test were response latency and response discriminability (B’) scores, which are sensitive
to attention and impulse control domains respectively. The B’ score is the signal
detection measure of the strength of trace required to elicit a response (range -1.00 to
+1.00). Thus, it is the tendency to respond regardless of whether the target sequence is
present and uses the p(hit) and p(fa) results. A score close to +1.00 indicates that the
subject gave few false alarms.
IGT. This is a computer task measuring reward/punishment based decision-
making. It involves four decks of cards (A, B, C and D). Each time a participant selects
a card, a specified amount of play money is awarded. However, interspersed among
these rewards, there are probabilistic punishments (monetary losses). Two of the decks
of cards (A and B) produce high immediate gains; however, in the long run, they will
take more money than they give, and are thus considered disadvantageous. The other
two decks (C and D) are considered advantageous, as they result in small, immediate
gains, but will yield more money than they take in the long run. The performance
measure was the net score calculated by subtracting the number of disadvantageous
choices (decks A and B) from the number of advantageous choices (decks C and D). An
equivalent parallel version of the ABCD task in which decks are labelled K, L, M and N
was utilised in the post-TSST administration. These versions have shown adequate test-
retest reliability and ecological validity in relation to decision-making [21].
87
Visual Analogue Scales (VAS). We used two Visual Analogue Scales (VAS) designed
to rate arousal and stress. For arousal scale the individual must indicate the extent to
which they perceived as active and alert (from nothing active to very active). For stress
scale they must indicate how much stress they feel (from no stress to very much stress).
We used the mean scores of each dimension.
Statistical analyses
The main hypotheses were examined utilizing mixed repeated measures analyses of
variance including Time as the repeated-measures factor, Group as the between-groups
factor, and cortisol levels (as measured in μg/dl) and RVP’s mean response latency and
B’ scores and IGT’s net scores as dependent measures. Cortisol and RVP performance
measures were log-transformed (base 10) to meet the normal distribution, but for the
sake of clarity the Figures report non-transformed measures. IGT scores fitted to the
normal distribution as assessed by Kolgomorov-Smirnov tests. We also performed
correlation analyses between change scores of cortisol levels (T2—T1) and change
scores of cognitive performance (T2—T1) and between both change scores and
biological and psychological measures. These change measures were non- normally
distributed and therefore we applied Spearman’s rank correlation analyses. Two
participants from the Excess weight group (n = 37) and one participant from the Normal
weight group had missing cortisol data at T1 and T2 (n = 41). With regard to cognitive
tests, there was no missing data in the Excess weight group (n = 39), whereas in the
Normal weight group three participants had invalid data for RVP response latency and
IGT (n = 39) at T1 or T2, and three participants had invalid data for RVP B’ (n = 38) at
T1 or T2.
3. Results
88
Cortisol response
We found a significant Time x Group interaction on cortisol levels, F (3,74) = 4.36, p =
0.008. Cortisol mildly increased in Excess weight participants after the TSST.
Independent-sample t- tests showed that Excess weight and Normal weight participants
did not significantly differ on cortisol levels before TSST (T1). However, Excess
weight adolescents showed significantly increased cortisol levels after TSST (T2), t =
1.94, p = 0.05, Cohen’s d = 0.5 (Fig 2). Moreover, cortisol increase between T2 and T1
correlated with amount of fat, Spearman’s Rho = 0.30, p = 0.01. Between-group
differences were also statistically significant at T3, t = 2.44, p = 0.02, and T4, t = 2.63, p
= 0.01. However, this effect seems to be driven by decreased cortisol levels in the
Normal weight group (Fig 2).
Fig 2. Cortisol levels (μg/dl units) in adolescents with excess weight and adolescents with normal weight
before and after exposure to the Trier Social Stress Task (TSST). T1 represents cortisol levels before
TSST; T2 represents cortisol levels immediately after TSST termination; T3 and T4 represents cortisol
levels 10 and 20 minutes after TSST termination.
89
Cognitive performance
MOT. Pre-TSST scores showed that both groups had similar baseline response
latencies. Further, both groups showed mild reductions of response latencies between
the pre-TSST measure and the post-TSST measure (Fig 3).
RVP—Response latency. We found a significant Time x Group interaction, F
(1,76) = 6.35, p = 0.01 (Fig 3). Independent-sample t-tests showed that Excess weight
and Normal weight participants did not significantly differ in the pre-TSST measure.
However, they showed marginally significant differences in the post-TSST measure, t
(78) = 1.75, p = 0.08, Cohen’s d = 0.4, with Excess weight participants performing
significantly poorer than Normal weight controls. There was no significant correlation
between T2—T1 cortisol levels and T2—T1 RVP Response Latency.
RVP—Response discriminability. We did not find a significant Time x Group
interaction, F (1,75) = 0.99, p = 0.32. There were no main effects of Time or Group,
although visual inspection shows Excess weight participants performed better than
Normal weight participants in both pre- and post-TSST measures (Fig 3).
Decision-making—IGT. We did not find a significant Time x Group interaction,
F (1,77) = 0.005, p = 0.94. There was a significant main effect of Time, F (1,77) = 6.01,
p = 0.02, indicating that both groups exhibited significantly poorer performance after
the TSST (Fig 3). There was no significant correlation between T2—T1 cortisol levels
and T2—T1 IGT performance.
90
Fig 3. Cognitive performance in adolescents with excess weight and adolescents with normal weight
before and after exposure to the Trier Social Stress Task (TSST). Top panel Y axes represent time in
milliseconds. The Y axis in the bottom-left panel represents signal detection derived Beta scores, ranging
from 0 to 1. The Y axis in the bottom-right panel represents Iowa Gambling Task net scores, ranging
from -60 to +60.
Correlations between biological and psychological measures and cognitive
performance in T2—T1. We found a positive correlation between levels of uric acid and
change in RVSP response latency performance between T2 and T1, Spearman’s Rho =
0.46, p = 0.0001, and a negative correlation between thyroxine levels and change in
Iowa Gambling Task performance between T2 and T1, Spearman’s Rho = -0.27, p =
0.03. We also found a negative correlation between scores of external eating and RVSP
response latency performance between T2 and T1, Spearman’s Rho = -0.27, p = 0.02.
Visual Analogue Scales (VAS). We did not find a significant Time x Group
interaction on VAS of arousal or stress but results were in the expected direction, with
both groups showing more subjective arousal and stress after the TSST.
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Post-hoc analyses in the subsample of participants showing enhanced cortisol
response. The primary analyses indicated that in the normal weight group cortisol levels
did not change after stress, and therefore there is a concern that cognitive changes were
due to spurious factors. To address this issue, we run additional analyses in the
subsample of participants who showed sizeable increments in cortisol levels after stress,
including 24 participants of the Excess weight group (57% of the original sample) and
20 participants of the Normal weight group (48% of the original sample). The results of
these analyses were coherent with the main findings. We found a significant Time x
Group interaction on RVP’s latency scores, F (1,41) = 6.17, p = 0.02, whereby a drop in
performance was only observed in the Excess weight group. Moreover, there was a
significant correlation between T2—T1 cortisol levels and T2—T1 RVP Response
Latency (Spearman’s Rho = 0.25, punilateral = 0.05) (Fig 4).
Fig 4. Correlation between between T2—T1 cortisol levels (X Axis) and T2—T1 RVP Response Latency
(Y Axis) within the subsample of participants showing TSST-induced increases in cortisol levels.
92
4. Discussion
We show that social stress specifically increases cortisol levels and hinders attentional
response latency in adolescents with excess weight. Conversely, social stress failed to
show significant effects on attention response discriminability. Moreover, both excess
weight and normal weight adolescents displayed poorer decision-making performance
after the social stressor. These findings indicate that adolescents who are overweight
and obese have enhanced stress reactivity in response to social stressors, which
selectively impacts on attentional skills. Since adolescents with excess weight are
markedly exposed to social stressors during everyday lives, our findings suggest that
stress immunization strategies should be put in place to prevent the harmful impact of
social stress on cognition and therefore on progression of obesity.
In agreement with our primary hypothesis, social stress induced greater cortisol
response in overweight and obese adolescents. The effect was mild but the specific
impact on participants with excess weight agrees with the notion that repetitive social
stress may induce sensitization of the hypothalamic-pituitary-adrenal (HPA) axis [22]
and purportedly of the HPA axis associations with fronto-limbic systems [23–25]. The
discrepancy between our finding of cortisol increase and a previous negative finding in
obese adults [26] suggests that adolescence compared to adulthood is a more sensitive
time period for abnormal sensitization of stress systems, likely due to ongoing neural
maturation of these systems [7,27]. Further, both preclinical and clinical evidence
shows that social stressors such as social evaluation and social exclusion are particularly
challenging for adolescents [8,28,29]. The potential mechanisms for the specific impact
of social stress on stress reactivity in adolescents with excess weight include the
additive or synergistic interactions between social stress and inflammation [30,31]
93
and/or between social stress and obesity-related neuroadaptations in anterior cingulate
and limbic regions that are essential for stress regulation [32,33]. Our finding is
particularly relevant in view of the significant association between cortisol reactivity
and obesity-related behaviours [34,35], and of the emerging evidence suggesting that
high levels of stress can longitudinally predict the progression of obesity [36].
We also showed a significant impact of social stress on attentional performance in
adolescents with excess weight. The effect was again mild and pointed to stress-related
hindering of the capacity to get benefit from a repeated administration of the task.
Previous findings indicate that repeated administration of CANTAB attentional tests is
associated with significant improvements in performance (of at least 0.3 in Cohen’s d
effect size) [37], and this is what we observed in the control group. However, excess
weight adolescents were unable to get benefitted from this repeated administration. The
effect was specific for attention-related latency adjustments, but not for psychomotor-
related reaction times. Therefore, it suggests a detrimental impact of stress on attention
regulation.6 This notion is consistent with the neural networks interactions between the
HPA axis and medial prefrontal cortex and anterior cingulate cortex regions involved in
attention regulation [38–40]. In support, neuroimaging studies have shown that the
impact of stress on executive attention is mediated by structural (gray matter)
neuroadaptations in prefrontal cortex and anterior cingulate cortex regions [41]. This
stress-related attentional hurdle has a high translational value, as individual differences
in response latencies to attentional probes are longitudinally associated with increases in
BMI [12], implying that adequate control of social stress and/or cognitive boosting of
attentional resources may contribute to prevent chronic obesity. This notion is
consistent with our finding of significant correlations between less improvement of
attentional performance (between T1 and T2) and higher maladaptive eating patterns
94
such as external eating, which reflects attentional bias towards food related cues.
Further, both social stress and attentional skills are significantly associated with
advantageous social functioning and academic performance [3], and therefore our
finding highlights the potential benefit of controlling social stress to improve social and
career outcomes in the long-term.
Furthermore, we found poorer decision-making after the social stressor in both
adolescents with excess weight and adolescents with normal weight. Since cortisol
levels dropped between T3 and T4 (the time window of decision-making task
performance) it is unlikely that this finding can be attributed to the effects of acute
stress. However, it might be attributed to broader effects of the social stressor, such as
the social evaluation context. The latter notion agrees with previous experimental
evidence showing that adolescents make riskier choices than young adults or adults
when they are under social evaluation [42]. The lack of specificity of our result implies
that the impact of social evaluation on decision-making is mediated by neural
mechanisms that are similarly sensitized in adolescents regardless of BMI/weight status,
or that different neural mechanisms mediate a similar impact of social evaluation on
decision-making in excess weight and normal weight adolescents. In favour of the first
notion, neuroimaging studies have shown that the impact of social evaluation on
decision-making is mediated by increased activation of ventral striatal and orbitofrontal
regions [43], which are generally sensitized during adolescence. In favour of the second
notion, we have observed that excess weight and normal weight adolescents recruit
different brain circuitries during the pondering of social decisions [44]. Future studies
are warranted to address this question. In any case, our finding might have general
implications for prevention of obesity during adolescence as we know that adolescents
who are overweight or obese have higher exposure to social evaluations [3] and that
95
subsequent risky choices are longitudinally associated with weight gain and obesity
[11].
We conclude that social stress response is sensitized in adolescents with excess weight,
hindering their attentional function. The study has important strengths including the
experimental design, the power-informed sample size, the detailed phenotypic
characterization and the group matching of excess weight and normal weight
adolescents, and the objective measurement of stress reactivity with cortisol biomarkers.
However, the results should be as well appraised in light of relevant limitations. It is
particularly important to stress that unlike the original TSST [45], the virtual reality
TSST was not able to induce significant increases of cortisol levels in the control group.
We selected this stressor because it was capable of inducing mild but sizeable stress in
the laboratory at the same time that it reduced the ethical implications of stressing “at
risk” obese adolescents [18]. In agreement with this assumption, our results indicate that
the stress manipulation was actually more effective in obese adolescents (57% of
participants showed increased cortisol levels) than in controls (only 48% of participants
showed increased cortisol levels). There are however several factors that may explain
the variability in stress induction, such as degree of belief in the cover story or degree of
immersion in the virtual reality environment, that were not systematically controlled in
this study. Therefore, further studies are warranted to reassess the validity of this virtual
reality version, and to replicate our findings using TSST versions that are able to
unequivocally reproduce the original TSST stress induction. Moreover, in absence of a
“no-stress” control condition, we cannot ascertain a causal link between stress and
cognitive performance. However, we base our interpretation on previous evidence
showing that improvement (rather than stability or decrease) in performance is typically
expected in “no-stress” repeated administration designs [37]. A related limitation is the
96
negative finding in relation to cognitive impulsivity. Since mild arousal improves
inhibitory control in adolescents, it is plausible that the mild nature of the stressor
fostered cognitive impulsivity increases rather than (expected) decreases after TSST.
Future studies are warranted to address these limitations, to expand on the biological,
psychological and socio-economic mediators of the impact of social stress on cognition,
and to longitudinally assess the relevance of this experimental effect on public health
indicators of the progression of obesity.
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Capítulo 7. Negative social evaluation impairs executive
functions in adolescents with excess weight: associations with
autonomic responses.
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Capítulo 7. Negative social evaluation impairs executive functions in excess weight adolescents: associations
with autonomic responses
1. Introduction
Overweight and obesity in adolescence have sharply increased over recent decades,
reaching epidemic levels (1). The socioeconomic changes that have occurred in recent
decades in Western societies, associated with the unlimited access to food, have
modified the way we perceive food and regulate intake. These processes are
increasingly influenced by a variety of factors besides homeostatic regulation, like
sensory cues (e.g., taste, smell, texture and appearance), availability, motivational and
affective states, pleasure seeking, etc. All of these factors influence what and how much
people eat even when they are not hungry (2). In the last few years, obesity is being
increasingly considered as a brain-related dysfunction similar to that occurring in
addictions (3), where the motivational value of highly palatable food is significantly
increased, while the top-down or executive control mechanisms that would normally
regulate reward-driven responses are diminished (4, 5). Executive control mechanisms
are relevant to the regulation of eating behavior (6), since they allow for adjustment of
behaviour in a flexible way in situations that require a change in a strong habitual
response or resistance to temptation (7). The abnormal interaction between reward
signal processing and executive control functioning has also been related to a tendency
to select immediate and appetizing (high in calories and/or sugar) rewarding choices,
although these have negative consequences in the long term (8, 9). The imbalance
between these two systems can be greater in adolescence, a period characterized by the
relative immaturity of the prefrontal cortex, responsible for executive control, in
addition to the relative maturity of striatal areas responsible for reward processing (10).
Therefore, during adolescence, the activity of rewards system may prevail over that of
executive control mechanisms (11).
108
Another factor that can impair top-down control mechanisms is stress. Stress has a
harmful impact on cognitive skills, such as attention, cognitive control and decision-
making, which may contribute to obesity-related behaviours in adolescents (12).
Furthermore, psychosomatic theories hold that people with obesity tend to eat in
response to emotional distress, showing an “emotional eating pattern” (i.e., consuming
food impulsively) when under negative emotional states (13). Stress can also enhance
the propensity to eat high calorie “palatable” food via its interaction with central reward
pathways (14). For example, ghrelin and cortisol increase in response to social stressors
and influence reward motivation, thus modulating consumption of appetizing food (15,
16)
During adolescence, peer relations are particularly salient and can serve as a robust
source of distress (17). Adolescents with excess weight suffer from social stress, such as
bullying or social marginalization-exclusion, more frequently than their peers (18),
being subjected to frequent teasing about their body (19). Negative stereotypes toward
peers with excess weight begin early in childhood (20) and these social stressors can
negatively affect social adjustment and academic achievement (21). In this context,
study of the detrimental influence of social stress on executive functions may be of
crucial importance to understand deficient diet-related decision-making and poor
emotional-regulation-related overeating in adolescents.
Several studies have found deficits in executive functioning in adults and adolescents
with excess weight (22-25). However, to the best of our knowledge, no study has
analyzed the influence of social stress on executive functions in adolescents with excess
weight. Therefore, this study examined the effect of a social stressor on executive
performance in adolescents with excess versus normal weight. For this purpose, the
Trier Public Speaking Stress Social Task (TSST) (26, 27) was used. We analyzed the
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specific influence of negative social evaluation on executive functioning and autonomic
responses in adolescents with overweight. We hypothesized that excess weight
adolescents would show decreased executive performance after exposure to social stress
relative to normal weight adolescents. Outcome measures were working memory,
cognitive inhibition, and shifting (ability to follow different rules in a task and change
between them). Additionally, subjective and physiological (autonomic) indexes of stress
were recorded. For this purpose, heart rate (HR) and skin conductance (SC) were
continuously recorded during the TSST. Since adolescents with overweight are more
often exposed to negative peer evaluations than adolescents with normal weight (18,
19), we expected greater increases in perceived stress, HR and SC in excess versus
normal weight participants during the TSST. Furthermore, negative associations
between stress-induced subjective and physiological responses and post-TSST
executive performance were hypothesized.
2. Method
Participants
Sixty adolescents, 25 males and 35 females between 13 and 18 years of age,
participated. They were selected based on their sex and age-adjusted BMI percentile in
accordance with the guidelines of the International Obesity Task Force (IOFT) (28).
Normal weight participants (n=30) had BMIs ranging between the 5th and 84th
percentiles, and excess weight participants (n=30) had BMIs > the 85th percentile. Table
1 displays the socio-demographic, BMI and body fat percentage data. Participants were
recruited from high schools located in Jaén (Spain). They were screened for medical and
developmental conditions, medication use, and learning disabilities. Inclusion criteria
were: (i) aged range between 13 and 18 years; (ii) BMI > 5th percentile; and (iii) no
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history of neurological, psychiatric or eating disorders [measured using the Eating
Disorder Inventory (EDI-2)]. All participants had normal or corrected-to-normal vision.
Table 1. Participants’ socio-demographic characteristics, BMIs and body fat percentage.
Excess weight Normal weight

ta/chi squareb p
Mean SD Mean SD
Age 15.38 1.75 15.41 1.36 -0.08a 0.935
Sex (%Men/ women) 46.7/53.3 36.7/63.3 0.62b 0.601
BMI 28.53 2.96 20.04 2.05 12.87a <0.001
% Body fat 28.04 7.78 17.32 7.71 5.36a <0.001
BMI body mass index.
a
value of Student’s t;
b
value of Chi-square χ2
Executive Measures
Working memory–Letter-Number Sequencing (29): Participants were read a sequence in
which letters and numbers were combined, and were asked to reproduce the sequence,
first putting the numbers in ascending order and then the letters in alphabetical order.
The sum of the correct answers was considered.
Inhibition and shifting–Five-digit test (FDT (30): The FDT consists of four conditions
of increasing complexity. Conditions 1 and 2 evaluate processing and response speed.
In condition 3 (inhibition), participants have to count the number of digits contained
within various boxes, which constitutes an interference effect because the boxes contain
groups of digits that do not correspond to their arithmetic value. Finally, in part 4
(shifting), participants have to count or read, depending on whether the outline of the
box is normal (count, 80% of stimuli) or of double thickness (read, 20% of stimuli). The
difference in performance time between part 3 and the mean of parts 1 and 2 (inhibition
score), and the difference in performance time between part 4 and the mean of parts 1
and 2 (shifting score), were considered. Thus, a higher score denotes worse performance
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(i.e., the participant took more time). Errors in parts 3 (inhibition) and 4 (shifting) were
also analyzed.
Social stress task

To induce social stress in the laboratory, a validated Virtual Reality version of the Trier
Social Stress Task (TSST-VR) was used (26). This version of the TSST was previously
used in young people and has been shown to produce a significant increase in subjective
stress and arousal, skin conductance and cortisol levels (27, 31). Participants had to
deliver a speech about their personal characteristics, including both positive and
negative aspects, in front of a simulated audience. The task is divided into two parts
(each 2 min 30 s long). In the first task, the audience was interested and attentive to the
speech, giving nods of understanding to the participant (i.e., positive social evaluation).
In the second part, the audience began to show signs of disagreement with the speech,
talking and murmuring among themselves and criticising the participant´s words (i.e.,
negative social evaluation). The task included four phases: a baseline rest period (3
min), delivery of the task instructions and preparation for the speech by the participant
(3 m), speech during positive social evaluation, and speech during negative social
evaluation. This virtual reality version of the TSST is able to induce modest but
significant increases in cortisol and subjective stress responses (26).
Procedure
After obtaining permission from the high school´s directors, the study was presented to
each class of students and their participation was requested. The students who were
interested in taking part sent us the informed consent form, which was signed by their
parents if they were minors. Then, the participants were assigned to a group and a
specific day on which to complete the experimental session. Six high schools in Jaén
participated in the study. The recruitment rate was approximately 4% of the total
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number of students approached. Sessions started at 4 p.m. and participants were
required to be satiated (having had lunch about 1 hour before) and to not have taken any
caffeine. Weight and height were self-reported by participants for recruitment purposes
and BMI was calculated in the laboratory, using the exact height and weight data
collected on arrival. Body composition measures were also collected using the
Bodystat®1500 monitoring unit. The EDI-2 (32), validated in young people, was
administered to rule out eating disorders (binge eating, anorexia nervosa and bulimia
nervosa). Then, executive functioning measures were conducted before TSST onset
(pre-TSST) and immediately after completion of the TSST (post-TSST). The post-TSST
evaluation was administered immediately after TSST. During the two evaluations,
participants first completed the Letter-Number Sequencing and then the Five Digit Test.
Subjective stress was measured by a visual analogue scale (VAS, ranging from 1 to 10;
no stress to extreme stress) before and after exposure to TSST. The virtual reality TSST
was carried out in a soundproof room, with white walls and without any distracting
stimuli. The equipment consisted of a computer running the program containing the
social scenes, and a projector for their display on the wall. Previous validation studies
indicated increases in skin conductance and salivary cortisol during the task, both when
scenes were presented via goggles or projected on to a screen (31). However,
participants rated task immersion as being higher with the wall-screen presentation
versus the goggles (31). Surround-sound headphones were used to allow perception of
the sound emanating from the room where the audience was situated, and the murmurs
and comments of the listeners. The Ethics Committee of the Universidad de Jaén
approved the study. Both participants and parents signed informed consent forms.
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Psychophysiological Data Acquisition and Processing

HR and SC were continuously recorded during the TSST using a Biopac MP150
polygraph (Biopac Systems Inc., USA). HR (beats per minute) was derived from an
electrocardiogram (ECG) recorded at 1000 Hz. ECG electrodes (Ag/AgCl) were
attached to the participant’s right mid-clavicle and the lowest left rib (left wrist as the
ground). HR was extracted from ECG recordings using the software AcqKnowledge
3.9.1 (Biopac Systems Inc.) and edited for artifacts (when present) via linear
interpolation. SC (micro-Siemens, μS) was recorded at a sampling rate of 500 Hz using
Ag–AgCl electrodes filled with an inert 0.05 M NaCl electrolyte cream and attached to
the palmar surface of the second and third middle phalanges of the participant’s non-
dominant hand. Two participants (one from each group) had unusable SC recordings.
Group comparisons were carried out with Student’s t-test for independent samples.
Responses to the TSST were analyzed by repeated measures ANOVA with Time (pre-
and post-TSST) as the repeated-measures factor and Group (Excess versus Normal
weight) as the between-subject factor. Although the TSST consisted of four phases,
given our specific interest in the effect of social evaluation, HR and SC analyses were
restricted to the difference between the latter two parts of the TSST involving social
evaluation (positive versus negative social evaluation). Associations between variables
were analyzed by Pearson’s correlations. To simplify the correlation analysis, change
scores were computed as the difference between the post- and pre-TSST values.
3. Results
Associations between measures
In the whole sample, the change in HR was positively associated with changes in stress
VAS scores (r=0.32, p=0.013), “shifting errors” (r=0.30, p=0.02), “inhibition errors”
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(r=0.38, p=0.003) and the “shifting score” (r=0.26; p=0.046). The change in SC
correlated inversely with the change in Letter-Number Sequencing (r=-0.33, p=0.01),
and positively with the change in stress VAS scores (r=0.26, p=0.047). Finally, the
change in stress VAS scores correlated positively with the change in “inhibition errors”
(r=0.46, p<0.001). BMI was positively associated with post-TSST “inhibition errors”
(r=0.51, p<0.001), “shifting errors” (r=0.32, p=0.001) and stress VAS scores (r=0.31,
p=0.015).
Subjective stress
A Time x Group interaction was found for stress VAS scores (F1,58=9.76, p=0.003,
𝜂𝜂𝑝𝑝2 =0.14). While in adolescents with excess weight stress levels increased from pre- to
post-TSST evaluation (F1,29= 65.89, p<0.001, 𝜂𝜂𝑝𝑝2 =0.69), the change in adolescents with
normal weight did not reach significance (F1,29=2.66, p=0.115, 𝜂𝜂𝑝𝑝2 =0.08) (Table 2).
Table 2. Descriptive scores and group comparisons for stress (VAS) and neuropsychological
measures before TSST (PRE-scores) and after TSST (POST-scores)
t p d´
Mean SD Mean SD
Stress Pre 1.49 1.65 1.82 1.91 0.72 0.474 0.18

Stress Post 4.03 2.45 2.59 2.18 2.39 0.020 0.62
Letter-Number Sequence Pre 9.03 2.53 8.73 1.76 0.53 0.597 0.14
Letter-Number Sequence Post 9.03 2.93 10.87 2.70 2.52 0.015 0.65
Score-inhibition-5DigitTest Pre 17.13 7.16 13.75 5.33 2.07 0.042 0.54
Score-inhibition-5DigitTest Post 12.73 4.40 10.85 5.16 1.52 0.134 0.39
Score-shifting-5DigitTest Pre 22.37 6.80 20.81 5.99 0.94 0.353 0.24
Score-shifting-5DigitTest Post 21.07 3.86 16.52 4.84 4.02 <0.001 1.04
Errors-inhibition-5DigitTest Pre 0.77 0,97 0.70 0.95 0.27 0.067 0.01
Errors-inhibition-5DigitTest Post 1.70 0.95 0.37 0.61 6.44 <0.001 1.67
Errors-shifting-5DigitTest Pre 1.50 1.57 1.13 1.25 1.00 0.321 0.26
Errors-shifting-5DigitTest Post 2.37 2.35 0.80 1.29 3,19 0.002 0.83
VAS visual analogue scale; TSST Trier Social Stress Task; FDT Five-Digit Test.
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Psychophysiological measures
No group differences were found in HR or SC during the pre-TSST evaluation. A Time
x Group interaction was found for HR (F1,58=8.26, p=0.006, 𝜂𝜂𝑝𝑝2 = 0.13) (Figure 1). While
HR increased in adolescents with excess weight from the positive to the negative social
evaluation phase of TSST (F1,29=8.45, p=0.007, 𝜂𝜂𝑝𝑝2 =0.23), no change was observed in
adolescents with normal weight (F1,29=1.16, p=0.29, 𝜂𝜂𝑝𝑝2 =0.04). A Time x Group
interaction was also observed in SC (F1,56=4.76, p=0.033, 𝜂𝜂𝑝𝑝2 =0.08) (Figure 2). While
SC decreased in adolescents with normal weight from the positive to the negative social
evaluation phase of the TSST (F1,28=17.15, p<0.001, 𝜂𝜂𝑝𝑝2 =0.38), no change was observed
in adolescents with excess weight (F1,28=0.24, p=0.63, 𝜂𝜂𝑝𝑝2 =0.01).
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Executive functions
During the pre-TSST evaluation, excess weight participants showed greater scores in
the inhibition condition of FDT (i.e., lower inhibition) than normal-weight participants
(t=2.08, p=0.042, δ=0.54). No other significant differences arose during pre-TSST (see
Table 1). Significant Time x Group interactions were found for Letter-Number
Sequencing (F1,58=16.82, p<0.001, 𝜂𝜂𝑝𝑝2 =0.23) (Figure 3), “inhibition errors” in FDT
(F1,58=31.34, p<0.001, 𝜂𝜂𝑝𝑝2 =0.35), “shifting errors” in FDT (F1,58=10.80, p=0.024, 𝜂𝜂𝑝𝑝2 =
0.08) (Figure 4) and “shifting score” in FDT (F1,58=15.47, p=0.039, 𝜂𝜂𝑝𝑝2 =0.07).
Adolescents with normal weight significantly increased their performance after the
TSST in Letter-Number Sequencing (F1,29=26.14, p<0.001, 𝜂𝜂𝑝𝑝2 =0.47) and “shifting
score” (F1,29= 23.02, p<0.001, 𝜂𝜂𝑝𝑝2 =0.44) and decreased their “inhibition errors” (FDT)
(F1,29=6.59, p=0.01, 𝜂𝜂𝑝𝑝2 =0.19). By contrast, adolescents with excess weight increased
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their “inhibition errors” (FDT) (F1,29=25.38, p<0.001, 𝜂𝜂𝑝𝑝2 =0.467) and, marginally, their
“shifting errors” (FDT) (F1,29=4.15, p=0.051, 𝜂𝜂𝑝𝑝2 =0.13).
4. Discussion
Adolescents with excess weight, compared to those of normal weight, showed
impairments in measures of inhibition and shifting, and higher subjective stress levels,
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in response to the TSST. Furthermore, adolescents with excess weight showed a
differential psychophysiological pattern during the TSST. HR increased during the
negative social evaluation phase (relative to the positive phase) in this group, while no
change was observed in adolescents with normal weight. SC decreased in adolescents
with normal weight from the positive to the negative social evaluation phase, suggesting
habituation to the situation, but did not change in adolescents with excess weight. Skin
conductance is a variable that usually displays a decrease over the recording period,
denoting habituation to the situation. A flat recording, without any sign of decrease, is
usually interpreted as indicating a high electrodermal level (33).
Our findings suggest that adolescents with overweight-obesity have enhanced
sensitivity to social stressors. This is manifested both at subjective and physiological
levels. Subjectively, the greater increase in stress levels indicates that adolescents with
excess weight perceive the situation as more stressful than do adolescents with normal
weight. At the physiological level, results indicate a greater mobilization of
physiological resources and autonomic reactivity during social stress, particularly
during negative social evaluation, in adolescents with excess weight. The most common
motivation for using a public speaking task is that it elicits a social evaluation-related
threat (34). The inclusion of the two phases of the TSST as a function of feedback from
the audience (positive versus negative) allowed for a more specific analysis of social
evaluation, making our results more innovative. Taken together, these results support
the utility of differentiating between positive versus negative social evaluation during
the TSST for the study of the impact of social stress on autonomic and cognitive
functions.
The observed negative impact of social stress on executive functioning in adolescents
with excess weight is consistent with a previous study which showed impaired attention
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after TSST in adolescents with excess weight compared to adolescents with normal
weight (27). Negative emotional states in adults are known to impair cognitive capacity;
for example, depressive symptoms in people with obesity impair executive function
(35). Furthermore, emotional eating patterns, which are more prevalent in this
population (15), may additionally affect executive functioning. Specifically, socially
stressful situations evoke negative mood states and impair impulse control. The joint
influence of executive deficits and emotional eating patterns would lead to further
eating disinhibition. However, no previous studies have analyzed the effects of
emotional states on executive functioning in adolescents with excess weight.
Inhibition, shifting and working memory were negatively affected by social stress in our
excess weight adolescents. This suggests that social stress has a detrimental impact on
executive functioning in these adolescents, and this may influence their eating
behaviour. Usually, in pre-post cognitive evaluations, performance improves in the
second evaluation due to practice effects arising from repeated administration (36, 37).
In fact, in this study working memory improved significantly in the normal weight
group from the pre- to post- TSST evaluation. However, adolescents with excess weight
did not benefit from this learning experience, and in fact their performance decreased. A
previous study (27) using the same experimental protocol also found increases in
attention performance in normal weight participants from the pre- to post-TSST
evaluation, while excess weight participants were unable to benefit from the practice
effect. These results may be due to the greater levels of stress during the TSST in
adolescents with excess weight. Stress negatively affects abilities that require conscious
attention and effortful information processing, reducing therefore cognitive efficiency
(38). Greater cortisol responses to the TSST were found in the previous study (27), and
results of the present study showed higher heart rate and electrodermal reactivity to the
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social stress task in adolescents with excess weight. Furthermore, autonomic reactivity
after TSST, specifically electrodermal response, correlated inversely with working
memory performance in the whole sample. Therefore, the greater autonomic and stress
response in adolescents with excess weight can increase stress interference in this group
and therefore lead to a deficit in learning from the repeated administration of the tasks.
Executive functioning may have multiple direct and indirect influences on obesity in
adolescence. Although available evidence links executive functioning and obesity (24,
39), the specific mechanisms mediating this association are less well-known. Some
studies have found that executive dysfunction is associated with obesity-related
behaviours in childhood and adolescence via increasing intake, disinhibiting eating, and
reducing physical activity. The inability to inhibit impulses predicted higher food
intake, a higher body weight and less weight loss after a weight reduction intervention
(40). Deficits in inhibition can impact impulse control and thus the capacity to restrict
intake of appetizing foods (high fat/sugar). Impairments in shifting may influence the
capacity to regulate and modify eating behaviours in order to prevent harmful health
consequences. Furthermore, this deficit may lead to adolescents with excess weight
persisting in their unhealthy eating habits. Impairments in working memory could affect
the ability to maintain cognitive control, making it more difficult to engage in healthy
activities and intervention programs. Finally, disinhibited eating in obese adolescents
was associated with reduced orbitofrontal volume and executive dysfunctions, which
were most pronounced in terms of working memory and inhibition (41). Conversely,
executive function skills were positively associated with healthy eating habits, such as
fruit and vegetable intake, and physical activity (42, 43).
We observed group differences before social stress only in the “inhibition score” (FDT),
with lower performance in excess than normal weight adolescents. However, no
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differences were found in shifting or working memory. These results are concordant
with a previous study reporting selective alterations in inhibition in adolescents with
obesity versus normal weight adolescents (43). Another study found selective
alterations in inhibition and shifting, but not working memory, in excess weight and
obese adolescents (24). In contrast, others authors found significant differences between
obese and normal adolescents in working memory as well as attention, but not in
intelligence or verbal fluency (44). Discrepancies between studies may be due to
differences in testing methods, samples and levels of BMI.
As expected, the change in subjective stress was positively associated with the change
in HR, SC and “inhibition errors” (FDT). This suggests that levels of subjective stress
may modulate both psychophysiological responses and executive-inhibition functions.
In this way, negative social evaluations may induce a greater increase in stress levels
and autonomic responsiveness, and a reduction of inhibition capacity, in excess weight
adolescents relative to those with normal weight. The deleterious influence of negative
social evaluation on executive control in adolescents with excess weight may exacerbate
difficulties in eating behaviour control, eventually triggering overconsumption.
The change in HR during social evaluation was positively associated with the change in
“shifting errors”, “inhibition errors” and “shifting score” in the whole sample. The
change in SC was negatively associated with the change in Letter-Number Sequencing
performance (i.e., greater habituation of skin conductance was associated with better
working memory). These results suggest that modulation of autonomic activity by
social stress may index, or additionally influence, executive functioning in adolescents
with excess weight. This harmful effect on executive functioning may lead to problems
in real life, such as poor regulation of eating habits. However, studies in adults also
using the TSST did not find differences in HR, blood pressure or cortisol responses
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between obese and normal weight individuals (15). This discrepancy may be due to the
non-inclusion of specific positive-negative evaluation phases in their TSST, or may
reflect a greater vulnerability to social stress in adolescents than adults. In line with the
greater autonomic response found in our study, a greater cortisol response after the
TSST has been previously found in excess weight than in adolescents with normal
weight (27).
Executive functioning is still developing during adolescence, since prefrontal areas
reach full development at maturity (45). A growing body of literature suggests an
altered balance between the earlier-developing limbic system and the later developing
frontal/executive system (46) during adolescence. Furthermore, in this period, the
opinions of peers and general social evaluation become a central aspect for self-image
development (47). Adolescents with excess weight frequently suffer from negative
social evaluations and social stressors during their everyday lives, which may lead to
greater vulnerability to social stress, especially if a negative social evaluation
component is included. It would be reasonable to assume that adolescents with excess
weight would show a blunted stress response due to habituation to repeated stress
exposure. However, previous studies using this same TSST protocol found greater
increases in salivary cortisol in excess weight than in normal weight adolescents (27).
These results suggest the development of a sensitization process to social stress in
adolescents with excess weight.
Therefore, due to all of the factors listed above, adolescents with excess weight are an
important target group for cognitive interventions based on stress regulation strategies,
executive function improvement and prevention of harmful eating behaviours. In this
regard, some evidence already suggests that executive functioning training for obese
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children can improve working memory, inhibition and shifting, being useful in weight-
loss maintenance (48).
Regarding its strengths, our study used an innovative strategy to evaluate the impact of
social stress, particularly negative social evaluation, on adolescents with excess weight,
as well as the inclusion of autonomic variables as objective indices of stress. Among the
limitations, we used a virtual reality audience in our TSST instead of the actual public,
which might have decreased the realism of the situation and the stress-elicited
responses. However, this version of the TSST was validated in previous studies and
produced a reliable stress response (26, 27, 31). Furthermore, the inclusion in future
studies of a non-stress control condition (also with two cognitive evaluations) is
recommended to rule out more possible general disruption of cognitive processes in
excess weight adolescents. Regarding the study design, the absence of any
counterbalancing of the order of presentation of positive versus negative feedback
conditions might have influenced the results. Therefore, this aspect should be taken into
account in future studies. Additionally, we did not assess factors like emotional eating
or loss of control in eating behaviour, which may be relevant to overeating. Finally,
longitudinal studies are necessary to better analyse the influence of stress-induced
executive functioning decrements on the propensity to overeat and become obese in the
future in adolescents with excess weight.
In summary, our results showed a harmful impact of social stress, specifically negative
social evaluation, on executive functioning of adolescents with excess weight.
Adolescents with overweight performed worse after TSST in inhibition and shifting
than those with normal weight, and they did not benefit from learning in the domain of
working memory, in contrast to adolescents with normal weight. Furthermore, in
association with the observed decreases in neuropsychological performance, adolescents
124
with excess weight showed greater subjective and autonomic stress responses to
negative social evaluation. Given the relevance of high order executive functions to
self-control of eating behaviour (49, 50), the results presented herein highlight the value
of assessing the social evaluation context, and how it may be associated with
differential changes in cognitive functioning in adolescents with overweight. This
stress-mediated impairment in cognitive functioning could increase the risk for future
obesity. Interventions aimed at social stress coping strategies and improvement of
executive functions could be useful in the prevention of obesity in adulthood.
Authors’ Statement of Conflict of Interest. The authors declare no conflicts of interest.
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130
131
Capítulo 8. Risky decision-making after exposure to a food-
choice task in excess weight adolescents: relationships with
high-calorie food preferences and hunger
Moreno-Padilla, M., Fernández-Serrano, M. J., & Reyes del Paso, G. (2018). Risky
decision-making after exposure to a food-choice task in excess weight adolescents:
Relationships with high-calorie food preferences and hunger. Plos One. Under review.
132
133
Capítulo 8. Risky decision-making after exposure to a food-choice task in excess weight adolescents:
relationships with high-calorie food preferences and hunger
1. Introduction
The prevalence of overweight and obesity in adolescence has increased considerably in
recent decades [1,2]. Excess weight in adolescents is a strong predictor of adult obesity
[3]. Overweight and obesity, being associated with increased incidence rates of diabetes,
cardiovascular diseases and certain kinds of cancer, are currently the fifth-leading
mortality risk factor (World Health Organization [WHO]).
In the last few decades, drastic changes in the environment and lifestyles have modified
the way we perceive foods and regulate their intake [4]. The availability of a wide range
of foods, and overexposure to marketing-related images of foods in Western societies,
has led to what, and how much, to eat becoming a decision-making matter. Obesity has
been proposed as a problem of food addiction, with overeating explained as an
imbalance between motivational and control-inhibition systems [5,6]. From this theory,
it is proposed that in vulnerable individuals, the consumption of large amounts of
appetizing food (high in fat and/or sugar) could cause an imbalance in the interaction of
these systems, resulting in an increase in the motivational-reinforcing value of
appetizing food and a weakening of the control-inhibitory system [6]. This deficit in
control and inhibitory influences would lead to impulsive and compulsive intake of
appetizing foods, and as a consequence, to the development and maintenance of obesity
[6].
The impact of inhibitory control on eating behaviour seems to be particularly relevant
during adolescence [7], a developmental period in which both motivational tendencies
and impulse control skills strongly modulate goal-directed behaviour [8]. Furthermore,
decision-making skills are particularly relevant in adolescents, in whom executive
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control areas (prefrontal areas) are not completely developed and seem to maximize
reward at the expense of risk [8].
A relevant perspective in impulsive decision-making is the concept of risk-taking. Risk-
taking propensity refers to the appetitive processes underlying a behavioral
predisposition to take risks in response to signals for potential reward, which also
confers a probability of unattractive results [9]. In recent years, the concept of risk-
taking has been used to describe impulsive behavior in drug addiction and obesity
[10,11]. Previous studies have repeatedly shown that drug abusers are risk prone, as
evidenced by self-reports of sensation seeking [12] and behavior in laboratory risk-
taking tasks [13]. Obesity is also associated with greater risk-taking, showing an
association with risky patterns of responses in tasks like the Iowa Gambling Task (IGT)
[14].
Adolescents are known to have a tendency to take more and greater risks than
individuals in other age ranges in many life domains, such as unprotected sex, criminal
behavior, dangerous driving, and experimenting with alcohol and other drugs [15].
Furthermore, adolescents who are reward sensitive and have difficulties in controlling
their behavior appear to be most susceptible to involvement in risky behavior [16].
There is increasing evidence that individual differences in the tendency to overeat are
related to impulsivity, possibly due to increasing reactivity to environmental food-
related cues [17]. Neurocognitive studies have shown that obesity and addiction are
both associated with increased impulsive decision-making and attentional bias in
response to drug or food cues, respectively [18]. Several studies have analyzed
attentional bias in individuals with obesity, but the results have been inconsistent
[19,20]. When participants were tested in a hungry state, no differences were found, but
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when they were satiated at the time of testing, greater attentional bias was found in
excess compared to normal weight adults [21]. However, specific literature on
adolescents is scarce. To the best of our knowledge, only one study has found increased
attentional bias and impulsivity to food cues in adolescent girls, as well as reduced
activation of frontal inhibitory regions [22].
Regarding appetitive motivation, substance use disorders (addiction) and obesity, and
subjective states of craving and hunger, are associated with attentional bias for drug-
and food-related stimuli, respectively [23,24]. Furthermore, previous studies showed
that drug-cue reactivity is positively associated with increases in impulsivity and risk-
taking in substance abusers [25].
Decision making in eating behaviour can be studied by food choices tasks. Food
decisions concern what, when, and how much to eat. Food choices can lead to
overconsumption, when there is an increased preference for appetizing food (high in fat
and/or sugar). Therefore, the study of decision making is extremely important in this
population, since decision making based in unhealthy choices can lead to weight more
gain and develop or maintain obesity.
This study examined the effect of exposure to food pictures, in a food-choice task, on
subsequent measures of risky decision-making and hunger levels in adolescents with
excess versus normal weight. Risk seeking was assessed through the Balloon Analogue
Risk Task (BART). Riskiness on the BART was related to self-reported engagement in
real-world risk-taking behaviours [26]. To study the influence of exposure to food
pictures, performance on the BART and feelings of hunger were evaluated both before
and after the food choice task. We hypothesized that adolescents with excess weight
would show greater risky decision-making after exposure to food pictures, while no
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change was expected in normal weight adolescents. We expected to find greater
increases in hunger levels after the food-choice task in excess versus normal weight
participants. Finally, we expected to find more food-appetizing choices among excess
weight adolescents, as well as associations between impulsivity measures, hunger levels
and risk-taking outcomes.
2. Methods
Participants
In total, 56 adolescents (24 males and 32 females) aged between 13 and 18 years
participated in the study. They were selected based on their age adjusted body mass
index (BMI) percentile in accordance with the guidelines of the International Obesity
Task Force [27] criteria: normal weight participants (n=29), with age-adjusted BMI
values in the range between the 5th and the 84th percentile, and excess weight
participants (n=27), with age adjusted BMI values above the 85th percentile. However,
the participant of higher weight in the normal weight group has a percentile of 70.
Socio-demographic, BMI, waist-hip ratio and fat percentage data are displayed in Table
1. Participants were recruited from high schools located in Jaén (Spain). The inclusion
criteria were: (i) aged between 13 and 18 years; and (ii) no history of neurological or
psychiatric disorders. All participants had normal or corrected-to-normal vision.
Table 1. Participants’ socio-demographic characteristics, BMI, percentage of body fat

and waist-hip ratio.
a b
Excess weight Normal weight t /chi square p
Mean SD Mean SD
a
Age 15.28 1.82 15.43 1.39 -0.36 0.723
b
Sex (%Men/women) 46.7/53.3 36.7/63.3 1.72 0.189
a
BMI 28.33 2.74 20.12 2.05 12.76 <0.001
a
Waist-Hip ratio 0.85 0.05 0.82 0.07 1.69 0.097
a
% Body fat 27.34 7.71 17.90 7.16 4.75 <0.001
a
b
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Instruments
Self-reported measures
- Spanish version of the short UPPS-P impulsive behavior scale [28]: the UPPS-P is a
20-item inventory designed to measure five components of impulsive behavior:
sensation seeking, lack of perseverance, lack of premeditation and urgency (positive and
negative). Each item on the UPPS-P is rated on a four-point scale ranging from 1
(strongly agree) to 4 (strongly disagree). Positive Urgency is defined as the tendency to
act rashly to obtain reinforcement when experiencing positive emotions, while Negative
Urgency refers to the tendency to engage in impulsive behaviours under conditions of
negative affect. Sensation seeking describes individuals' tendency to seek out novel,
complex, and intense sensations and experiences, and a predisposition to take risks to
realise these experiences. Lack of Premeditation refers to the tendency to think and
reflect on the consequences of an act before engaging in that act or taking a decision.
Lack of Perseverance refers to an individual’s inability to remain focused on a task that
may be boring or difficult.
- A visual analogue scale (VAS) designed to rate hunger levels. Participants had to
indicate how hungry they were feeling on a scale ranging from 1 to 10 (not hungry to
very hungry).
Risk-taking task
The BART [29] is a 20-trial computerized task that models real-world risk behavior
according to the concept of balancing the potential for reward and harm [29]. The
participant is presented with a balloon and asked to pump it up by clicking a button on
the screen. With each pump, the participant obtains 25 cents and the balloon increases
slightly in size. However, each balloon also has a concealed probability of exploding
after an unspecified number of pumps. Participants were told that at some point each
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balloon would burst. Before the balloon explodes, the participant can press “Collect
money,” which saves his or her earnings to a permanent bank. If the balloon explodes
before the participant collects the money, all earnings for that balloon are lost, and the
next balloon is presented. Each successful click increases the participants’ temporary
payoff but increases the risk of the balloon exploding. Thus, each pump confers not
only greater risk but also greater potential reward.
In this version of the task, the maximum number of pumps possible for a given balloon
was 128, thus the probability of the balloon exploding on Pump 1 was 1/128. If there
was no explosion after this first pump, the probability of explosion on Pump 2 was
1/127, and so on up until the 128th pump. Accordingly, the average break point or
“optimal stopping point” for each balloon was 64 pumps.
Dependent variables are the average number of pumps of unexploded balloons and the
number of exploded balloons (higher scores indicate greater risk-taking propensity).
Food-choice task
A food preference decision-making task was used in this study. Two types of food
pictures were utilized: appetizing (high levels of fats and/or sugars) and healthy.
Appetizing cues included, for instance, sausages and chocolate and healthy cues
included, for instance, fruits and salads. In each trial, pairs of pictures of these different
types of foods were presented in three conditions (appetizing vs. healthy, appetizing vs.
appetizing and healthy vs. healthy). Participants had to choose between the two options
by pressing a computer keyboard. Each trial begins with a fixation cross which lasts
from 3 to 6 seconds, varying between trials. Then, the images of the two options appear
for 5 seconds (one on the left side of the screen and the other one on the right side of
screen, with the positions of the appetizing and healthy foods varying among trials). The
order of presentation of the images was counterbalanced across the participants. Then,
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the fixation cross was represented. There were a total of 30 choice trials, with 10
choices for each decision category, preceded by four practice trials. The outcome
measure was the number of selections of each type of food.
Procedure
Height, weight and body composition measures (Bodystat®1500 monitoring unit) were
collected on arrival of the participant. Subsequently, the UPPS-P impulsivity
questionnaire was administered followed by the BART (pre-task). Then, participants
performed the food-choice task, and immediately after, the BART was administrated
again (post-task). Subjective hunger evaluation (VAS) was carried out before (and after
UPPS-P) (pre-task) and after completion of the food-choice task (post-task). The Ethics
Committee for Human Research of the Universidad de Jaén approved the study. Both
participants and parents signed informed consent forms.
Group comparisons were carried out with Student t-test for independent samples. BART
and hunger measures were analyzed by repeated measures ANOVA with Time (pre- and
post-task) as the repeated-measures factor and Group (Excess vs. Normal weight) as the
between-subject factor. Additionally, we have carried out ANCOVA analyses including
the covariables of Sensation Seeking and Positive Urgency in order to assess the
influence of these variables on the pre- to post- change. Associations between variables
were analyzed by Pearson correlations. Finally, mediation analyses were performed
with the PROCESS macro for SPSS. To assess the significance of partial mediation
effects, confidence intervals from the bootstrapping estimation techniques were used.
For a significant meditational effect, the limits of confidence interval should not include
the 0 value [30, 31]. In order to simplify these analyses, change scores were calculated
as the post-task value minus the pre-task value.
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3. Results
Self-reported measures
The groups differed in two dimensions of the impulsivity questionnaire (UPPS-P),
sensation seeking (t=2.17, p=0.034, δ=0.58) and positive urgency (t=2.14, p= 0.037,
δ=0.56), with greater scores in the excess versus normal weight adolescents (Table 2).
A Time x Group interaction was found for hunger VAS scores (F1,54 = 8.56, p =0.005,
𝜂𝜂𝑝𝑝2 =0.14). Although both groups showed significant increased hunger levels, the
increase from the pre- to post-task evaluation was greater in excess weight (F1,26= 33.72,
p<0.001, 𝜂𝜂𝑝𝑝2 =0.57) versus normal weight adolescents (F1,28=17.37, p< 0.001, η2p =0.38)
(Table 2).
Additionally, results of ANCOVA showed that Sensation Seeking had a significant
effect on the change in hunger levels in the whole sample (F1,53= 4.13, p=0.047,
𝜂𝜂𝑝𝑝2 =0.072). Furthermore, a Sensation Seeking x group x time (F1,53= 8.40, p=0.001,
𝜂𝜂𝑝𝑝2 =0.241) interaction was found. In order to analyze this interaction we explored the
effect of the covariable in each group separately. Sensation Seeking influenced the
change in hunger levels in the excess weight group (F1,25 = 7.97, p=0.009, 𝜂𝜂𝑝𝑝2 =0.242),
but not in the normal weight group (F1,27= 0.03, p=0.869, 𝜂𝜂𝑝𝑝2 =0.001). Regarding food
choices, excess weight adolescents chose significantly more appetizing foods than
normal weight adolescents (Table 2).
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Table 2. Means and standard deviations (SD) of impulsivity (UPPS-P), hunger (VAS)
measures, appetizing and healthy choices. Results of the group comparisons (t and p)
are also displayed.
Excess weight Normal weight t p

Mean SD Mean SD
UPPS-P Urg- 11.89 8.65 10.90 3.44 0.57 0.570
UPPS-P Urg+ 9.96 2.12 8.86 1.73 2.14 0.037
UPPS-P SS 11.19 2.63 9.62 2.74 2.17 0.034
UPPS-P LPrem 8.37 1.94 8.24 2.59 0.21 0.835
UPPS-P LPers 7.63 2.10 8.31 2.56 -1.08 0.284
UPPS-P Total 46.04 9.63 47.03 8.09 -0.42 0.676
Hunger Pre 1.35 1.48 2.35 2.26 -1.94 0.057
Hunger Post 4.94 2.62 3.88 2.77 1.48 0.144
A_Choices 7.11 2.06 4.38 2.53 4.41 <0.001
H_Choices 2.89 2.06 5.62 2.53 -4.41 <0.001
Note: Urg-: Negative Urgency; Urg+: Positive Urgency; SS: Sensation Seeking; LPrem: Lack of Premeditation; LPers:
Lack of Perseverance; A_Choices: appetizing choices; H_Choices: healthy choices
Risk-taking task (BART)

Significant Time x Group interactions were found for the average number of pumps of
unexploded balloons (F1,54= 5.68, p=0.021, 𝜂𝜂𝑝𝑝2 =0.10) (Fig 1) and exploded balloons
(F1,54= 7.38, p=0.009, 𝜂𝜂𝑝𝑝2 =0.12) (Fig 2). The average number of pumps of unexploded
balloons (F1,26= 14.57, p=0.001, 𝜂𝜂𝑝𝑝2 =0.36) and exploded balloons (F1,26= 6.33, p=0.018,
𝜂𝜂𝑝𝑝2 =0.20) increased in excess weight adolescents after the food-choice task, while no
significant changes were observed in normal weight adolescents (p>0.23). While no
group differences in the BART were observed in the pre-task evaluation (exploded
balloons: p=0.855; average number of pumps on unexploded balloons: p=0.702), the
above-described differential responses to the food choice task led to increased risk-
taking (exploded balloons) in the excess versus normal weight adolescents during the
post-task evaluation (t=2.43;p=0.019; δ =0.67).
The inclusion of Sensation Seeking and Positive Urgency as covariables in these
analyses did not change the above results.
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Fig 1. Average Number of Pumps on Unexploded Balloons in the Pre-Task and Post-
Task evaluations as a function of group.
Fig 2. Number of Exploded Balloons in the Pre-Task and Post-Task evaluations as a
function of group.
Associations between measures

In the whole sample (Table 3), the change in hunger levels was positively associated
with the change in the number of exploded balloons, the number of exploded balloons
after the food-choice task and the average number of pumps on unexploded balloons
143
before and after the food-choice task. Sensation Seeking was positively associated with
the change in hunger levels, the number of appetizing choices made in the food choice
task, the number of exploded balloons and the average number of pumps on unexploded
balloons after the food-choice task. Positive Urgency, Lack of Perseverance and UPPS-
P total scores were positively correlated with the number of appetizing choices. Finally,
BMI was positively associated with the change in the number of exploded balloons, the
number of exploded balloons after the food-choice task, Positive Urgency, Sensation
Seeking and the number of appetizing choices.
In the excess weight group (Table 4), the change in hunger levels was positively
associated with the change in the number of exploded balloons, the number of exploded
balloons after the food-choice task, the average number of pumps on unexploded
balloons before and after the food-choice task and sensation seeking scores. Sensation
Seeking was positively associated with the number of exploded balloons after the food
choice task. UPPS-P total scores were correlated with the number of appetizing choices.
Finally, Lack of Perseverance was positively associated with BMI and the number of
exploded balloons before the food choice task. In the normal weight group (Table 5),
Negative Urgency, Lack of Perseverance and UPPS-P Total scores correlated positively
with the number of appetizing choices. Finally, BMI was positively associated with
Lack of Premeditation.
Results of mediation analysis showed that the change in hunger levels mediated the
difference in the number of exploded balloons between the pre- and post-
administrations of the BART in excess weight participants (Bootstrapping Lower Limit
Confidence Interval = 0.04, Bootstrapping Upper Limit Confidence Interval = 0.54),
and not in normal weight participants (Bootstrapping Lower Limit Confidence Interval
= -0.14, Bootstrapping Upper Limit Confidence Interval = 0.06).
144
Table 3. Pearson correlations between variables in the whole sample are displayed.
n=56 Hunger_ UPPSP_ UPPSP_ UPPSP_ UPPSP_ UPPSP_ UPPSP_ BMI

Change T U+ U- SS LPrem LPers
Hunger_change 1 0.05 0.03 -0.00 0.34* 0.01 -0.17 0.25

EB_Change 0.33* -0.13 -0.08 -0.03 0.23 -0.04 -0.16 0.30*
ANPUB_Change 0.08 -0.20 0.09 0.10 0.17 -0.06 -0.22 0.18
EB_PRE 0.20 0.16 0.06 0.22 0.22 0.06 0.25 0.09
EB_POST 0.43** 0.01 -0.02 0.15 0.37** 0.01 0.06 0.33*
ANPUB_PRE 0.28* 0.14 -0.06 0.00 0.18 0.02 0.18 0.11
ANPUB_POST 0.34* -0.06 0.02 0.12 0.28* -0.04 -0.04 0.22
A_Choices 0.24 0.42** 0.36** 0.07 0.27* 0.25 0.29* 0.45**
BMI 0.25 0.04 0.33* 0.09 0.27* 0.16 0.01 1
EB: Exploited Balloons; ANPUB: Average Number of Pumps on Unexploded Balloons; T: total; U+: Positive Urgency;
U-: Negative Urgency; SS: Sensation Seeking; LPrem: lack of premeditation; LPers: lack of perseverance; A_Choices:
appetizing choices; BMI: Body Mass Index
** Correlation is significant at the 0.01 level (2-tailed)
* Correlation is significant at the 0.05 level (2-tailed)
Table 4. Pearson correlations between variables in excess weight group are displayed.
Normal weight Change T U+ U- SS LPrem LPers
Hunger_change 1 -0.04 -0.03 0.03 -0.03 -0.08 -0.18 0.14

EB_Change -0.14 -0.30 -0.25 -0.28 0.13 -0.15 -0.06 -0.07
ANPUB_Change -0.27 -0.19 -0.14 -0.17 0.29 -0.15 -0.19 -0.24
EB_PRE 0.03 0.27 0.04 0.18 0.07 -0.01 0.13 0.32
EB_POST -0.10 -0.02 -0.19 -0.09 0.19 -0.14 0.06 0.24
ANPUB_PRE 0.10 0.04 -0.14 -0.07 0.01 -0.06 0.09 0.27
ANPUB_POST -0.04 -0.11 -0.21 -0.16 0.18 -0.18 -0.09 0.06
A_Choices -0.15 0.51** 0.32 0.43* 0.10 0.22 0.57** -0.18
BMI 0.14 0.26 0.12 -0.06 0.12 0.37* 0.20 1
145
Table 5. Pearson correlations between variables in normal weight group are displayed.

Excess weight Change T U+ U- SS LPrem LPers
Hunger_change 1 0.14 -0.11 -0.05 0.49** 0.07 -0.11 -0.30

EB_Change 0.46* 0.03 -0.16 0.02 0.16 0.03 -0.18 0.06
ANPUB_Change 0.14 -0.19 0.14 0.21 -0.17 0.06 -0.17 -0.14
EB_PRE 0.32 0.07 0.08 0.26 0.38 0.15 0.42* -0.01
EB_POST 0.60** 0.07 -0.07 0.21 0.41* 0.15 0.17 0.04
ANPUB_PRE 0.43* 0.26 -0.01 0.03 0.38 0.15 0.33 -0.01
ANPUB_POST 0.48** 0.02 0.08 0.26 0.27 0.16 0.14 -0.15
A_Choices 0.24 0.57** 0.20 -0.17 0.23 0.36 0.20 0.22
BMI -0.30 0.12 0.22 0.08 0.01 0.17 0.39* 1
4. Discussion
Results showed that after the food-choice task adolescents with excess weight displayed
increased values in the two risk-taking measures of the BART than adolescents with
normal weight. Adolescents with excess weight also showed a greater increase in
hunger levels (VAS scores) after exposure to the food-choice task. Furthermore, excess
weight adolescents showed greater scores in Positive Urgency and Sensation Seeking
(UPPS-P), as well as an increased number of appetizing selections in the food-choice
task, compared to normal weight adolescents. Finally, significant associations were
found between the change in hunger feelings, risk-taking and impulsivity measures.
Food-visualization effects on risk-taking

Our findings suggest that adolescents with excess weight have enhanced reactivity to
food cues, since the food-choice task led to an increase in risk-taking in these
individuals. Yeomans and Brace (2015) [32] showed similar results in a study
comparing restrained versus overeating-susceptible healthy women selected according
to their scores in on the disinhibition and restraint scales of the Three Factor Eating
146
Questionnaire (TFEQ) [33]. They found that exposure to food cues led to a greater risk
propensity (measured with the BART) in women susceptible to overeating in
comparison with restrained women. However, they found group differences in BART
measures both before and after food cue-exposure, while we only observed differences
after the food-choice task. The pre-task discrepancy may be due to differences in the
studies samples, as they selected their sample based on uncontrolled eating (TFEQ),
while we selected ours based on BMI.
To our knowledge, this is the first study to analyse the influence of food cues
visualization on risk-taking in adolescents with excess weight. The fact that excess
weight adolescents increase risky decision-making after food exposure may be relevant
to our understanding of the role of food cues in the development of unhealthy eating
behaviours in modern societies. Motivational mechanisms could be involved in food
cue-enhanced risky decision-making. In general, it is known that positive mood states
induce increased risk-taking [34], which in turn promotes further gratification-seeking
behaviour to maintain a positive mood. For example, undergraduate college students are
more likely to drink on days of celebration than during the week [35], and individuals
may also engage in risky drinking to enhance a pre-existing positive mood [36]. This
hypothesis is in line with our results of greater positive urgency (reward seeking under a
positive mood) in excess weight adolescents. In line with this result, Fernández-Serrano
y cols. (2011) [37], using the Iowa gambling task (IGT) in polysubstance users, found
that drug-users (who showed a risky pattern of decision-making under normal
conditions) decreased their risk-taking in a negative affective context (visualization of
negative images while performing the IGT) to a level similar to that observed in
controls, while they increased their risky decisions on the IGT during a positive
affective context evoked by drug cue visualization.
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Food-visualization effects on hunger levels and its associations with risk-taking

The food-choice task led to a greater increase in hunger feelings in excess weight group.
Food cues could be associated with greater reward value in adolescents with excess
weight than in normal weight adolescents. Evidence points to greater neural reactivity in
the reward system in obese versus normal weight individuals during high-calorie food
visualization [38]. Therefore, appetizing food cues may evoke an approach response to
reward, leading to greater hunger feelings and enhanced impulsive risk-taking
behaviours [39]. In fact, in our study, a greater number of appetizing choices in the
food-choice task were found in excess versus normal weight adolescents. Therefore, this
purported greater underlying reactivity to appetizing food cues in obese individuals may
mediate the observed impulsive behaviour after food visualization.
Furthermore, we found a positive association between risk-taking (greater number of
exploded balloons and average number of pumps on unexploded balloons) and the
change in hunger levels in the whole sample and in the excess weight group
particularly, but not in the normal weight group. Besides, the change in hunger levels
was also positively associated with the average number of pumps of unexploded
balloons after the food-choice task in adolescents with excess weight. Therefore, food
visualization and the consequent increase in hunger lead to enhanced risk-taking in
excess weight adolescents, what may cause alterations in impulses control and hinder
the intake control. Furthermore, subjective hunger may predispose an individual to
believe that his/her body is in a state of homeostatic imbalance that must be restored
through the intake of food. This may increase the predisposition to overeat in current
society, given the ubiquitousness of full of fatty/sweet food cues. Therefore, these
results suggest that greater hunger feelings may predispose to enhanced risk-taking in
148
excess weight adolescents, which can lead to greater seeking of the reward
consumption, in this case appetizing foods high in fats and / or sugars.
Impulsivity measures and its associations with hunger levels and appetizing choices
Excess weight adolescents showed greater scores in Positive Urgency and Sensation
Seeking than normal weight adolescents. Available evidence concerning impulsivity
traits in obese adolescents is scarce. In the two studies available on adolescents with
excess weight, no groups differences in impulsivity were found [7, 40]. As a possible
explanation for these differences versus the current study, the mean age of the excess
weight participants in these previous studies was 14.19±1.38 and 14.22±1.4 years, lower
than that in our study (15.28±1.82 years). The mean age of our study is characterized by
greater freedom and less control by parents, so it is more likely that adolescents around
this age develop behaviours such as searching for new experiences or immediate
rewards. For example, significant relationships between sensation seeking and
adolescent alcohol use, cigarette smoking and marijuana use have been reported, with
older adolescents being more likely to engage in these types of risky behaviours [41].
Conversely, Nazarboland and Fath (2015) [42] found greater Sensation Seeking in
highly obese adolescents (BMI>35) than in normal weight adolescents.
Sensation Seeking was positively associated with the change in hunger levels in excess
weight participants. Furthermore, this variable mediated the difference in hunger levels
in this group between the pre- and post- food-choice task evaluations. This suggests that
the impulsivity trait may not only be associated with eating preferences, but also with
changes in subjective feelings of hunger, which could stimulate overeating and the
intake of high-calorie foods, leading to obesity.
149
Regarding to this, Sensation Seeking has long been associated with elevated drug intake
in humans (43). Therefore, the influence of Sensation Seeking on a greater increase in
hunger feelings in excess weight adolescents may support the hypothesis of a greater
reactivity to food signals (i.e., increased seeking for rewards and positive reinforcement)
in these participants.
A preference for appetizing food in the food-choice task was associated with
impulsivity measures in our whole sample. Specifically, Sensation Seeking and Positive
Urgency (both related to greater reward sensitivity), which may indicate a mediational
role of impulsivity in determining food preferences. These results corroborate previous
evidence. Davis y cols. (2007) [44] found in women ranging from normal weight to
obese that reward sensitivity was positively linked to overeating and high sugar-fat food
preferences. Nederkoorn y cols. (2010) [45] found that participants with greater
impulsivity gained more weight during a 1-year period. It has been proposed that
impulsivity may accelerate the acquisition of Pavlovian conditioning to appetitive cues
[46]. All of this evidence suggests that exposure to appetitive food cues, via interaction
with impulsivity traits, may play an important role in the development of unhealthy
eating behaviours. In modern societies, given the high availability of, and frequent
exposure to, high calorie foods, individuals with high reward sensitivity are predisposed
to consumption beyond their caloric needs. The enhanced preference for fat-sweet foods
is explained by their greater reinforcing value, especially in individuals with excess
weight [47].
As the incentive salience of appetizing food cues increases, seeking out and consuming
this type of food becomes an important goal, exceeding feeding homeostatic regulation
[48]. This represents a risky behaviour, since consuming foods high in fat and/or sugar
is associated with weight gain in children and adolescents and, therefore, increased risk
150
of obesity [49]. Macchi, MacKew and Davis (2017) [50] assessed eating habits and risk-
taking (BART) in adolescents and found that choices on the BART were riskier in
adolescents who made unhealthier food choices. These findings are congruent with
studies observing that adolescents with higher risk-taking on the BART consistently
engaged in greater risk-taking activities outside of the laboratory, such as smoking,
drinking, gambling or substance abuse [51-53].
Limitations
Regarding limitations of the study, there are a number of issues that need to be
addressed in future studies, like differentiating among obese, overweight and normal
weight participants, the inclusion of objective eating behaviour measures (in the home
and/or the lab), and the fulfilment of a more exhaustive decision-making evaluation.
Furthermore, future studies should evaluate the longitudinal influence of risk-taking on
weight gain. Finally, the lack of a control group not exposed to the food-choice task
manipulation makes it difficult to discern whether the changes in hunger feelings and
decision-making are due to the visualization of food, the mere passage of time or the
repeated administration of the test. Future studies will be necessary to address this
limitation by including an appropriate control group.
Conclusions
In summary, the results showed that excess weight adolescents increased their risky
decision-making after food-choice task exposure, where this was associated with an
increase in hunger levels. Furthermore, adolescents with excess weight displayed
greater scores in impulsivity measures, which were positively associated with the
number of appetizing choices in the food-choice task. Excess weight in adolescence is a
risk factor for the development of future health problems and obesity. In current western
societies, given the high availability of, and exposure to, high-calorie foods, decision-
151
making has become a crucial factor in maintaining healthy eating habits. Since risk-
taking is more prevalent in adolescence, it may be important to empower adolescents to
make healthy decisions to prevent future obesity. Impulse control and decision-making
should be an important target to prevent risky eating behaviour in adolescents.
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Capítulo 9. Increased food choice-evoked brain activation in
adolescents with excess weight: relationship with subjective
craving
Moreno-Padilla, M., Verdejo-Román, J., Fernández-Serrano, M. J., & Reyes del Paso,
G., Verdejo-García, G. (2018). Increased food choice-evoked brain activation in
adolescents with excess weight: relationship with subjective craving. Appetite. Under
review.
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Capítulo 9. Increased food choice-evoked brain activation in adolescents with excess weight: relationships with
subjective craving
1. Introduction
The prevalence of adolescent overweight and obesity has steeply increased over the last
two decades, reaching epidemic levels (1). In most cases, overweight and obesity are the
result of food choices characterized by high calorie intake. When these choices are
consolidated at an early age, obesity is more severe and associated with worse long-term
consequences (2).
Although food consumption is an essential human behaviour, factors that regulate
dietary choices are complex and poorly understood. Food intake is influenced by a
variety of factors besides homeostatic regulation, like sensory cues (e.g., taste, smell,
texture and appearance), availability, motivational and affective states, pleasure seeking,
etc. All of these aspects influence what, and how much, humans eat even when they are
satiated. These factors are associated with specific patterns of regional cerebral blood
flow (rCBF), particularly within brain regions commonly implicated in motivation,
emotion, memory, and behavioural control (3).
Previous studies have demonstrated that brain activation in response to food pictures is
a useful measure to examine both sensitivity to food cues and vulnerability to the
development or maintenance of overweight (4, 5). High-fat foods evoked activation in
brain regions associated with reward value processing (e.g. dorsal/ventral striatum,
orbitofrontal cortex [OFC]), as well as with the representation of internal body states
such as hunger (insula) (6, 7).
Comparisons of rCBF between obese and normal-weight individuals have shown
differential responses to food cues associated with weight status (6, 8, 9). Obese
individuals show greater activation to food cues in comparison to normal-weight
participants in multiple brain regions, including reward system-related ones, like the
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prefrontal cortex (PFC), OFC, anterior cingulate cortex (ACC), insula, amygdala, and
striatum during hunger states (10); the PFC, caudate, hippocampus, and temporal lobe
immediately after eating (8); and the striatum, insula, hippocampus, and parietal lobe
during neutral appetitive states (neither hungry or satiated) (6). In addition, differential
activation to food types (high- and low-calorie) has also been examined in relation to
weight. The majority of reported results of direct comparisons between normal-weight
and obese/overweight groups indicate greater activation in response to high-calorie food
cues in similar brain regions among overweight/obese individuals (6, 8, 10).
Another way to study brain activation during eating behaviour is by using food choice
paradigms. Food decisions concern what, when, and how much to eat. Food choices can
lead to overconsumption, when more energy is consumed than expended. The brain
mechanisms underpinning food choices have been examined in neuroimaging studies.
Several neural processes are involved in feeding behaviour. Firstly, the visual system is
very important to guide food selection. Inputs from the visual system elicit a specific
pattern of brain activation related to preparation for food ingestion, which evokes the
desire to eat, as well as cognitive processes such as memory retrieval and hedonic
evaluation of the specific food (11, 12). Secondly, visual food cues activate the reward
neural circuitry (e.g., PFC, OFC, amygdala, dorsal and ventral striatum, hypothalamus,
and insula) (10). Moreover, high-calorie food cues specifically elicit a greater response
in these regions relative to low-calorie food images (13, 14).
Recent theoretical models highlight that decision-making skills are a key factor in
controlling caloric intake in modern environments, since these are characterized by open
access to food and strong media-driven appeals to eat high-calorie food (15). Decision-
making skills are particularly pertinent in the case of adolescents, in whom transitions in
brain development appear to be geared towards maximizing reward at the expense of
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risk (16). Neuroimaging studies have confirmed that adolescents have hypersensitive
striatal responses to reward prediction (17, 18) and high activation of brain areas
implicated in the promotion of risk-taking (OFC) during decision-making (19).
However, the neural correlates of food choices in adolescents have been less well-
studied. This matter is particularly important, as the probability that an obese adolescent
develops into an obese adult is much higher than that of a normal-weight adolescent
(20). Moreover, once people have become overweight or obese, it is quite difficult for
them to regress to a stable healthy weight. The important increase in the prevalence of
obesity in children and adolescents, the complications of overweight / obesity for health
and the greater tendency to continue being overweight or obese in adulthood make
prevention of obesity the alternative of choice and the optimal strategy to stop the
spread of the obesity epidemic.
In this study, we used functional magnetic resonance imaging (fMRI) to assess brain
regions associated with food choices between appetizing (i.e., high sugar, high fat) and
plain food in adolescents with excess weight (i.e., overweight and obese) versus normal
weight. We also aimed to evaluate the association between choice-evoked brain
activation and subjective self-reported food craving. We hypothesized that excess
weight participants, in comparison with the normal weight ones, would show greater
neural responsiveness in the corticolimbic reward system during food choices between
appetizing and plain foods (i.e., OFC, ACC, insula, ventral striatum and amygdala). We
also hypothesized that this choice-evoked activation in these areas would correlate with
food craving in the excess-weight group.
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2. Methods
Participants
Seventy-three adolescents (age range: 14-19 years) participated in the study. They were
classified into two groups, excess weight [n=38] (27 adolescents with obesity and 11
adolescents with overweight) or normal weight [n=39], according to their age- and sex-
adjusted body mass index (BMI) percentile, following the International Obesity Task
Force (IOFT) criteria (21). There were no significant differences in age or sex between
groups. Demographic and body composition data are summarized in Table 1.
The recruitment of participants was carried out throughout the province of Granada
(Andalusia, Spain) in hospitals and high schools, as well as via press and radio
advertisements. The inclusion criteria were defined as follows: (i) aged between 14 and
19 years; (ii) BMI percentiles falling within the intervals categorized as overweight or
obesity (≥85: Excess weight group), or normal weight (5 to 84: Normal weight group);
(iii) absence of any history or current evidence of neurological mental disorders as
assessed via interviews with participants and their parents; (iv) absence of any history or
current evidence of eating disorders (e.g., binge eating, bulimia nervosa, anorexia
nervosa) assessed with the Eating Disorders Inventory-2 (EDI-2) and (v) absence of any
contraindication to undergo the fMRI session (i.e. metal prosthesis or claustrophobia).
All participants had normal or corrected-to normal vision.
The study was approved by the Ethics Committee for Human Research of the
Universidad de Granada. Both the participants and their parents signed an informed
consent form.
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Table 1
Socio-demographic characteristics, BMI and percentage of fat for each group.
tc/chi p-value
Excess weight (n=38) Normal weight (n=39) squared
Mean (SDb) Mean (SD)
Age 16.47 (1.66) 16.58 (1.36) -0.30c 0.768
Sex (%men/women 47.37/52.63 48.72/51.28 0.00d 0.991
a
BMI 29.89 (3.72) 21.36 (2.07) 12.58c < 0.001
Fat (%) 29.03 (10.28) 15.61 (7.39) 6.56c < 0.001
a:
Body Mass Index; : Standard Deviation; : value of Student’s t; : value of Chi-square χ2
b c d
Procedure
This study consisted of two sessions. In the first session, all participants were pre-
exposed to foods in a catered tasting session conducted 1 week before scanner
acquisition. The participants tasted all foods included later in the fMRI task in order to
become familiar with the specific foods (and their corresponding flavours, textures and
sizes) that were going to be used in the fMRI tasks. The purpose of the tasting was to
establish a context closer to real life in the food choice task. Then, they had to rate the
different foods on a 1- to 10-point self-report scale indexing how much they liked each
meal.
In the second session, we conducted the fMRI task. When participants arrived at the lab,
we used an automated scale (Tanita BC-420 GP Supplies Ltd., London) to measure their
weight and body fat percentage. Body fat percentage was estimated via Bioelectrical
Impedance Analysis. All of the sessions were carried out at the same time of day (4
p.m.), and always fMRI tasks were carried out between one and three hours after lunch.
The teenagers finished their lessons in the high school about 2.30 p.m., after that they
took lunch and at 4 p.m. they started the session. Given the study had a larger protocol
that included more measures assessed before fMRI, participants usually started the
fMRI tasks at about 5 p.m. Just before the fMRI session, before beginning the task
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inside the scanner, and after finishing the fMRI session, participants rated their hunger
from 0 to 100 points on a visual analogue scale in response to the question of “how
hungry are you now?”
fMRI task
A food preference decision-making task was used. The food pictures used in the task
were taken earlier in the tasting session. All pictures were shot ad hoc for the study
using standardized presentation and lighting conditions. Therefore, all images were
matched for visual properties and serving size (about a portion to all food images).
Three types of food were utilized: appetizing (food with high levels of fats and sugars),
plain (defined as natural food or low in fats and/or sugars) and functional (foods that are
prepared not only for their nutritional characteristics but also to fulfil a specific
function, such as improving health and reducing the risk of disease). Appetizing cues
included, for instance, sausages, chocolate, cake, cheese and chips and plain cues
included, for instance, fruits, yoghurt, cereals and salads. In each trial, pairs of these
different types of food were presented to participants (appetizing vs. plain, appetizing
vs. functional and plain vs. functional). Participants were instructed to choose between
these two options taking into account their own preference for one or the other meal.
The question presented was: “If you had to eat one of these foods, which would you
choose?” Each trial began with a fixation cross, which appeared for 4 seconds. Then,
images of the two options appeared for 5 seconds (one on the left side of the screen and
the other one on the right side). The order of presentation of the images was
counterbalanced among the participants. Then, the fixation cross was presented again
(Fig 1). There were a total of 36 choice trials with 12 choices for each decision type.
Participants were instructed to press a button in order to choose the food that they
preferred. Stimuli were presented through magnetic resonance-compatible liquid crystal
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display goggles (Resonance Technology Inc., Northridge, CA, USA), and responses
were recorded with the Evoke Response Pad System (Resonance Technology Inc.).
Participants were instructed to press the button with their thumb if they preferred the
food on the left side, or the button with their forefinger for food on the right side.
According to the objectives of this study, we focused only on the choice between
appetizing food and plain food. The primary behavioral measure was the number of
selections of appetizing and plain foods.
After the fMRI session, participants assessed their "craving" for each food presented
earlier in the scanner on a 9-points scale (1, they did not desire the meal; 9, desired the
meal excessively). Valence and arousal for each meal were also assessed via Self-
Assessment Manikin (SAM) (22). The stimuli were presented using a computer task
programmed using e-Prime software, in which each stimulus was presented on the
screen for 5 seconds. The difference of score between subjective ratings of craving in
response to appetizing versus plain food (referred to as “Appetising vs. Plain Craving”)
was calculated.
Figure 1
Schematic representation of the fMRI task through depiction of the sequence of one
experimental trial
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Imaging data acquisition and processing

A 3.0 T clinical MRI scanner (Intera Achieva; Philips Medical Systems, Eindhoven,
The Netherlands), equipped with an eight-channel phased-array head coil, was used to
obtain a T2*-weighted echo-planar imaging sequence with the following parameters:
repetition time (TR) = 2000 ms, echo time (TE) = 35 ms, field of view (FOV) = 230 ×
230 mm, 96 × 96 matrix, flip angle = 90°, 21 4 mm axial slices, 1 mm gap, 162 scans. A
sagittal three-dimensional T1-weighted turbo-gradient-echo sequence (3DTFE) (160
slices, TR = 8.3 ms, TE = 3.8 ms, flip angle = 8°, FOV = 240 × 240, 1 mm3 voxels) was
also obtained in the same experimental session to discard gross anatomical
abnormalities.
Functional images were analyzed using Statistical Parametric Mapping (SPM8)
software (Wellcome Department of Cognitive Neurology, Institute of Neurology, Queen
Square, London, UK), running on MATLAB R2009 (MathWorks, Natick, MA). Prior to
preprocessing, all images were visually inspected for artifacts. Preprocessing included
reslicing to the first image of the time series, slice timing correction, normalization
(using affine and smooth nonlinear transformations) to an EPI template in Montreal
Neurological Institute (MNI) space, and spatial smoothing by convolution with a 3D
Gaussian kernel (full width at half maximum = 8 mm). No participant was excluded due
to excessive motion, defined as a degree of movement above 3 mm or 3 degrees in
either direction.
Data analysis
Group comparisons of sociodemographic, task, and self-reported variables were
performed with independent-sample t-tests (two-tailed).
For the neuroimaging analysis, the conditions of interest were modelled from the time at
which the food choice was presented to the time at which participants responded.
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subjective craving
Baseline was modelled as the time that the fixation cross was on the screen. Task
regressors were convolved with the SPM8 canonical hemodynamic response function.
The key contrast of interest was “appetizing vs. plain > baseline”, defined in first-level
(single subject) and between-group analyses.
One-sample t-tests were conducted to assess intra-group activations (healthy weight and
excess weight) in the contrasts of interest. Between-group comparisons were conducted
using two-sample t-tests. The statistical threshold used for all fMRI analyses, (i.e: intra-
and between-group analyses) was p< 0.05 false discovery rate (FDR) whole-brain
corrected, with a minimum cluster size extent (KE) of 10 contiguous voxels.
Finally, in order to examine the association between choice-evoked brain activation and
subjective food craving, the peak beta eigenvalues from each cluster of significant brain
differences between groups were extracted for each participant and correlated with the
“Appetising vs. Plain Craving” variable.
3. Results
No significant group differences in preferences for appetizing, plain or functional food,
or in any of the self-reported measures, were obtained (see Table 2).
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subjective craving
Table 2
Means (±SD) of food choices and self-reported measures (tasting, valence, arousal, craving
and hunger).
Excess weight (n=37) Normal- weight (n=36) p-value

Mean (SD) Mean (SD)
Appetizing food
Food Tasting 7.59 (1.09) 7.74 (1.15) 0.571
Valence 6.45 (1.09) 6.58 (1.19) 0.633
Arousal 5.32 (1.63) 5.48 (1.45) 0.657
Craving 5.61 (1.29) 5.75 (1.49) 0.679
Plain food
a
Food Tasting 7.43 (1.06) 7.28 (1.08) 0.552
Valence 6.22 (1.04) 6.2 (1.19) 0.956
Arousal 5.15 (1.43) 5.23 (1.22) 0.801
Craving 5.35 (1.13) 5.26 (1.38) 0.745
Number of Appetizing 14.62 (4.51) 15.64 (4.71) 0.349
choices
Number of Plain choices 14.11 (3.85) 14.28 (3.21) 0.839
%Appetizing-Plain choices 53.24 (20.57) 54.81 (18.97) 0.734
Appetizing vs. Plain 0.26 (0.93) 0.49 (0.73) 0.238
Craving
b
Hunger1 20.69 (21.2) 19.84 (18.9) 0.861
c
Hunger2 18.42 (21.06) 27.7 (24.56) 0.102
d
Hunger3 36.68 (27.67) 46.43 (28.15) 0.156
Brain activation during appetizing vs. plain food choices compared to baseline (fixation
cross)
Both groups show extensive activation in brain regions in response to the appetizing
versus plain food choices, including areas of the frontal cortex (dorsolateral prefrontal
cortex [dlPFC], dorsomedial prefrontal cortex [dmPFC] and ventrolateral prefrontal
cortex [vlPFC]), occipital cortex (visual cortex), and subcortical regions (thalamus,
caudate, striatum, insula and amygdala) (see table S1).
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subjective craving
Differences in patterns of brain activation between excess- and normal-weight
participants
The excess weight group, compared to the normal weight group, displayed increased
activation in the dlPFC (bilaterally), superior temporal cortex (bilaterally),
hippocampus, medial temporal cortex, putamen, superior frontal cortex, thalamus
(bilaterally), globus pallidus, inferior temporal cortex, OFC, ventrolateral prefrontal
cortex, dorsal ACC, insula and dorsal caudate during food choice processing (see Table
3). The normal-weight group had no additional activation versus the excess weight
group in any brain area (see Figure 2).
Table 3
Brain regions that show greater activation in “appetizing versus plain choices > baseline”
in excess weight group than in the normal weight group.
a
Region Side MNI coordinates Ke t-value
X Y Z
b
dlPFC Right 32 34 36 133 4.12
Left -34 44 10 199 5.26
f c
STCx Right 60 -20 2 364 4.58
Left -52 -30 6 131 4.19
d
Hippocampus Right 42 -16 -18 945 4.46
g c
MTC Right 46 -36 2 364 4.37
d
Putamen Right 34 -16 0 945 4.34
h
SFCx Right 10 36 48 241 4.32
d
Thalamus Right 10 -8 2 945 4.3
Left -6 -20 0 152 3.82
GlobusPallidus Left -12 -2 -4 51 4.22
i
ITC Left -60 -4 -18 93 4.15
j e
OFC Right 38 48 -6 182 4.13
k e
vlPFC Right 30 30 -20 182 3.96
l
Rostral ACC Right 6 48 4 91 3.88
ACC Left -10 36 16 96 3.82
Insula Right 40 6 -4 48 3.7
DorsalCaudate Right 12 10 8 23 3.74
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subjective craving
Figure 2
Between-group differences during “appetizing vs. plain > baseline” contrast.
1: dlPFC: dorsolateral prefrontal cortex; 2: Putamen; 3: Insula; 4: vlPFC: ventrolateral prefrontal cortex;
5: OFC: orbitofrontal cortex; 6: SFC: superior frontal cortex; 7: Thalamus; 8: Dorsal Caudate; 9: Rostral
ACC: rostral anterior cingulate cortex; 10: ACC: anterior cingulate cortex; 11: Thalamus; 12: Globus
Pallidus; 13: STC: superior temporal cortex; 14 ITC: inferior temporal cortex.
Association between brain activation and subjective food craving
In the excess-weight group “Appetising vs. Plain Craving” correlated with appetizing
versus plain food choice-evoked activation in the dorsolateral and ventrolateral
prefrontal cortices, ACC, insula, superior/medial/inferior temporal cortices, dorsal
caudate, putamen and thalamus while in the normal-weight group only insula was
correlated with “Appetising vs. Plain Craving” (see Table 4). We performed an FDR
adjustment for multiple comparisons and the regions that remained significant were the
right dlPFC, dorsal caudate and superior temporal cortex only in the excess weight
group.
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subjective craving
Table 4
Correlations between craving scores (Appetizing vs. Plain Craving) and “appetizing
versus plain choices > baseline” brain activation as a function of group. Only areas with
significant correlations are displayed.
Excess weight Normal weight Fisher
Side MNI coordinates p-value r p-value r p
x y Z
b
dlPFC Left -34 44 10 0.04 0.35 0.43 -0.136 0.017
a
Right 32 34 36 0.001 0.53 0.819 -0.04 0.004
c a
TSC Right 60 -20 2 0.003 0.49 0.84 0.035 0.017
d
TMC Right 46 -36 2 0.04 0.34 0.221 0.209 0.274
Putamen Right 34 -16 0 0.01 0.43 0.385 0.149 0.097
e
TIC Left -60 -4 -18 0.03 0.38 0.628 0.083 0.092
f
vlPFC Right 30 30 -20 0.03 0.38 0.388 0.148 0.145
Thalamus Left -6 -20 0 0.02 0.4 0.892 -0.023 0.03
g
ACC Left -10 36 16 0.009 0.44 0.381 0.15 0.089
Insula Right 40 6 -4 0.03 0.38 0.049 0.33 0.405
a
DorsalCaudate Right 12 10 8 0.004 0.48 0.738 0.058 0.025
a
: These results survived FDR correction for multiple comparison;b: Dorsolateral Prefrontal Cortex; c: Temporal
Superior Cortex; d: Temporal Medial Cortex; e: Temporal Inferior Cortex; f: Ventrolateral Prefrontal Cortex; g:
Anterior Cingulate Cortex
4. Discussion
We found that adolescents with excess weight, compared to those with normal weight,
have higher brain activation in frontal, striatal, insular and mid-temporal regions during
choices between appetizing and plain food cues and, furthermore, this activation
correlated with subjective measures of craving. Neural responses in these regions during
food cue exposure in the obese participants were consistent with previous studies (6, 10,
23-25), but there is a lack of studies focused on food choices in adolescents with excess
weight; adolescence is an extremely important life stage, since it can be considered as
the step prior to the development of obesity in adulthood. Furthermore, the context in
which food choices are made is a novel field of research within this population.
Decision making with respect to food choices may be considered the basis of healthy
eating habits.
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subjective craving
During brain activation in our food choice task, we observed significantly increased
neural responses in the excess-weight group in the dlPFC and vlPFC, which are
implicated in cognitive control (26, 27). Research in the decision-making and self-
control literatures points to the particular importance of these regions (28-30). In fact, it
is possible that the greater activation in these areas relates to inhibitory processes in
response to the general belief that high-calorie foods are unhealthy and should be
avoided. This increased activation in the inhibitory system may be a reaction to greater
reward processing, as evoked by the high calorie stimulus (10). This fact may indicate
that in overweight adolescents confronted with appetizing-healthy choices, stronger
top–down control by the dlPFC on subcortical regions is necessary to produce the
appropriate behavioural control (31). In fact, our findings are consistent with Davids y
cols (2010) (25) who also found increased activation of dlPFC to food cues in obese
children and also explained this fact as a greater inhibitory control effort. Therefore, the
greater inhibitory control may be the cause of the lack of group differences in
behavioural measures. Furthermore, adolescents with excess weight may present a bias
regarding their eating choices, since adolescents are more susceptible to social
desirability because of the importance given to their peer’s opinions. Social desirability
has been described as a tendency to overestimate desirable traits and behaviors and
underestimate undesirable ones, when using self-reported measures (32). Among
children and adolescents, socially desirable responding is considered part of normal
development (33). In this case, adolescent with excess weight may think that to choose
appetizing food cues is frowned upon due to his body image and, therefore, they end up
choosing the healthy option. Klesges y cols, (2004) (34) reported that participants
underestimates of sweetened beverage preferences and lower ratings of weight concerns
and dieting behaviors were related to social desirability.
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subjective craving
Another part of the PFC showing increased activation in our excess weight group was
the OFC. This area plays an important role in food-related neural circuitry and responds
preferentially to high-calorie food cues (6, 10). The OFC integrates multiple sources of
information regarding reward outcomes to derive a value signal. According to
Grabenhorst and Rolls (2011) (35), the reward value is ‘passed’ onward from the OFC
to higher cognitive regions such as vlPFC, dlPFC and ACC. Regarding our results,
increased activation in the OFC in excess weight adolescents may indicate greater
processing of high-calorie food cues in terms of reward. The ACC, which was also
more activated by the appetizing versus healthy food choice in our study, is thought to
integrate this reward value with information about planned or anticipated actions and
associated costs (35).
On the other hand, the excess weight group showed increased activation in the insula.
The insula and OFC are interconnected as the primary and secondary gustatory cortex.
A large number of studies found that insula is involved in craving (36), with specific
reactivity to visual food cues, as well as anticipation and consumption of foods in obese
individuals (37), and environmental drug cues in drug abusers (38). These results are in
accordance with previous studies (13, 14, 39) showing the involvement of temporo-
insulo-opercular and orbitofrontal networks in food processing. Furthermore, Yoku, Ng
and Stice (2011) (40) found that youth who showed elevated reward circuitry
responsivity, specifically in OFC, during appetizing food cue exposure were at
increased risk for weight gain.
Finally, we found greater activation in the dorsal striatum (caudate and putamen) in the
appetizing versus plain food choice. This area is a part of the habit learning system,
which has previously been linked to lowered dopamine D2 receptor availability in obese
(41) and drug-addicted individuals (42-46).
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subjective craving
The reward deficiency theory has been advanced to clarify how a baseline hypo
functioning dopamine system may lead to compulsive intake of substances of abuse, as
individuals attempt to self-medicate via direct manipulation of neurotransmitter levels
(47). This model has also been proposed for individuals with excess weight, similarly
self-medicating by overconsumption of high-fat/high-sugar foods (47-49). Dopamine is
involved in encoding the pleasure associated with food intake. Highly appetizing foods
and drugs of abuse directly affect the mesolimbic system, with consumption of each
type of substance increasing dopamine levels (50, 51). The incentive-sensitization
model of obesity posits that repeated pairings of reward from food intake and cues that
predict impending food intake result in a hyper-responsivity of dopamine-based reward
circuitry to food cues, contributing to craving and overeating (52). Therefore, in our
study, food choice-induced anticipation of palatable food can elevate activity in the
fronto-limbic circuitry, thought to correspond to striatal dopamine release (50, 53).
In general, our findings showed greater brain reactivity to food cues in adolescents with
excess weight. Neural food cue reactivity as indexed by fMRI has been shown to be
prospectively associated with food choice (54, 55), snack consumption (5), future
weight gain in adolescent girls (40), and women (56), weight status in women (57) and
outcome in a weight-loss program (58). Therefore, our findings may be extremely
relevant to appropriate decision-making of food consumption. In fact, there are already
preliminary results that show that regional brain activity elicited by food cues of high
incentive salience is reduced during ‘motivational neurofeedback’, in which participants
receive real-time feedback of this activity through changes in the cue’s visible size, also
showing a significant reduction of hunger after successful downregulation (59).
As a second result, we found a positive relation between the variable “Appetizing vs.
Plain Craving” and brain activation in the food choice task only in the excess weight
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subjective craving
group. This result might imply that the desire and subjective value that excess weight
adolescents give to food cues is important, and related to the cognitive processing that
they engage in when choosing between appetizing and plain food cues. This outcome is
consistent with the results of Jastreboff y cols. (2013) (60), who found that in obese but
not lean individuals, food craving correlated positively with neural activity in
corticolimbic-striatal brain regions during presentation of favourite foods. It seems that
it is not only people with obesity show greater food reactivity and subsequent craving,
but also overweight (without reaching obesity levels). On the other hand, in a food
choice processing, normal weight adolescents seem to give less importance to the
subjective value of food cues given their lack of associations between craving and brain
processing. However, there are no differences in behavioral craving between groups.
This fact may be due to the social desirability as we have commented previously. In a
recent systematic review, Boswell and Kober, (2016) (61) demonstrated a robust
prospective and predictive relationship between measures of food cue reactivity,
including the conscious experience of craving and subsequent food-related outcomes.
Overall, their results suggested that food cue reactivity and craving explained a
substantial amount (7–26%) of the variance in food-related outcomes. The abundance of
food and food cues in the modern ‘toxic food environment’ may function as conditioned
stimuli that serve as triggers for increased food consumption and can lead to weight
gain on a population level (62-64).
All of our results support the “food addiction model”. Brain areas showing food-
craving-related activation in this study have been reported to be activated in drug
craving studies. The relationship between the dorsal striatal network and food craving
was significant in the overweight group in this study, in accordance with the notion of
an addictive dimension of obesity. Moreover, we found a positive relationship between
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subjective craving
dlPFC activation and craving, which may suggest that participants who require more
inhibitory control during the appetizing-plain food choice show more craving for this
high-calorie food (and hence there is a need for greater control). In summary, a bunch of
regions seems to be involved in the experience of affect or emotion, memory, higher-
level processing of chemosensory stimuli, and the establishment of incentive salience.
However, there are several limits to these similarities between drug and food addiction
that should be addressed in upcoming investigations.
The main conclusion of this study is that adolescents with excess weight have increased
activation in several regions involved in reward and emotional salience when they are
faced to choose between appetizing versus plain food. The results also suggest that
adolescents with excess weight ascribe greater importance to the incentive value of
appetizing food, since subjective craving correlated with the brain regions activated
during food choices, although no differences in behavioral craving were found between
groups. The difference between groups in relation to craving was only observed at brain
level.
The findings of the present study have treatment implications. Interventions for obese
adolescents should not solely focus on prominent or physical symptoms, but should also
target basic cognitive control functions and processes related to the emotion-processing
system, such as altered reward-related decision making, to address specific impairments
in patients with excess weight. Our results also show the importance of interventions
focused on strategies to enhance inhibitory control in this population, in order to
improve the outcomes of obesity treatments. The ability to resist temptations and
craving in response to high-calorie food is extremely important to prevent unhealthy
eating behaviors. Cue reactivity and craving to food cues may be directly relate to real-
life behavior, given that their effect on subsequent food-related outcomes is comparable
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subjective craving
with real food exposure. Therefore, to promote a reduction in exposure to food cues in
the environment of adolescents with excess weight could be an important target for
obesity prevention policies.
Furthermore, more research into the neural correlates of food choice may provide better
insight into the effects of age, sex, and weight on food-related decision-making
processes, and provide targets for healthy eating interventions. Since an overweight
child or adolescent has a high probability of developing into an overweight adult,
prevention of overconsumption of unhealthy foods and formation of healthy eating
habits in children is crucial in order to reverse the prognosis.
This study had some limitations, such as the type of contrast that we used (appetizing
and plain food cues vs. baseline), since some of the activations are not specifically
related to decision making. However, this limitation was partially overcome due to the
fact that significant correlations were found with the craving measure. On the other
hand, although we observed clear and extensive differences between our obese and
control samples, because we used a cross-sectional experimental design, it was not
possible to determine whether the observed effects represent the causes or consequences
of obesity. Moreover, it would be interesting if the functional implications of the current
results could be addressed in longitudinal studies. Furthermore, research is needed to
compare the results obtained between participants in fasted and satiated states. Finally,
the effects of the menstrual cycle should be taken into account in future studies, since a
number of studies have reported that brain activation and decision making processes are
modulated by the hormonal stage of the menstrual cycle during exposure to food cues
(65, 66).
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Conclusion
In summary, this neuroimaging study strongly supports the hypothesis of behavioural
studies whereby overeating in obese individuals is triggered by exaggerated reactivity to
stimuli associated with high-calorie foods. It might be expected, for example, that an
exaggerated activation of the reward system in response to high-incentive food cues
would predict weight gain, especially in subjects at risk for obesity. Conversely, the
magnitude of activation in response to high-incentive food cues might discriminate
between those who were subsequently successful or unsuccessful in losing weight
and/or maintaining weight loss. It would be of interest to determine whether the
responsiveness of a hyperactive reward system could be moderated in response to
successful anti-obesity therapy, and whether such neuroadaptation would lead or follow
the weight loss.
Author contributions: MMP and JVR carried out the experiments and analyzed data.
MMP wrote the paper with the contributions and approval of all authors.
Funding: This work was supported by projects grants from the Andalusian Council of
Innovation, Science and Industry (P10-HUM-6635-NEUROECOBE). MMP is funded
by a pre-doctorate scholarship from the University of Jaén.
Disclosures: The authors declare no conflicts of interest.
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IV. DISCUSIÓN,
CONCLUSIONES Y
PERSPECTIVAS
FUTURAS
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Capítulo 10
Discusión
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Capítulo 10. Discusión
Uno de los principales retos del siglo XXI a nivel mundial es el abordaje del problema
de la obesidad. Por tanto, el estudio de los factores que contribuyen a la creciente
prevalencia de este problema es, sin duda, uno de los principales desafíos científicos
actuales. Diversos modelos científicos han postulado que el conocimiento de los
mecanismos de procesamiento cerebral, así como los procesos cognitivos asociados,
puede aportar información muy útil a la hora de explicar la ocurrencia y el
mantenimiento de la obesidad (Rangel, 2013). La revisión de la literatura realizada al
inicio de nuestra investigación nos permitió comprobar la existencia de alteraciones
cognitivas en la población con obesidad, paralelismos con la adicción a drogas, así
como peculiaridades sociales y biológicas propias de la etapa de la adolescencia.
Observamos, sin embargo, que existía un escaso número de estudios sobre aquellos
factores que podrían predisponer y estar asociados con el exceso de peso en la
adolescencia. Partiendo de esta premisa, los objetivos de esta tesis pueden resumirse
principalmente en tres. El primero estaba dirigido a analizar el efecto del estrés social,
muy frecuente en adolescentes con exceso de peso, sobre el rendimiento cognitivo y la
actividad fisiológica asociada a este. El segundo objetivo estaba dirigido a examinar la
influencia de la visualización de una tarea de elección alimenticia sobre la toma de
decisiones de riesgo en adolescentes con exceso de peso, así como analizar la asociación
con variables de impulsividad, el nivel de hambre subjetivo, el tipo de elecciones
alimenticias y el IMC. Por último, el tercer objetivo estaba dirigido al análisis de la
activación cerebral ante una tarea de elección alimenticia en adolescentes con exceso de
peso, así como a estudiar la asociación de esta activación cerebral con el craving
subjetivo reportado por los alimentos mostrados en la tarea.
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Los resultados de nuestros estudios avalaron las hipótesis propuestas: encontramos
diferencias entre los adolescentes con exceso de peso y los adolescentes con normopeso,
en la mayoría de los procesos estudiados.
En relación con nuestro primer objetivo, este se dividió en dos objetivos específicos que
se corresponden con los dos primeros estudios que conforma esta tesis. El primer
estudio consistió en analizar la influencia del estrés social en procesos de atención y
toma de decisiones, mientras que el segundo investigó dicha influencia en el
rendimiento ejecutivo. Los resultados obtenidos en el primer estudio mostraron que el
estrés social produce un efecto perjudicial en el rendimiento atencional en los
adolescentes con exceso de peso, y que, a su vez, este decremento en el rendimiento
estaba asociado a un mayor aumento del cortisol en este grupo. En cuanto al segundo
estudio, los resultados también revelaron un efecto perjudicial del estrés social en el
rendimiento ejecutivo en el grupo de adolescentes con exceso de peso. Además, este
déficit estuvo asociado con una mayor reactividad autonómica en el grupo de exceso de
peso.
En relación con nuestro segundo objetivo, los resultados de nuestro tercer estudio
mostraron que los adolescentes con exceso de peso presentaban mayor cantidad de
elecciones de alimentos apetitosos (altos en grasas y/o azúcares) así como mayor
puntuación en algunas variables de impulsividad como urgencia positiva y búsqueda de
sensaciones. Así mismo, los resultados también manifestaron que la visualización de
imágenes de alimentos impactaba en una mayor toma de riesgos en el grupo de exceso
de peso, así como una asociación positiva entre la toma de riesgos y la cantidad de
alimentos apetitosos elegidos y las variables de impulsividad.
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Por último, en relación a nuestro tercer objetivo, los resultados de nuestro cuarto estudio
mostraron que los adolescentes con exceso de peso tenían mayor activación cerebral en
áreas relacionadas con la recompensa al visualizar una tarea de elección alimenticia. Así
mismo, esta activación estaba asociada positivamente, en el grupo de exceso de peso,
con el craving que mostraban los participantes por los alimentos presentados en la tarea.
En conjunto, estos resultados tienen una serie de implicaciones tanto teóricas como
clínicas que abordaremos a continuación.
1. Implicaciones teóricas
En relación a las implicaciones del primer estudio, los resultados mostraron que los
adolescentes con sobrepeso y obesidad presentan mayor reactividad en respuesta a
estresores sociales, reflejado en un mayor aumento de cortisol, lo que impactaba
selectivamente en sus capacidades atencionales. Por otro lado, nuestros resultados son
particularmente relevantes en cuanto a las asociaciones significativas entre la
reactividad del cortisol y los comportamientos relacionados con la ganancia de peso (Lu
y cols., 2014, van Strien, Roelofs & de Weerth, 2013), y la emergente evidencia que
sugiere que niveles altos de estrés puede predecir longitudinalmente la progresión de la
obesidad (Kubzansky y cols., 2014). Así mismo, el efecto perjudicial del estrés social en
la capacidad atencional también tiene importantes implicaciones ya que otros estudios
han comprobado que las alteraciones individuales en las latencias de respuesta se
asocian longitudinalmente con aumentos en el IMC (Frazier‐Wood y cols., 2014). Esta
noción es consistente con nuestro hallazgo de correlaciones significativas entre una
menor mejoría del rendimiento atencional tras el estresor social en el grupo de exceso
de peso y patrones de alimentación maladaptativos más elevados, como la alimentación
externa, que refleja un sesgo atencional hacia las señales relacionadas con los alimentos.
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Además, tanto el estrés social como el déficit en las habilidades atencionales están
significativamente asociados con un peor funcionamiento social y rendimiento
académico (Rouach y cols., 2007).
En cuanto a las implicaciones de nuestro segundo estudio, los resultados mostraron, al
igual que en el primer estudio, que los adolescentes con exceso de peso mostraban
mayor reactividad ante el estrés social, y en concreto ante las evaluaciones negativas,
reflejado en una mayor actividad autonómica y mayores niveles de estrés subjetivo.
Además, esta situación de estrés social provocaba un efecto perjudicial en el
rendimiento ejecutivo del grupo con exceso de peso, el cual estaba asociado con la
mayor actividad autonómica durante la fase de evaluación social negativa. Las
implicaciones son similares a las del estudio anterior, pero hemos de añadir que las
funciones ejecutivas son tremendamente importantes en lo que se refiere a control del
comportamiento, por tanto, creemos que estos resultados son cruciales para entender por
qué el impacto del estrés social puede derivar en un peor control de impulsos y, por
tanto, en una posible sobreingesta. De hecho, los déficits ejecutivos han sido asociados
con comportamientos relacionados con la obesidad en la infancia (mayor ingesta,
alimentación desinhibida, y reducción del ejercicio físico). Por tanto, estos déficits
pueden conllevar que los adolescentes con exceso de peso persistan en sus hábitos
alimenticios no saludables. En conjunto, observamos que el estrés social produce un
efecto perjudicial en el rendimiento cognitivo en los adolescentes con exceso de peso.
En cuanto a las implicaciones teóricas del tercer estudio, los resultados sugieren que los
adolescentes con exceso de peso tienen mayor reactividad a las señales alimenticias, ya
que la tarea de elección alimenticia provoca un incremento tanto en la toma de riesgos
como en los niveles de hambre en este grupo. Además, el grupo con exceso de peso
presentó mayor nivel de impulsividad reflejado en mayores puntuaciones en las
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variables de Urgencia Positiva y Búsqueda de Sensaciones, así como un mayor número
de elecciones de alimentos apetitosos en la tarea de elección alimenticia. Asimismo, se
encontraron en toda la muestra asociaciones positivas entre los cambios en los niveles
de hambre y la toma de riesgos, así como asociaciones con las variables de impulsividad
y el IMC. Hasta nuestro conocimiento, este es el primer estudio que analiza la influencia
de la visualización de señales de comida en la toma de riesgos en adolescentes con
exceso de peso. Además, el grupo de adolescentes con exceso de peso también
mostraron mayor nivel de urgencia positiva, lo que indica una mayor tendencia a la
búsqueda de refuerzos bajo estados de ánimo positivos. Estos resultados están en línea
con los hallazgos de Fernández-Serrano y cols. (2011), los cuales mostraban que los
poli-consumidores de sustancias incrementaban su toma de riesgos en la IGT en
contextos afectivos positivos, como la visualización de señales de drogas. Así mismo,
una mayor preferencia por los alimentos apetitosos en la tarea de elección alimenticia
estuvo asociada positivamente con las medidas de Urgencia Positiva y Búsqueda de
Sensaciones en nuestra muestra. Estos resultados corroboran la evidencia previa de que
participantes con mayores niveles de impulsividad eran más propensos a la sobreingesta
de alimentos altos en grasas y/o azúcares y por tanto a la ganancia de peso (Davis y
cols., 2007; Nederkoorn, Houben, Hofmann, Roefs & Jansen, 2010). Toda esta
evidencia sugiere que la exposición a señales de alimentos apetitosos en interacción con
rasgos impulsivos, puede jugar un importante rol en el desarrollo y mantenimiento de
hábitos alimenticios no saludables. En las sociedades occidentales modernas, dada la
alta disponibilidad y la frecuente exposición a alimentos con alto contenido calórico, las
personas con alta sensibilidad a la recompensa están predispuestas a la sobreingesta,
ignorando sus necesidades calóricas. La mayor preferencia por los alimentos grasos y/o
dulces se explica por su mayor valor reforzante, especialmente en personas con exceso
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de peso. Esto representa un comportamiento de riesgo, ya que el consumo de este tipo
de alimentos está asociado con el aumento de peso en niños y adolescentes y, por lo
tanto, con un mayor riesgo de obesidad (Millar y cols., 2014). Por último, el mayor
incremento del hambre en el grupo con exceso de peso y la asociación positiva entre la
toma de riesgos y los niveles de hambre sugiere que el nivel subjetivo de hambre puede
predisponer a un individuo a creer que su cuerpo está en un “falso” estado de
desequilibrio homeostático que debe restaurarse mediante la ingesta de alimentos.
En cuanto a las implicaciones teóricas del cuarto estudio, los hallazgos aportados por
los patrones de activación durante la neuroimagen indican que los adolescentes con
exceso de peso presentan una mayor activación de áreas relacionadas con la recompensa
(regiones frontales, estriatales, insulares y medio-temporales) ante una tarea de elección
entre imágenes alimenticias, lo que podría indicar una mayor sensibilidad ante las
señales de comida. La mayoría de los estudios que han encontrado mayor activación
cerebral en el circuito de la recompensa durante la exposición a señales de comida se
han realizado en participantes con obesidad (Scharmüller, Übel, Ebner & Schienle,
2012; Connolly y cols., 2013; Rothemund y cols., 2007; Stoeckel y cols., 2008). Por
tanto, nuestros resultados son innovadores ya que muestran un procesamiento cerebral
incrementado en personas con IMCs asociados a sobrepeso, sin tener que llegar a
presentar un IMC asociado a obesidad. Además, la mayoría de los estudios también se
centran en adultos, por lo que hemos abordado de manera más profunda los factores
asociados al exceso de peso en un período tan crítico como es la adolescencia.
Los adolescentes con exceso de peso también mostraron mayor activación en el dlPFC.
Nuestra explicación de este hecho está basada en otros estudios que sugieren que existe
un mayor esfuerzo para redirigir su preferencia alimenticia por lo que utilizan un mayor
control inhibitorio, así como por el concepto de deseabilidad social (Davids y cols.,
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2010; Klesges y cols., 2004). Esto explicaría que no haya diferencias conductuales en
las elecciones alimenticias entre los dos grupos. Por otro lado, la mayor activación en el
OFC que muestran los adolescentes con exceso de peso está asociado, según los
resultados de diferentes estudios, con un riesgo incremento de ganancia de peso
(Yokum, Ng & Stice, 2011). En cuanto a la mayor a activación del estriado dorsal, este
resultado está en línea con los modelos de la auto-medicación o “reward deficiency
syndrome RDS” que proponen que existe un nivel basal más bajo de DA en el sistema
mesolímbico en personas con obesidad, al igual que ocurre en personas adictas a
sustancias, y que resulta en una falta de placer o refuerzo proveniente de actividades que
normalmente si lo proporcionan (Volkow y cols, 1996; 1997; Volkow & Wise, 2005;
Heinz y cols., 2004; Martínez y cols., 2004). Siguiendo este modelo, los alimentos
altamente apetitosos y las drogas de abuso afectan directamente al sistema mesolímbico,
y el consumo de dichas sustancias aumentaría los niveles de DA cerebral conllevando
así un aumento del placer (Small, Jones-Gotman & Dagher, 2003; Rada, Avena &
Hoebel, 2005). Por lo tanto, en nuestro estudio, la anticipación inducida por la elección
de alimentos apetitosos puede elevar la actividad en el circuito fronto-límbico, que se
corresponde con la liberación de DA en el sistema estriatal y así generar un efecto
reforzante. Así mismo, la mayor reactividad cerebral ante señales alimenticias ha sido
asociada de forma positiva con el consumo de snacks entre horas y el incremento de
peso y, de forma negativa con los resultados en un programa de pérdida de peso
(Lawrence, Hinton, Parkinson & Lawrence, 2012; Yokum y cols., 2011; Demos,
Heatherton & Kelley, 2012; Murdaugh, Cox, Cook & Weller, 2012). Por tanto, nuestros
resultados sugieren que el procesamiento cerebral ante señales alimenticias es un factor
extremadamente importante a tener en cuenta en cuanto al control del comportamiento
alimenticio se refiere.
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Un segundo resultado que encontramos en nuestro cuarto estudio fue la asociación
positiva entre la activación cerebral ante la tarea de elección alimenticia y el craving
informado por los participantes con exceso de peso. Este resultado podría implicar que
el deseo y el valor subjetivo que los adolescentes con exceso de peso otorgan a las
señales alimenticias son muy importantes, ya que están estrechamente asociados con el
procesamiento cerebral que realizan ante una tarea de elección alimenticia. Además, la
evidencia sugiere que la reactividad ante las señales de alimentos junto con el craving
explica una cantidad importante de la varianza en los resultados relacionados con las
intervenciones en exceso de peso (Boswell & Kober, 2016), mostrándose como fuertes
predictores en este sentido. Como conclusión, todos estos resultados apoyan el modelo
de “adicción a la comida” basado en los existentes paralelismos entre los mecanismos
neurobiológicos subyacentes en la adicción a sustancias y la obesidad (Volkow y cols.,
2013a; 2013b), aunque es necesaria mucha más investigación en este ámbito.
2. Implicaciones clínicas
Las implicaciones clínicas de nuestros resultados son múltiples y se pueden agrupar en
dos: (i) la contribución que realizan a la comprensión de la importancia de la
intervención en el exceso de peso en la adolescencia, y (ii) las aportaciones que realizan
en cuanto a la mejora del conocimiento de la influencia de las señales alimenticias en
multitud de procesos y, por tanto, su necesaria inclusión en los programas de
intervención.
En cuanto a la primera contribución, derivada de nuestro primer y segundo estudio,
podemos concluir que la presencia y alta frecuencia del estrés social en adolescentes
con exceso de peso puede tener influencias perjudiciales en el rendimiento cognitivo en
esta población y esto puede conllevar al aumento de la ingesta a través de múltiples
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factores (alimentación emocional, falta de control de impulsos, persistencia en los
patrones de alimentación, etc). Por lo tanto, intervenciones basadas en estrategias de
manejo del estrés, así como herramientas alternativas para afrontar las situaciones de
“alimentación emocional” que eviten el uso de la sobreingesta como estrategia de
afrontamiento, son extremadamente importantes de cara a evitar las posibles
consecuencias negativas que el estrés social crónico pueda estar causando en el origen o
mantenimiento del exceso de peso. A su vez, el entrenamiento en habilidades sociales y
de afrontamiento del estrés en situaciones sociales puede mejorar el desempeño social
en esta población y, por ende, mejorar su autoestima y bienestar, así como su
rendimiento académico que como hemos visto anteriormente también se puede ver
afectado negativamente. En segundo lugar, derivado del tercer estudio podemos afirmar
que en los adolescentes con exceso de peso se produce un aumento en sus niveles de
hambre y toma de riesgos después de la visualización de señales de alimentos y, dado
que en la adolescencia la toma de riesgos e impulsividad es mucho mayor, las
intervenciones centradas en este aspecto son fundamentales. Por ejemplo, se podrían
llevar a cabo intervenciones centradas en el entrenamiento de la capacidad para demorar
la recompensa y para aumentar el tiempo que se dedica a decidir, llevando a cabo un
razonamiento más profundo sobre las ventajas e inconvenientes tanto a corto como a
largo plazo de cada elección. De esta manera, los adolescentes podrían llegar a adquirir
las habilidades necesarias para cambiar sus hábitos alimenticios basados en alimentos
que ofrecen una recompensa inmediata por aquellas opciones saludables que ofrecen
una recompensa beneficiosa para su salud más a largo plazo. En general, son necesarios
tratamientos que fomenten la mejora del control del comportamiento, a través de
intervenciones basadas en la mejora de las funciones ejecutivas, ya que creemos que
esto impactará en sus comportamientos alimenticios. Por último lugar, en relación a los
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resultados del cuarto estudio, y teniendo en cuenta las singularidades psicobiológicas
que presenta la etapa de la adolescencia (mayor importancia del sistema hedónico de
recompensa a expensas de las áreas relacionadas con el control ejecutivo), observamos
que en los adolescentes con exceso de peso presentan mayor activación de áreas
relacionadas con la recompensa aunque también presentan mayor activación en áreas
implicadas en el control del comportamiento como es el dlPFC. Este último resultado
implica que los adolescentes con exceso de peso intentan inhibir la conducta no
saludable a nivel cerebral pero que no es suficiente para suprimir finalmente el
comportamiento. Estudios recientes apuestan por la técnica de estimulación transcraneal
con corriente directa (tDCS) como una herramienta eficaz en el tratamiento de la
obesidad. Concretamente, la mayoría de los estudios se centran en la estimulación del
dlPFC como estrategia para reducir el craving por la comida y la consecuente ingesta
(Uher y cols., 2005; Barth y cols., 2011; Forcano, Mata, de la Torre & Verdejo-García,
2018). Como conclusión, los resultados de esta tesis evidencian el papel crítico de la
adolescencia en la aparición y desarrollo del exceso de peso y la obesidad.
El segundo grupo de implicaciones clínicas de esta tesis doctoral se focalizaría sobre la
influencia de las señales alimenticias en los comportamientos relacionados con la
ingesta de alimentos. A través del tercer y cuarto estudio, hemos comprobado la
reactividad que presentan los adolescentes con exceso de peso a este tipo de señales y su
asociación con variables como el hambre, toma de riesgos o craving. Por tanto,
nuestros resultados indican que es necesario implementar intervenciones dirigidas a la
prevención de comportamientos alimenticios no saludables. Por ejemplo, hemos
observado que la reactividad y el craving a las señales alimenticias pueden estar
directamente relacionados con el comportamiento en la vida real, ya que sus efectos en
los resultados posteriores relacionados con el comportamiento alimenticio son
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comparables con la exposición a comida real. Por tanto, consideramos que promover
una reducción en la exposición a señales alimenticias en el contexto de los adolescentes
con exceso de peso debe ser un objetivo cardinal en las políticas de prevención de la
obesidad. De hecho, ya hay resultados preliminares que muestran que la actividad
cerebral provocada por señales de alimentos de alto valor hedónico se reduce durante el
"neurofeedback motivacional", en el que los participantes reciben retroalimentación de
esta actividad en tiempo real a través de cambios en el tamaño de las señales
alimenticias, mostrando una reducción significativa del hambre después de una auto-
regulación inhibitoria del comportamiento (Ihssen, Sokunbi, Lawrence, Lawrence, &
Linden, 2017). Por tanto, nuestros resultados indican que sería adecuado implementar
intervenciones centradas en la auto-regulación inhibitoria del comportamiento del
individuo con el fin de poder adquirir estrategias que permitan resistir a la tentación tras
la visualización de alimentos apetitosos. Así mismo, sería conveniente el desarrollo de
políticas basadas en la reducción de mensajes que promueven el consumo de alimentos
altos en grasas y/o azúcares, así como las señales alimenticias derivadas de esta
publicidad. Esta medida ayudaría a la prevención del desarrollo de la obesidad, y
específicamente, el desarrollo de la obesidad en la adolescencia, una etapa más
vulnerable debido a todos los factores comentados anteriormente.
En resumen, nuestros datos apoyan los resultados de estudios previos (Batterink,
Yokum y Stice, 2010; Nederkoorn y cols, 2006, 2010; Lowe y Fisher, 1983) que
apuntan que la obesidad podría estar relacionada con una mayor reactividad emocional
y un pobre control inhibitorio, y añadimos nuevos resultados como la influencia
perjudicial del estrés social, la mayor toma de riesgos tras la exposición a señales de
alimentos y la asociación entre la activación cerebral y el craving en el grupo de
adolescentes con exceso de peso. En conclusión, consideramos de vital importancia la
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inclusión de intervenciones centradas en la capacitación de los adolescentes con exceso
de peso para el afrontamiento exitoso del estrés, mejora de habilidades ejecutivas y de
control del comportamiento que impacten en una menor toma de riesgos y un
comportamiento alimenticio saludable, estrategias para resistir la tentación ante señales
y alimentos altamente calóricos y, por último, y de forma general, el intento de
reducción de las señales alimenticias de alto contenido calórico en nuestro actual
ambiente.
3. Fortalezas y limitaciones
Uno de los principales puntos fuertes de nuestros estudios es la metodología empleada
para la selección de la muestra. Variables sociodemográficas como el sexo, la edad y los
años de educación se encuentran igualados entre grupos. Además, diversos trastornos
metabólicos (p.ej. diabetes, hipertensión, obesidad mórbida) y psicopatológicos (p.ej.
depresión, y trastornos alimenticios como bulimia o trastorno por atracón) fueron causa
de exclusión de nuestras investigaciones, garantizando que las diferencias encontradas
entre grupos se debieran exclusivamente a los factores analizados y no a otros trastornos
comórbidos. Por último, la gran variedad de técnicas utilizadas (fMRI, registro
psicofisiológico, evaluación neuropsicológica, medidas de autoinforme, etc.) enriquece
los resultados obtenidos.
Estos resultados podrían estar limitados por algunos condicionantes. Por un lado, la
naturaleza correlacional de nuestros estudios no permite inferir causalidad y, por tanto,
otras explicaciones alternativas pueden ser posibles. Otra posible limitación es la
utilización de varias muestras por lo que hay que tener precaución a la hora de trasladar
las conclusiones obtenidas entre los estudios.
205
Capítulo 11
Conclusiones
206
207
Capítulo 11. Conclusiones
A partir de los resultados obtenidos en los distintos estudios de esta tesis, se derivan las
siguientes conclusiones:
1. El estrés social produce un deterioro en pruebas que miden la capacidad
atencional en los adolescentes con exceso de peso. Este deterioro está asociado a
una mayor reactividad psicofisiológica, medida a través de cortisol salival.
2. La evaluación social negativa produce un deterioro ejecutivo (incluyendo
medidas de memoria de trabajo, inhibición y flexibilidad) en los adolescentes
con exceso de peso. Este deterioro está asociado una mayor reactividad
psicofisiológica, medida a través de la tasa cardíaca y la conductancia
electrodermal.
3. Los adolescentes con exceso de peso presentan mayor reactividad a las señales
alimenticias ya que tras su visualización aumenta en mayor medida sus niveles
de hambre y presentan una mayor toma de riesgos. Además, los adolescentes
con exceso de peso presentan mayores puntuaciones en algunos rasgos de
impulsividad, como la Urgencia Positiva y la Búsqueda de Sensaciones, los
cuales están asociados con el aumento del hambre y la toma de riesgos en este
grupo.
4. Los adolescentes con exceso de peso presentan una mayor activación en áreas
cerebrales relacionadas con el circuito de la recompensa ante la visualización de
una tarea alimenticia. Esta activación, en este grupo, se asocia positivamente con
el craving por los alimentos mostrados en la tarea.
En general, nuestros resultados resultan innovadores puesto que contribuyen a señalar
algunos de los factores que pueden estar influyendo en el exceso de peso, además de
señalar la importancia de la intervención en la adolescencia debido a sus características
diferenciales en múltiples aspectos: mayor estrés social, toma de riesgos e impulsividad,
208
Capítulo 11. Conclusiones
además de las singularidades psicobiológicas propias de esta etapa. Todos estos factores
hacen que la adolescencia sea un período crítico a la hora de desarrollar o mantener
problemas relacionados con comportamientos compulsivos, y en particular, con la
sobreingesta de alimentos. De estos resultados también se desprende la importancia de
tener en cuenta las señales de alimentos altamente calóricos (imágenes, anuncios
publicitarios, escaparates, etc.) como elemento disparador de la conducta alimenticia e
incluirlo en los programas de intervención con el fin de promover estrategias para
controlar la tentación derivada de la continua exposición a éstos. Además, dado que los
niños y adolescentes con sobrepeso tienen una alta probabilidad de convertirse en
adultos con sobrepeso, la prevención del consumo excesivo de alimentos no saludables
y la formación de hábitos alimenticios saludables en estas etapas es crucial para revertir
el pronóstico.
209
Capítulo 12
Perspectivas futuras
210
211
Capítulo 12. Perspectivas futuras
Las conclusiones derivadas de esta tesis nos permiten generar nuevas preguntas de
investigación que creemos sería interesante explorar en estudios futuros. Entre ellas
podríamos destacar:
1. Profundizar en el conocimiento de los efectos del estrés social en la conducta
alimenticia de los adolescentes con exceso de peso a través de estudios
longitudinales que permitan el establecimiento de relaciones causales entre
ambos.
2. Evaluar a través de investigaciones más ecológicas si, efectivamente, la
visualización de alimentos altos en grasas y/o azúcares conlleva una mayor
ingesta de estos alimentos, y por tanto impacta en un mayor aumento de peso.
3. Estudiar más profundamente a través de fMRI los correlatos neurales de las
elecciones con alimentos reales. Analizar la actividad cerebral durante todo el
proceso, es decir antes de realizar la elección y cuando se consume el alimento y
observar las diferencias entre un grupo de adolescentes con exceso de peso y
uno con normopeso. Esta metodología permitiría que los resultados obtenidos
fueran más fácilmente transferibles a la vida real.
4. Realizar intervenciones centradas en el craving que presentan los adolescentes
con exceso de peso hacia alimentos altamente calóricos con el objetivo de
controlar la tentación, y ver si las modificaciones en el valor hedónico que se le
otorga a los alimentos tiene consecuencias en el procesamiento cerebral ante la
visualización de éstos.
5. Realizar estudios utilizando la técnica tDCS para intentar reducir el craving a
través de la estimulación repetida del dlPFC mejorando así las capacidades de
autocontrol del individuo; y estudiar la viabilidad de incluir esta técnica en
programas de tratamiento de la obesidad.
212
Capítulo 12. Perspectivas futuras
6. Analizar si a través de un programa de intervención centrado en el afrontamiento
de estrés se producen resultados beneficiosos en los hábitos alimenticios a través
de modificaciones en los comportamientos relacionados con la “alimentación
emocional”. Así la reducción del impacto el estrés social también influiría en la
disminución de los efectos perjudiciales en sí que produce el estrés crónico en la
cognición.
7. Analizar el efecto de los genes relacionados con la transmisión de la dopamina,
en concreto DRD2-A1 y DRD4-7R, en el rendimiento ejecutivo de adolescentes
con exceso de peso. Diferentes estudios han mostrado que padecer obesidad y
tener el alelo DRD4-7R parecer conferir una debilidad en términos de
rendimiento ejecutivo. Sin embargo, los estudios son escasos, con muestra
insuficiente y no están centrados en los adolescentes con exceso de peso.
213
V. DOCTORADO
INTERNACIONAL
214
215
Doctorado internacional
1. Summary
The increase in the obesity prevalence has become, in recent decades, according to
the World Health Organization, one of the main public health problems worldwide.
Obesity is a complex condition in which many factors intervene. In ancient times,
people regulated their intake according to their metabolic states of hunger and
satiety, however, in today's western societies what and how much to eat has become
a decision-making matter. Recent studies suggest that the change in current lifestyle,
based on sedentary lifestyle and unhealthy eating habits, is responsible for the
dramatic increase in the prevalence of obesity.
Excess weight and obesity have also increased exponentially in childhood and
adolescence, critical stages in the development of the individual. Adolescence is a
stage in which the individual is especially vulnerable due to its behavioral
peculiarities. In this stage, behaviours aimed at the reward search and propensity to
risk are frequent, as well as a decrease in executive control and the ability to
regulate behavior effectively. In this regard, various studies confirm the existence of
disturbances in executive functioning in overweight adolescents compared with
adolescents with healthy weight. The executive functions allow a better regulation
of the behavior, and specifically, of the eating behavior.
Furthermore, excess weight in adolescence not only causes negative consequences
at the health level (type II diabetes, higher probability of developing obesity in
adulthood and its harmful medical consequences, etc.) but it is also associated with a
social stress increase due mainly to the frequent teasing referred to their body image
that they receive from their peers and that can even lead to marginalization and
social exclusion. Therefore, adolescents with excess weight suffer greater social
216
stress in their day to day. Numerous studies point to the detrimental effect of stress
on cognitive performance. Also, stress may also alter eating patterns through various
mechanisms.
As we have commented previously, the homeostatic mechanisms have gone to
second place to explain the eating behavior, being the decision-making processes
extremely important in this matter. Specifically, impulsive behavior can play an
important role in obesity during childhood and adolescence. Different studies have
shown that the cues visualization related to drug use produces an increase in
impulsivity levels and induces a greater risk taking, increasing as a consequence the
risk of consumption in individuals addicted to substances. Also, several studies
show that people with excess weight have an attentional bias and greater reactivity
towards food signals high in fats and / or sugars.
Moreover, in recent years, various studies underscore the superimposition of the
neurobiological pathways involved in substance abuse and obesity resulting in the
creation of the concept "food addiction". The drugs of abuse use the same neural
mechanisms that modulate the motivation to consume food; therefore, there is a
parallelism between the brain circuits involved in the loss of control and excessive
food intake that characterizes obesity and compulsive drug use. The alteration of the
dopamine brain circuits is central in these two pathologies. Specifically, the brain
reward system is a central component to develop and monitor motivated behaviours.
Therefore, knowledge of its functioning is vital to better understand the problem of
obesity. During exposure to highly appetizing foods, reward circuit areas may
promote greater dopamine release due to the great salience of the stimulus and thus
lead to a greater predisposition to overeating. It also happens in studies with
populations addicted to substances during exposure to drugs cues. In general, the
217
results of fMRI studies carried out so far point to an increased response in areas of
the reward circuit, both in adults and in overweight adolescents, when processing
food images, especially those with a high fat content and sugars.
Taking into consideration all previous, the objectives of this doctoral thesis were: 1)
study the influence of social stress on neuropsychological performance in
adolescents with excess weight and adolescents with normal weight, 2) analyse the
influence of food cues visualization in a risk decision-making task and its
relationship with impulsivity, in adolescents with excess weight compared to
adolescents with normal weight, y 3) analyse brain processing during food choices
and its relation to subjective craving, in excess weight adolescents and normal
weight adolescents.
To address these objectives, 4 studies were carried out. The results obtained
showed: 1) social stress is associated with worse attentional and executive
performance in excess weight adolescents who also experience greater autonomic
reactivity to this stress compared to adolescents with normal weight (study 1 and 2); studies
2) adolescents with excess weight make more risky decisions after exposure to food
cues and have higher levels of impulsivity than adolescents with normal weight
(study 3); and 3) there is greater activation of brain areas related to the reward
circuit during the exposure to food-choice task in the group of excess weight
adolescents and an association between activation in these areas and the craving
reported by the participants towards the foods presented in the task was found (study
4).
These results could be very useful at a theoretical level, contributing to the
advancement of knowledge of the factors that are predisposing to weight gain in
218
adolescence, as well as to clinical level, promoting new treatments that take into
account neuropsychological and emotional variables that contribute to improve
paediatric interventions aimed at reducing the excess weight problems.
2. Conclusions
From the results obtained in the different studies of this thesis, the following
conclusions are derived:
1. Social stress produces deterioration in tasks that measure the attention capacity
in adolescents with excess weight. This deterioration is associated with a greater
psychophysiological reactivity, measured through salivary cortisol.
2. Negative social assessment produces executive impairment (including measures
of working memory, inhibition and flexibility) in excess weight adolescents.
This deterioration is associated with a greater psychophysiological reactivity,
measured through heart rate and electrodermal response.
3. Adolescents with excess weight have a greater reactivity to food cues since after
their visualization they increase their hunger levels and they present a greater
risk taking. In addition, adolescents with excess weight present higher scores in
some traits of impulsivity, such as Positive Urgency and Sensations Seeking,
which are associated with increased hunger and risk taking in this group.
4. Adolescents with excess weight have greater activation in brain areas related to
the reward circuit when they are exposed to a food task. This activation, in this
group, is positively associated with craving for the foods shown in the task.
In general, our results are innovative since they help to point out some of the factors that
may be influencing excess weight, as well as pointing out the importance of
intervention in adolescence due to its differential characteristics in multiple aspects:
219
greater social stress, risk taking and impulsivity, in addition to the psychobiological
peculiarities of this stage. All these factors make adolescence a critical period when it
comes to developing or maintaining problems related to compulsive behaviors, and in
particular, with overeating. These results also reveal the importance of taking into
account the highly caloric foods cues (images, advertisements, shop windows, etc.) as a
trigger element of eating behavior and include it in intervention programs in order to
promote strategies for control the temptation derived from the continuous exposure to
them. In addition, since children and adolescents with excess weight have a high
probability of becoming overweight adults, the prevention of excessive consumption of
unhealthy foods and the formation of healthy eating habits in these stages is crucial to
reverse the prognosis.
3. Future perspectives
The conclusions derived from this thesis allow us to generate new research questions
that we believe would be interesting to explore in future studies. Among them we could
highlight:
1. Deepen the knowledge of the effects of social stress on the eating behavior of
excess weight adolescents through longitudinal studies that allow the
establishment of causal relationships between them.
2. Evaluate through more ecological research if, effectively, the visualization of
foods high in fats and / or sugars leads to a greater intake of these foods, and
therefore impacts on a greater weight gain.
3. Study more deeply through fMRI the neural correlates of elections with real
foods. Analyse the brain activity during the whole process, that is before making
the choice and when the food is consumed and observe the differences between
220
a group of adolescents with excess weight and one with normal weight. This
methodology would allow the results obtained to be more easily transferable to
real life.
4. Carry out interventions focused on craving presented by adolescents with excess
weight towards high caloric foods in order to control the temptation, and see if
the change in the hedonic value that is given to food has consequences in brain
processing display of these.
5. Conduct studies using the tDCS technique to try to reduce craving through the
repeated stimulation of the dlPFC, thus improving the self-control capabilities of
the individual; and study the feasibility of including this technique in obesity
treatment programs.
6. Analyse if through an intervention program focused on coping with stress,
beneficial results are produced in eating habits through changes in behaviours
related to "emotional eating". Thus, reducing the social stress impact would also
influence the reduction of the detrimental effects that chronic stress produces on
cognition.
7. Analyse the effect of genes related to the transmission of dopamine, specifically
DRD2-A1 and DRD4-7R, on the executive performance of adolescents with
excess weight. Different studies have shown that obesity and having the allele
DRD4-7R seem to confer a weakness in terms of executive performance.
However, studies are scarce, with insufficient sample and are not focused on
adolescents with excess weight.
221
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VII. ANEXOS
ARTÍCULOS PUBLICADOS
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251
RESEARCH ARTICLE
Social Stress Increases Cortisol and Hampers

Attention in Adolescents with Excess Weight
Antonio Verdejo-Garcia1,2*, Maria Moreno-Padilla1, M. Carmen Garcia-Rios3,
Francisca Lopez-Torrecillas1, Elena Delgado-Rico1, Jacqueline Schmidt-Rio-Valle3,
Maria J. Fernandez-Serrano4
1 Department of Clinical Psychology and Institute of Neuroscience F. Oloriz, Universidad de Granada,
Granada, Spain, 2 School of Psychological Sciences, Monash University, Melbourne, Australia, 3 School of
Health Sciences, Universidad de Granada, Granada, Spain, 4 Department of Psychology, Universidad de
Jaen, Jaen, Spain
* [email protected]
a11111
Abstract
Objective
To experimentally examine if adolescents with excess weight are more sensitive to social
stress and hence more sensitive to harmful effects of stress in cognition.
OPEN ACCESS
Citation: Verdejo-Garcia A, Moreno-Padilla M, Design and Methods

Garcia-Rios MC, Lopez-Torrecillas F, Delgado-Rico
We conducted an experimental study in 84 adolescents aged 12 to 18 years old classified
E, Schmidt-Rio-Valle J, et al. (2015) Social Stress
Increases Cortisol and Hampers Attention in in two groups based on age adjusted Body Mass Index percentile: Normal weight (n=42)
Adolescents with Excess Weight. PLoS ONE 10(4): and Excess weight (n=42). Both groups were exposed to social stress as induced by the vir-
e0123565. doi:10.1371/journal.pone.0123565 tual reality version of the Trier Social Stress Task –participants were requested to give a
Academic Editor: Suliann Ben Hamed, Centre de public speech about positive and negative aspects of their personalities in front of a virtual
Neuroscience Cognitive, FRANCE audience. The outcome measures were salivary cortisol levels and performance in cogni-
Received: October 23, 2014 tive tests before and after the social stressor. Cognitive tests included the CANTAB Rapid
Accepted: March 4, 2015 Visual Processing Test (measuring attention response latency and discriminability) and the
Iowa Gambling Task (measuring decision-making).
Published: April 21, 2015
Copyright: © 2015 Verdejo-Garcia et al. This is an

open access article distributed under the terms of the
Results
Creative Commons Attribution License, which permits Adolescents with excess weight compared to healthy weight controls displayed increased
unrestricted use, distribution, and reproduction in any cortisol response and less improvement of attentional performance after the social stressor.
medium, provided the original author and source are
credited.
Decision-making performance decreased after the social stressor in both groups.
Data Availability Statement: All relevant data are

within the paper and its Supporting Information files. Conclusion
Funding: This study has been funded by grants Adolescents who are overweight or obese have increased sensitivity to social stress, which
PSI2010-17290 (INTEROBE) from the Ministry of detrimentally impacts attentional skills.
Innovation and Science (MICINN), and P-10-HUM-
6635 (NEUROECOBE).
Competing Interests: The authors have declared

that no competing interests exist.
PLOS ONE | DOI:10.1371/journal.pone.0123565 April 21, 2015 1 / 12

Social Stress in Adolescent Obesity
Introduction
Adolescents with excess weight suffer substantial social stress including frequent peer bullying
and social marginalization and exclusion [1,2]. Crucially, the degree of exposure to these social
stressors is the most important predictor of poor psychological adjustment and poor academic
achievement in adolescents with obesity [3]. Moreover, neuroendocrine studies have shown
that non-fasting levels of the “hunger hormone” ghrelin increase in response to social stressors
(i.e., the Trier Social Stress Task, involving a public speak) [4] and that the awakening response
of the “stress hormone” cortisol positively associates with subsequent lipid intake [5]. There-
fore, social stress is a potent determinant of poor cognition and poor food choices in adoles-
cents with excess weight. This phenomenon could be explained by the harmful impact of social
stress on cognitive skills such as attention, cognitive control and decision-making, which con-
tribute to obesity-related behaviours in adolescents [6]. The harmful impact of persistent social
stressors on cognition in adolescents with obesity is likely to be enduring as stress induces neu-
roadaptations in prefrontal and limbic regions particularly during adolescence [7,8]. Therefore,
examining whether social stress hampers cognition in adolescents with excess weight is essen-
tial for prevention of cognitive decline and hence progression of obesity. However, to date no
studies have experimentally assessed this notion. In this study we examined if a social stressor-
the Trier public speaking stress task- specifically increases cortisol levels and hampers cognitive
performance in adolescents with excess weight compared to adolescents with normal weight.
We specifically assessed the impact of social stress on outcome measures of attention, cognitive
inhibition and decision-making. We selected these outcomes because they reflect the function
of frontal-limbic systems [9,10] and are longitudinally associated with weight gain in pediatric
populations [11,12]. We hypothesized that adolescents with excess weight would show greater
cortisol response to the social stressor, and greater detrimental impact of social stress on atten-
tion and decision-making performance.
Methods
Participants
Eighty-four adolescents aged between 12 and 18 years old participated in the study. They were
classified in two groups (Normal weight [n = 42] and Excess weight [n = 42]) based on their
age adjusted Body Mass Index (BMI) percentile [13]. Sample size was estimated through power
analysis. The existing evidence about the impact of the Trier Social Stress Task (TSST) on se-
lected outcome variables was correlational (i.e., the association between TSST-induced cortisol
changes and decision-making performance is between 0.3 and 0.4) [14,15]. Therefore, we esti-
mated that in order to achieve adequate power (80%) to detect a ρH1 = 0.3 association between
the independent variable (stress) and the cognitive outcomes (attention and decision-making)
84 participants would be required (S1 Fig). This sample size was deemed acceptable for the
mixed repeated-measures design. The classification of the two groups was conducted in align-
ment with the guidelines of the International Obesity Task Force and the Centers for Disease
Control and Prevention: Normal weight participants had age adjusted BMI percentiles in the
range between the 5th and the 84th percentile, and Excess weight participants had age adjusted
BMI percentiles 85 (Table 1). Three participants from the Excess weight group provided in-
valid cortisol samples, and therefore the final study sample comprised 42 Normal weight and
39 Excess weight participants. Participants’ socio-demographic characteristics, BMIs, percent-
age fat and blood count obtained biochemical parameters are as well displayed in Table 1. Par-
ticipants also completed The Dutch Eating Behavior Questionnaire [16] which was used to

Table 1. Descriptive scores for the demographic, biometric and blood count characteristics of adolescents with excess and normal weight.
Variables Mean SD Mean SD ta/chi squareb p

Age 15.59 1.91 15.62 1.83 -.07a .944
b
Gender (% Men/Women) 52.4/47.6 43.2/56.8 .72 .262
BMI 29.87 3.57 20.87 2.06 13.73a .000
Fat (%) 31.97 9.15 17.99 6.94 7.69a .000
DEBQ
Emotional 23.68 9.33 24.03 9.02 -0.17a .858
External 28.64 7.11 31.28 7.68 -1.71a .091
Restraint 25.55 7.22 19.30 7.81 3.98a .000
Glucose 92.57 6.03 92.14 6.64 .276a .783
a
Cholesterol 158.07 27.35 148.47 20.89 1,64 .104
Triglycerides 70.64 28.76 63.13 27.32 1.09a .279
HDL 56.80 12.49 58.73 12.82 -.61a .541
LDL 90.85 21.08 80.51 14.96 2.38a .020
Insulin 47.28 57.78 53.34 114.18 -.25a .802
Uric Acid 5.08 0.87 4.39 0.97 2.98a .004
Thyroxine 1.33 0.43 1.44 0.68 -0.79a .451
a
b
doi:10.1371/journal.pone.0123565.t001
characterise psychological traits relevant to maladaptive eating behaviours (i.e., external eating,
emotional eating and restraint) (Table 1).
Participants were recruited from the paediatrics and endocrinology services of the Hospital
“Virgen de las Nieves” in Granada (Spain), and from schools located in the same geographical
area. The inclusion criteria for participants were defined as follows: (i) age range between 12
and 18 years old; (ii) BMI percentiles falling within the intervals categorized as overweight or
obesity (85—Excess weight group), or normal weight (5–85—Normal weight group); and
(iii) absence of history or current evidence of neurological or psychiatric disorders, assessed by
participants and parents interviews and the Eating Disorder Inventory [17]. All participants
had normal or corrected-to-normal vision.
Experimental procedures
Fig 1 displays a schematic representation of the experiment. In order to induce social stress in
the laboratory we utilised a previously validated Virtual Reality version of the Trier Social
Stress Task (TSST) [18]. Participants had to perform a stressing task which consisted of deliv-
ering a speech about personal characteristics including both positive and negative aspects of
themselves in front of a simulated audience. Participants were told that this audience would at-
tend the speech and subsequently evaluate its quality. However, the virtual audience was pro-
grammed to look progressively bored and disappointed with the speech. The speech was
followed by a mental calculation test (serially subtracting 17, starting from 2013). Cortisol lev-
els were measured via saliva samples collected before onset of the TSST (T1), after completion
of the TSST and the calculation test (10 minutes after TSST onset—T2) and after performance
on each of the attention and decision making cognitive probes (20 and 30 minutes after TSST
onset-T3 and T4- respectively). Cognitive measures were conducted in a fixed order before
TSST onset (pre-TSST, overlapping with T1) and after completion of the TSST and the

Fig 1. Schematic representation of the experiment.

doi:10.1371/journal.pone.0123565.g001
calculation test (post-TSST, overlapping with T2). To minimize practice effects, we utilised
parallel versions of all tasks in the post-TSST administration. The original validation study
showed that this virtual reality TSST is able to induce modest but sizeable increases in cortisol
and subjective stress responses [18]. Moreover the virtual audience tamed the ethical concerns
associated with the negative impact of the social stressor on adolescents’ participants. The Eth-
ics Committee for Human Research of the Universidad de Granada approved the study. Both
participants and parents signed informed consent.
Cortisol measurement. Participants were told not to smoke, eat or drink coffee for at least
30 minutes before the experiment. All the experimental sessions were conducted at the same
time of the day (4–5 pm) based on pilot data obtained in this cohort prior to study onset indi-
cating that diurnal cortisol levels were stable during these hours. Saliva was collected via a com-
mercially available device: Salivette Cortisol (Sarstedt, Numbrecht, Germany). This device is
composed of a cotton tube (similar to dental cotton), and two plastic tubes that fit one inside
the other. Subjects were told to place cotton salivettes inside their mouth and gently chew and/
or suck on them for 1–3 min until they became soaked in saliva. The cotton tube was inserted
inside the plastic tube, which was then capped. Saliva samples were stored at -20°C until re-
quired for assay. Samples were analyzed at the University Hospital, using the electrochemilu-
minescence immunoassay “ECLIA” method. This method is designed for use in Roche
Elecsys 1010/2010 automated analyzers and in the Elecsys MODULAR NALYTICS E170 mod-
ule. We computed two different metrics from each cortisol sample (microgram/deciliter and
nanomol/liter). The correlation between both metrics at the different time points ranged from
0.8 and 0.9.
Cognitive measures. We utilized three computerized tests: two subtests from the Cam-
bridge Neuropsychological Test Automated Battery (CANTAB) [19], Motor Screening (MOT)
and Rapid Visual Information Processing (RVP), and the Iowa Gambling Task (IGT) [20]. Al-
ternate versions of each test were used in pre-stress and post-stress administrations.
MOT. The main objective of this test is to provide a baseline measure of the subjects’ basic
motor skills in terms of reaction times and accuracy. After a demonstration of the correct way
to point on the computer screen using the forefinger of the dominant hand, the subjects must
point to a series of stimuli (crosses) popping up in turn. The outcome measure of this test was
response latency.
RVP. This is a test of visual sustained attention with an impulse control component. A
white box is displayed in the centre of the computer screen, inside which digits, from 2 to 9, are
displayed in a pseudo-random order, at the rate of 100 digits per minute. The subject must de-
tect consecutive odd or even sequences of digits (for example, 2-4-6) and respond by pressing
the touch pad. The outcome measures of this test were response latency and response

discriminability (B’) scores, which are sensitive to attention and impulse control domains re-
spectively. The B’ score is the signal detection measure of the strength of trace required to elicit
a response (range -1.00 to +1.00). Thus, it is the tendency to respond regardless of whether the
target sequence is present and uses the p(hit) and p(fa) results. A score close to +1.00 indicates
that the subject gave few false alarms.
IGT. This is a computer task measuring reward/punishment based decision-making. It in-
volves four decks of cards (A, B, C and D). Each time a participant selects a card, a specified
amount of play money is awarded. However, interspersed among these rewards, there are prob-
abilistic punishments (monetary losses). Two of the decks of cards (A and B) produce high im-
mediate gains; however, in the long run, they will take more money than they give, and are
thus considered disadvantageous. The other two decks (C and D) are considered advantageous,
as they result in small, immediate gains, but will yield more money than they take in the long
run. The performance measure was the net score calculated by subtracting the number of dis-
advantageous choices (decks A and B) from the number of advantageous choices (decks C and
D). An equivalent parallel version of the ABCD task in which decks are labelled K, L, M and N
was utilised in the post-TSST administration. These versions have shown adequate test-retest
reliability and ecological validity in relation to decision-making [21].
Visual Analogue Scales (VAS). We used two Visual Analogue Scales (VAS) designed to
rate arousal and stress. For arousal scale the individual must indicate the extent to which they
perceived as active and alert (from nothing active to very active). For stress scale they must in-
dicate how much stress they feel (from no stress to very much stress). We used the mean scores
of each dimension.
The main hypotheses were examined utilizing mixed repeated measures analyses of variance
including Time as the repeated-measures factor, Group as the between-groups factor, and cor-
tisol levels (as measured in μg/dl) and RVP’s mean response latency and B’ scores and IGT’s
net scores as dependent measures. Cortisol and RVP performance measures were log-trans-
formed (base 10) to meet the normal distribution, but for the sake of clarity the Figures report
non-transformed measures. IGT scores fitted to the normal distribution as assessed by Kolgo-
morov-Smirnov tests. We also performed correlation analyses between change scores of corti-
sol levels (T2—T1) and change scores of cognitive performance (T2—T1) and between both
change scores and biological and psychological measures. These change measures were non-
normally distributed and therefore we applied Spearman’s rank correlation analyses. Two par-
ticipants from the Excess weight group (n = 37) and one participant from the Normal weight
group had missing cortisol data at T1 and T2 (n = 41). With regard to cognitive tests, there was
no missing data in the Excess weight group (n = 39), whereas in the Normal weight group
three participants had invalid data for RVP response latency and IGT (n = 39) at T1 or T2, and
three participants had invalid data for RVP B’ (n = 38) at T1 or T2.
Results
Cortisol response
We found a significant Time x Group interaction on cortisol levels, F (3,74) = 4.36, p = 0.008.
Cortisol mildly increased in Excess weight participants after the TSST. Independent-sample t-
tests showed that Excess weight and Normal weight participants did not significantly differ on
cortisol levels before TSST (T1). However, Excess weight adolescents showed significantly in-
creased cortisol levels after TSST (T2), t = 1.94, p = 0.05, Cohen’s d = 0.5 (Fig 2). Moreover,
cortisol increase between T2 and T1 correlated with amount of fat, Spearman’s Rho = 0.30,

Fig 2. Cortisol levels (μg/dl units) in adolescents with excess weight and adolescents with normal
weight before and after exposure to the Trier Social Stress Task (TSST). T1 represents cortisol levels
before TSST; T2 represents cortisol levels immediately after TSST termination; T3 and T4 represents cortisol
levels 10 and 20 minutes after TSST termination.
p = 0.01. Between-group differences were also statistically significant at T3, t = 2.44, p = 0.02,
and T4, t = 2.63, p = 0.01. However, this effect seems to be driven by decreased cortisol levels in
the Normal weight group (Fig 2).
Cognitive performance
MOT. Pre-TSST scores showed that both groups had similar baseline response latencies.
Further, both groups showed mild reductions of response latencies between the pre-TSST mea-
sure and the post-TSST measure (Fig 3).
RVP—Response latency. We found a significant Time x Group interaction, F (1,76) =
6.35, p = 0.01 (Fig 3). Independent-sample t-tests showed that Excess weight and Normal
weight participants did not significantly differ in the pre-TSST measure. However, they showed
marginally significant differences in the post-TSST measure, t (78) = 1.75, p = 0.08, Cohen’s
d = 0.4, with Excess weight participants performing significantly poorer than Normal weight
controls. There was no significant correlation between T2—T1 cortisol levels and T2—T1 RVP
Response Latency.
RVP—Response discriminability. We did not find a significant Time x Group interac-
tion, F (1,75) = 0.99, p = 0.32. There were no main effects of Time or Group, although visual in-
spection shows Excess weight participants performed better than Normal weight participants
in both pre- and post-TSST measures (Fig 3).
Decision-making—IGT. We did not find a significant Time x Group interaction, F (1,77)
= 0.005, p = 0.94. There was a significant main effect of Time, F (1,77) = 6.01, p = 0.02, indicat-
ing that both groups exhibited significantly poorer performance after the TSST (Fig 3). There
was no significant correlation between T2—T1 cortisol levels and T2—T1 IGT performance.
Correlations between biological and psychological measures and cognitive performance
in T2—T1. We found a positive correlation between levels of uric acid and change in RVSP
response latency performance between T2 and T1, Spearman’s Rho = 0.46, p = 0.0001, and a
negative correlation between thyroxine levels and change in Iowa Gambling Task performance
between T2 and T1, Spearman’s Rho = -0.27, p = 0.03. We also found a negative correlation

Fig 3. Cognitive performance in adolescents with excess weight and adolescents with normal weight
before and after exposure to the Trier Social Stress Task (TSST). Top panel Y axes represent time in
milliseconds. The Y axis in the bottom-left panel represents signal detection derived Beta scores, ranging
from 0 to 1. The Y axis in the bottom-right panel represents Iowa Gambling Task net scores, ranging from -60
to +60.
between scores of external eating and RVSP response latency performance between T2 and T1,
Spearman’s Rho = -0.27, p = 0.02.
Visual Analogue Scales (VAS). We did not find a significant Time x Group interactions
on VAS of arousal or stress but results were in the expected direction, with both groups show-
ing more subjective arousal and stress after the TSST (S2 Fig).
Post-hoc analyses in the subsample of participants showing enhanced cortisol re-
sponse. The primary analyses indicated that in the normal weight group cortisol levels did
not change after stress, and therefore there is a concern that cognitive changes were due to spu-
rious factors. To address this issue, we run additional analyses in the subsample of participants
who showed sizeable increments in cortisol levels after stress, including 24 participants of the
Excess weight group (57% of the original sample) and 20 participants of the Normal weight
group (48% of the original sample). The results of these analyses were coherent with the main
findings. We found a significant Time x Group interaction on RVP’s latency scores, F (1,41) =
6.17, p = 0.02, whereby a drop in performance was only observed in the Excess weight group
(See S2 Fig). Moreover, there was a significant correlation between T2—T1 cortisol levels and
T2—T1 RVP Response Latency (Spearman’s Rho = 0.25, punilateral = 0.05) (Fig 4).
Discussion
We show that social stress specifically increases cortisol levels and hinders attentional response
latency in adolescents with excess weight. Conversely, social stress failed to show significant ef-
fects on attention response discriminability. Moreover, both excess weight and normal weight
adolescents displayed poorer decision-making performance after the social stressor. These

Fig 4. Correlation between between T2—T1 cortisol levels (X Axis) and T2—T1 RVP Response Latency (Y Axis) within the subsample of
participants showing TSST-induced increases in cortisol levels.
findings indicate that adolescents who are overweight and obese have enhanced stress reactivity
in response to social stressors, which selectively impacts on attentional skills. Since adolescents
with excess weight are markedly exposed to social stressors during everyday lives, our findings
suggest that stress immunization strategies should be put in place to prevent the harmful im-
pact of social stress on cognition and therefore on progression of obesity.
In agreement with our primary hypothesis, social stress induced greater cortisol response in
overweight and obese adolescents. The effect was mild but the specific impact on participants
with excess weight agrees with the notion that repetitive social stress may induce sensitization
of the hypothalamic-pituitary-adrenal (HPA) axis [22] and purportedly of the HPA axis associ-
ations with fronto-limbic systems [23–25]. The discrepancy between our finding of cortisol in-
crease and a previous negative finding in obese adults [26] suggests that adolescence compared
to adulthood is a more sensitive time period for abnormal sensitization of stress systems, likely
due to ongoing neural maturation of these systems [7,27]. Further, both preclinical and clinical
evidence shows that social stressors such as social evaluation and social exclusion are particu-
larly challenging for adolescents [8,28,29]. The potential mechanisms for the specific impact of
social stress on stress reactivity in adolescents with excess weight include the additive or syner-
gistic interactions between social stress and inflammation [30,31] and/or between social stress
and obesity-related neuroadaptations in anterior cingulate and limbic regions that are essential
for stress regulation [32,33]. Our finding is particularly relevant in view of the significant asso-
ciation between cortisol reactivity and obesity-related behaviours [34,35], and of the emerging
evidence suggesting that high levels of stress can longitudinally predict the progression of obe-
sity [36].
We also showed a significant impact of social stress on attentional performance in adoles-
cents with excess weight. The effect was again mild and pointed to stress-related hindering of

the capacity to get benefit from a repeated administration of the task. Previous findings indicate
that repeated administration of CANTAB attentional tests is associated with significant im-
provements in performance (of at least 0.3 in Cohen’s d effect size) [37], and this is what we ob-
served in the control group. However, excess weight adolescents were unable to get benefitted
from this repeated administration. The effect was specific for attention-related latency adjust-
ments, but not for psychomotor-related reaction times. Therefore, it suggests a detrimental im-
pact of stress on attention regulation.6 This notion is consistent with the neural networks
interactions between the HPA axis and medial prefrontal cortex and anterior cingulate cortex
regions involved in attention regulation [38–40]. In support, neuroimaging studies have shown
that the impact of stress on executive attention is mediated by structural (gray matter) neuroa-
daptations in prefrontal cortex and anterior cingulate cortex regions [41]. This stress-related
attentional hurdle has a high translational value, as individual differences in response latencies
to attentional probes are longitudinally associated with increases in BMI [12], implying that ad-
equate control of social stress and/or cognitive boosting of attentional resources may contrib-
ute to prevent chronic obesity. This notion is consistent with our finding of significant
correlations between less improvement of attentional performance (between T1 and T2) and
higher maladaptive eating patterns such as external eating, which reflects attentional bias to-
wards food related cues. Further, both social stress and attentional skills are significantly associ-
ated with advantageous social functioning and academic performance [3], and therefore our
finding highlights the potential benefit of controlling social stress to improve social and career
outcomes in the long-term.
Furthermore, we found poorer decision-making after the social stressor in both adolescents
with excess weight and adolescents with normal weight. Since cortisol levels dropped between
T3 and T4 (the time window of decision-making task performance) it is unlikely that this find-
ing can be attributed to the effects of acute stress. However, it might be attributed to broader ef-
fects of the social stressor, such as the social evaluation context. The latter notion agrees with
previous experimental evidence showing that adolescents make riskier choices than young
adults or adults when they are under social evaluation [42]. The lack of specificity of our result
implies that the impact of social evaluation on decision-making is mediated by neural mecha-
nisms that are similarly sensitized in adolescents regardless of BMI/weight status, or that differ-
ent neural mechanisms mediate a similar impact of social evaluation on decision-making in
excess weight and normal weight adolescents. In favor of the first notion, neuroimaging studies
have shown that the impact of social evaluation on decision-making is mediated by increased
activation of ventral striatal and orbitofrontal regions [43], which are generally sensitized dur-
ing adolescence. In favor of the second notion, we have observed that excess weight and normal
weight adolescents recruit different brain circuitries during the pondering of social decisions
[44]. Future studies are warranted to address this question. In any case, our finding might have
general implications for prevention of obesity during adolescence as we know that adolescents
who are overweight or obese have higher exposure to social evaluations [3] and that subsequent
risky choices are longitudinally associated with weight gain and obesity [11].
We conclude that social stress response is sensitized in adolescents with excess weight, hin-
dering their attentional function. The study has important strengths including the experimen-
tal design, the power-informed sample size, the detailed phenotypic characterization and the
group matching of excess weight and normal weight adolescents, and the objective measure-
ment of stress reactivity with cortisol biomarkers. However, the results should be as well ap-
praised in light of relevant limitations. It is particularly important to stress that unlike the
original TSST [45], the virtual reality TSST was not able to induce significant increases of corti-
sol levels in the control group. We selected this stressor because it was capable of inducing mild
but sizeable stress in the laboratory at the same time that it reduced the ethical implications of

stressing “at risk” obese adolescents [18]. In agreement with this assumption, our results indi-
cate that the stress manipulation was actually more effective in obese adolescents (57% of par-
ticipants showed increased cortisol levels) than in controls (only 48% of participants showed
increased cortisol levels). There are however several factors that may explain the variability in
stress induction, such as degree of belief in the cover story or degree of immersion in the virtual
reality environment, that were not systematically controlled in this study. Therefore, further
studies are warranted to reassess the validity of this virtual reality version, and to replicate our
findings using TSST versions that are able to unequivocally reproduce the original TSST stress
induction. Moreover, in absence of a “no-stress” control condition, we cannot ascertain a caus-
al link between stress and cognitive performance. However, we base our interpretation on pre-
vious evidence showing that improvement (rather than stability or decrease) in performance is
typically expected in “no-stress” repeated administration designs [37]. A related limitation is
the negative finding in relation to cognitive impulsivity. Since mild arousal improves inhibitory
control in adolescents, it is plausible that the mild nature of the stressor fostered cognitive im-
pulsivity increases rather than (expected) decreases after TSST. Future studies are warranted to
address these limitations, to expand on the biological, psychological and socio-economic medi-
ators of the impact of social stress on cognition, and to longitudinally assess the relevance of
this experimental effect on public health indicators of the progression of obesity.
Supporting Information
S1 Fig. Power analysis calculations.
(TIF)
S2 Fig. Visual Analogue Scales for arousal—left panel- and stress—right panel- in excess
and normal weight adolescents before and after the Trier Social Stress Task (TSST).
(TIF)
Author Contributions
Conceived and designed the experiments: AVG. Performed the experiments: MMP EDR JSRV.
Analyzed the data: AVG. Contributed reagents/materials/analysis tools: MGR. Wrote the
paper: AVG MFS FLT.
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ann. behav. med. (2018) XX:1–9
DOI: 10.1093/abm/kay051
REGULAR ARTICLE (INCLUDING REVIEWS)
Negative Social Evaluation Impairs Executive Functions in

Adolescents With Excess Weight: Associations With Autonomic
Responses
María Moreno Padilla, MS1 • María J. Fernández-Serrano, PhD1 • Antonio Verdejo García, PhD2
• Gustavo A. Reyes del Paso, PhD1
Published online: XX XXXX 2018

© Society of Behavioral Medicine 2018. All rights reserved. For permissions, please e-mail: [email protected].
Abstract
Background Adolescents with excess weight suffer social deterioration of executive functioning in adolescents
stress more frequently than their peers with normal with excess weight. Evoked increases in subjective stress
weight. and autonomic responses predicted decreased executive
Purpose To examine the impact of social stress, specifi- function. Deficits in executive skills could reduce cogni-
cally negative social evaluation, on executive functions in tive control abilities and lead to overeating in adolescents
adolescents with excess weight. We also examined asso- with excess weight. Strategies to cope with social stress
ciations between subjective stress, autonomic reactivity, to prevent executive deficits could be useful to prevent
and executive functioning. future obesity in this population.
Methods Sixty adolescents (aged 13–18 years) classified
into excess weight or normal weight groups participated. Keywords Obesity • Adolescence • Social stress
We assessed executive functioning (working memory, • Executive functions • Autonomic reactivity
inhibition, and shifting) and subjective stress levels
before and after the Trier Social Stress Task (TSST). The
TSST was divided into two phases according to the feed- Introduction
back of the audience: positive and negative social evalu-
ation. Heart rate and skin conductance were recorded. Overweight and obesity in adolescence have sharply
Results Adolescents with excess weight showed poorer increased over recent decades, reaching epidemic levels [1].
executive functioning after exposure to TSST compared The socioeconomic changes that have occurred in recent
with adolescents with normal weight. Subjective stress decades in Western societies, associated with the unlim-
and autonomic reactivity were also greater in adoles- ited access to food, have modified the way we perceive
cents with excess weight than adolescents with normal food and regulate intake. These processes are increasingly
weight. Negative social evaluation was associated with influenced by a variety of factors besides homeostatic
worse executive functioning and increased autonomic regulation, like sensory cues (e.g., taste, smell, texture
reactivity in adolescents with excess weight. and appearance), availability, motivational and affect-
ive states, pleasure seeking, and so on. All of these fac-
Conclusions The findings suggest that adolescents with
tors influence what and how much people eat even when
excess weight are more sensitive to social stress trig-
they are not hungry [2]. In the last few years, obesity is
gered by negative evaluations. Social stress elicited
being increasingly considered as a brain-related dysfunc-
tion similar to that occurring in addictions [3], where the
 María J. Fernández-Serrano
motivational value of highly palatable food is signifi-
[email protected] cantly increased, while the top-down or executive control
mechanisms that would normally regulate reward-driven
1
Department of Psychology, Universidad de Jaén, 23071 Jaén, responses are diminished [4, 5]. Executive control mech-
Spain anisms are relevant to the regulation of eating behavior
2
School of Psychological Sciences and Monash Institute of
[6], as they allow for adjustment of behavior in a flex-
Cognitive and Clinical Neurosciences, Monash University, ible way in situations that require a change in a strong
Melbourne, Australia habitual response or resistance to temptation [7]. The
Downloaded from https://academic.oup.com/abm/advance-article-abstract/doi/10.1093/abm/kay051/5043023

by university of winnipeg user
on 22 June 2018
2 ann. behav. med. (2018) XX:1–9
abnormal interaction between reward signal processing executive performance after exposure to social stress
and executive control functioning has also been related relative to normal weight adolescents. Outcome meas-
to a tendency to select immediate and appetizing (high in ures were working memory, cognitive inhibition, and
calories and/or sugar) rewarding choices, although these shifting (ability to follow different rules in a task and
have negative consequences in the long term [8, 9]. The change between them). In addition, subjective and phys-
imbalance between these two systems can be greater in iological (autonomic) indexes of stress were recorded.
adolescence, a period characterized by the relative imma- For this purpose, heart rate (HR) and skin conduct-
turity of the prefrontal cortex, responsible for executive ance (SC) were continuously recorded during the TSST.
control, in addition to the relative maturity of striatal As overweight adolescents are more often exposed to
areas responsible for reward processing [10]. Therefore, negative peer evaluations than adolescents with nor-
during adolescence, the activity of rewards system may mal weight [18, 19], we expected greater increases in
prevail over that of executive control mechanisms [11]. perceived stress, HR, and SC in excess versus normal
Another factor that can impair top-down control weight participants during the TSST. Furthermore, neg-
mechanisms is stress. Stress has a harmful impact on ative associations between stress-induced subjective and
cognitive skills, such as attention, cognitive control, physiological responses and post-TSST executive per-
and decision making, which may contribute to obesi- formance were hypothesized.
ty-related behaviors in adolescents [12]. Furthermore,
psychosomatic theories hold that people with obesity Method
tend to eat in response to emotional distress, showing
an “emotional eating pattern” (i.e., consuming food Participants
impulsively) when under negative emotional states [13].
Stress can also enhance the propensity to eat high calorie Sixty adolescents, 25 males and 35 females between 13
“palatable” food via its interaction with central reward and 18 years of age, participated. They were selected
pathways [14]. For example, ghrelin and cortisol increase based on their sex and age-adjusted body mass index
in response to social stressors and influence reward moti- (BMI) percentile in accordance with the guidelines of the
vation, thus modulating consumption of appetizing food International Obesity Task Force (IOFT) [28]. Normal
[15, 16]. weight participants (n = 30) had BMIs ranging between
During adolescence, peer relations are particularly the 5th and 84th percentiles, and excess weight partici-
salient and can serve as a robust source of distress [17]. pants (n = 30) had BMIs greater than the 85th percentile.
Adolescents with excess weight suffer from social stress, Table 1 displays the sociodemographic, BMI, and body
such as bullying or social marginalization-exclusion, fat percentage data. Participants were recruited from
more frequently than their peers [18], being subjected high schools located in Jaén (Spain). They were screened
to frequent teasing about their body [19]. Negative ste- for medical and developmental conditions, medication
reotypes toward peers with excess weight begin early in use, and learning disabilities. Inclusion criteria were (i)
childhood [20], and these social stressors can negatively age range between 13 and 18 years, (ii) BMI >5th per-
affect social adjustment and academic achievement [21]. centile, and (iii) no history of neurological, psychiatric,
In this context, study of the detrimental influence of or eating disorders (measured using the Eating Disorder
social stress on executive functions may be of crucial Inventory [EDI-2]). All participants had normal or cor-
importance to understand deficient diet-related decision rected-to-normal vision.
making and poor emotional-regulation-related overeat-
ing in adolescents. Executive Measures
Several studies have found deficits in executive func-
tioning in adults and adolescents with excess weight [22– Working memory—Letter-Number Sequencing [29]
25]. However, to the best of our knowledge, no study
has analyzed the influence of social stress on executive Participants were read a sequence in which letters and
functions in adolescents with excess weight. Therefore, numbers were combined, and were asked to reproduce
this study examined the effect of a social stressor on the sequence, first putting the numbers in ascending
executive performance in adolescents with excess ver- order and then the letters in alphabetical order. The sum
sus normal weight. For this purpose, the Trier Public of the correct answers was considered.
Speaking Stress Social Task (TSST) [26, 27] was used.
We analyzed the specific influence of negative social Inhibition and shifting—Five-Digit Test (FDT) [30]
evaluation on executive functioning and autonomic The FDT consists of four conditions of increasing com-
responses in overweight adolescents. We hypothesized plexity. Conditions 1 and 2 evaluate processing and
that excess weight adolescents would show decreased response speed. In Condition 3 (inhibition), participants

on 22 June 2018
ann. behav. med. (2018) XX:1–9 3
Table 1 Participants’ sociodemographic characteristics, BMIs and body fat percentage
Mean SD Mean SD t/chi-square p
Age 15.38 1.75 15.41 1.36 −0.08a .935

Sex (% Men/women) 46.7/53.3 36.7/63.3 0.62b .601
BMI 28.53 2.96 20.04 2.05 12.87a <.001
% Body fat 28.04 7.78 17.32 7.71 5.36a <.001
BMI body mass index.

a
Value of Student’s t.
b
Value of chi-square χ2.
have to count the number of digits contained within Procedure

various boxes, which constitutes an interference effect
because the boxes contain groups of digits that do not After obtaining permission from the high school’s direc-
correspond to their arithmetic value. Finally, in Part 4 tors, the study was presented to each class of students
(shifting), participants have to count or read, depending and their participation was requested. The students who
on whether the outline of the box is normal (count, 80% were interested in taking part sent us the informed con-
of stimuli) or of double thickness (read, 20% of stim- sent form, which was signed by their parents if they were
uli). The difference in performance time between Part 3 minors. Then, the participants were assigned to a group
and the mean of Parts 1 and 2 (inhibition score), and the and a specific day on which to complete the experimen-
difference in performance time between Part 4 and the tal session. Six high schools in Jaén participated in the
mean of Parts 1 and 2 (shifting score), were considered. study. The recruitment rate was approximately 4% of the
Thus, a higher score denotes worse performance (i.e., the total number of students approached. Sessions started
participant took more time). Errors in Parts 3 (inhibi- at 4 p.m., and participants were required to be satiated
tion) and 4 (shifting) were also analyzed. (having had lunch about 1 hr before) and to not have
taken any caffeine. Weight and height were self-reported
Social Stress Task by participants for recruitment purposes, and BMI was
calculated in the laboratory, using the exact height and
To induce social stress in the laboratory, a validated weight data collected on arrival. Body composition
virtual reality version of the Trier Social Stress Task measures were also collected using the Bodystat®1500
(TSST-VR) was used [26]. This version of the TSST was monitoring unit. The EDI-2 [32], validated in young
previously used in young people and has been shown to people, was administered to rule out eating disorders
produce a significant increase in subjective stress and (binge eating, anorexia nervosa, and bulimia nervosa).
arousal, SC, and cortisol levels [27, 31]. Participants had Then, executive functioning measures were conducted
to deliver a speech about their personal characteristics, before TSST onset (pre-TSST) and immediately after
including both positive and negative aspects, in front of completion of the TSST (post-TSST). The post-TSST
a simulated audience. The task is divided into two parts evaluation was administered immediately after TSST.
(each 2 min 30 s long). In the first task, the audience During the two evaluations, participants first completed
was interested and attentive to the speech, giving nods the Letter-Number Sequencing and then the FDT.
of understanding to the participant (i.e., positive social Subjective stress was measured by a visual analogue
evaluation). In the second part, the audience began to scale (VAS, ranging from 1 to 10; no stress to extreme
show signs of disagreement with the speech, talking and stress) before and after exposure to TSST. The TSST-VR
murmuring among themselves and criticizing the par- was carried out in a soundproof room, with white walls
ticipant’s words (i.e., negative social evaluation). The and without any distracting stimuli. The equipment con-
task included four phases: a baseline rest period (3 min), sisted of a computer running the program containing
delivery of the task instructions and preparation for the the social scenes, and a projector for their display on
speech by the participant (3 m), speech during positive the wall. Previous validation studies indicated increases
social evaluation, and speech during negative social in SC and salivary cortisol during the task, both when
evaluation. This virtual reality version of the TSST is scenes were presented via goggles or projected on to a
able to induce modest but significant increases in corti- screen [31]. However, participants rated task immersion
sol and subjective stress responses [26]. as being higher with the wall-screen presentation versus

on 22 June 2018
the goggles [31]. Surround-sound headphones were used four phases, given our specific interest in the effect of
to allow perception of the sound emanating from the social evaluation, HR and SC analyses were restricted
room where the audience was situated, and the murmurs to the difference between the latter two parts of the
and comments of the listeners. The Ethics Committee of TSST involving social evaluation (positive vs. negative
the Universidad de Jaén approved the study. Both partic- social evaluation). Associations between variables were
ipants and parents signed informed consent forms. analyzed by Pearson’s correlations. To simplify the cor-
relation analysis, change scores were computed as the
Psychophysiological Data Acquisition and Processing difference between the post- and pre-TSST values.
HR and SC were continuously recorded during the TSST Results

using a Biopac MP150 polygraph (Biopac Systems Inc.,
USA). HR (beats per minute) was derived from an electro- Associations Between Measures
cardiogram (ECG) recorded at 1,000 Hz. ECG electrodes
(Ag/AgCl) were attached to the participant’s right mid-
In the whole sample, the change in HR was positively
clavicle and the lowest left rib (left wrist as the ground).
associated with changes in stress VAS scores (r = .32,
HR was extracted from ECG recordings using the soft-
p = .013), “shifting errors” (r = .30, p = .02), “inhibi-
ware AcqKnowledge 3.9.1 (Biopac Systems Inc.) and
tion errors” (r = .38, p = .003), and the “shifting score”
edited for artifacts (when present) via linear interpola-
(r = .26, p = .046). The change in SC correlated inversely
tion. SC (micro-Siemens, μS) was recorded at a sampling
with the change in Letter-Number Sequencing (r = −.33,
rate of 500 Hz using Ag–AgCl electrodes filled with an
p = .01), and positively with the change in stress VAS
inert 0.05 M NaCl electrolyte cream and attached to the
scores (r = .26, p = .047). Finally, the change in stress
palmar surface of the second and third middle phalanges
VAS scores correlated positively with the change in
of the participant’s nondominant hand. Two participants
“inhibition errors” (r = .46, p < .001). BMI was positively
(one from each group) had unusable SC recordings.
associated with post-TSST “inhibition errors” (r = .51,
p < .001), “shifting errors” (r = .32, p = .001), and stress
Statistical Analyses
VAS scores (r = .31, p = .015).
Group comparisons were carried out with Student’s
t-test for independent samples. Responses to the TSST Subjective Stress
were analyzed by repeated measures ANOVA with
Time (pre- and post-TSST) as the repeated-measures A Time × Group interaction was found for stress VAS
factor and Group (Excess vs. Normal weight) as the scores, F(1, 58) = 9.76, p = .003, η2p = 0.14. While in ado-
between-subject factor. Although the TSST consisted of lescents with excess weight stress levels increased from
Table 2 Descriptive scores and group comparisons for stress (VAS) and neuropsychological measures before TSST (pre-scores) and after
TSST (post-scores)
Mean SD Mean SD t p d´
Stress Pre 1.49 1.65 1.82 1.91 −0.72 .474 0.18

Stress Post 4.03 2.45 2.59 2.18 2.39 .020 0.62
Letter-Number Sequence Pre 9.03 2.53 8.73 1.76 0.53 .597 0.14
Letter-Number Sequence Post 9.03 2.93 10.87 2.70 −2.52 .015 0.65
Score-inhibition-FDT Pre 17.13 7.16 13.75 5.33 2.07 .042 0.54
Score-inhibition-FDT Post 12.73 4.40 10.85 5.16 1.52 .134 0.39
Score-shifting-FDT Pre 22.37 6.80 20.81 5.99 0.94 .353 0.24
Score-shifting-FDT Post 21.07 3.86 16.52 4.84 4.02 <.001 1.04
Errors-inhibition-FDT Pre 0.77 0.97 0.70 0.95 0.27 .067 0.01
Errors-inhibition-FDT Post 1.70 0.95 0.37 0.61 6.44 <.001 1.67
Errors-shifting-FDT Pre 1.50 1.57 1.13 1.25 1.00 .321 0.26
Errors-shifting-FDT Post 2.37 2.35 0.80 1.29 3.19 .002 0.83
VAS visual analogue scale; TSST Trier Social Stress Task; FDT Five-Digit Test.

on 22 June 2018
pre- to post-TSST evaluation, F(1, 29) = 65.89, p < .001,

η2p = 0.69, the change in adolescents with normal weight
did not reach significance, F(1, 29) = 2.66, p = .115,
η2p = 0.08 (Table 2).
Psychophysiological Measures
No group differences were found in HR or SC during

the pre-TSST evaluation. A Time × Group interaction
was found for HR, F(1, 58) = 8.26, p = .006, η2p = 0.13
(Fig. 1). While HR increased in adolescents with excess
weight from the positive to the negative social evaluation
phase of TSST, F(1, 29) = 8.45, p = .007, η2p = 0.23, no
change was observed in adolescents with normal weight, Fig. 2. Mean skin conductance (micro-Siemens) during the pos-
F(1, 29) = 1.16, p = .29, η p = 0.04. A Time × Group inter-
2
itive and negative social evaluation phases of the Trier Social
action was also observed in SC, F(1, 56) = 4.76, p = .033, Stress Task. Bars indicate standard error of the mean.
η2p = 0.08 (Fig. 2). While SC decreased in adolescents
with normal weight from the positive to the negative η2p = 0.47, and “shifting score,” F(1, 29) = 23.02, p < .001,
social evaluation phase of the TSST, F(1, 28) = 17.15, η2p = 0.44, and decreased their “inhibition errors” (FDT),
p < .001, η2p = 0.38, no change was observed in ado- F(1, 29) = 6.59, p = .01, η2p = 0.19. By contrast, ado-
lescents with excess weight, F(1, 28) = 0.24, p = .63, lescents with excess weight increased their “inhibition
η2p = 0.01. errors” (FDT), F(1, 29) = 25.38, p < .001, η2p = 0.467, and,
marginally, their “shifting errors” (FDT), F(1, 29) = 4.15,
Executive Functions p = .051, η2p = 0.13.
During the pre-TSST evaluation, excess weight partic- Discussion

ipants showed greater scores in the inhibition condi-
tion of FDT (i.e., lower inhibition) than normal-weight Adolescents with excess weight, compared with those of
participants (t = 2.08, p = .042, δ = 0.54). No other normal weight, showed impairments in measures of inhi-
significant differences arose during pre-TSST (see bition and shifting, and higher subjective stress levels, in
Table 1). Significant Time × Group interactions were response to the TSST. Furthermore, adolescents with
found for Letter-Number Sequencing, F(1, 58) = 16.82, excess weight showed a differential psychophysiologi-
p < .001, η p = 0.23 (Fig. 3); “inhibition errors” in FDT,
2
cal pattern during the TSST. HR increased during the
F(1, 58) = 31.34, p < .001, η2p = 0.35; “shifting errors” negative social evaluation phase (relative to the positive
in FDT, F(1, 58) = 10.80, p = .024, η2p = 0.08 (Fig. 4); phase) in this group, while no change was observed in
and “shifting score” in FDT, F(1, 58) = 15.47, p = .039, adolescents with normal weight. SC decreased in ado-
η2p = 0.07. Adolescents with normal weight signifi-
lescents with normal weight from the positive to the
cantly increased their performance after the TSST in
Letter-Number Sequencing, F(1, 29) = 26.14, p < .001,
Fig. 1. Mean heart rate (beats per minute [BPM]) during the Fig. 3. Working memory scores (Letter-Number Sequencing)
positive and negative social evaluation phases of the Trier Social before and after the Trier Social Stress Task. Bars indicate stand-
Stress Task. Bars indicate standard error of the mean. ard error of the mean.

on 22 June 2018
stressful situations evoke negative mood states and

impair impulse control. The joint influence of executive
deficits and emotional eating patterns would lead to fur-
ther eating disinhibition. However, no previous studies
have analyzed the effects of emotional states on execu-
tive functioning in adolescents with excess weight.
Inhibition, shifting, and working memory were nega-
tively affected by social stress in our excess weight ado-
lescents. This suggests that social stress has a detrimental
impact on executive functioning in these adolescents,
and this may influence their eating behavior. Usually, in
pre–post cognitive evaluations, performance improves in
Fig. 4. Inhibition and shifting errors (Five Digit Test) before and the second evaluation due to practice effects arising from
after the Trier Social Stress Task in normal weight (NW) and
excess weight (EW) adolescents. Bars indicate standard error of repeated administration [36, 37]. In fact, in this study,
the mean. working memory improved significantly in the normal
weight group from the pre- to post-TSST evaluation.
negative social evaluation phase, suggesting habituation However, adolescents with excess weight did not benefit
to the situation, but did not change in adolescents with from this learning experience, and in fact, their perfor-
excess weight. SC is a variable that usually displays a mance decreased. A previous study [27] using the same
decrease over the recording period, denoting habituation experimental protocol also found increases in attention
to the situation. A flat recording, without any sign of performance in normal weight participants from the
decrease, is usually interpreted as indicating a high elec- pre- to post-TSST evaluation, while excess weight par-
trodermal level [33]. ticipants were unable to benefit from the practice effect.
Our findings suggest that overweight or obese adoles- These results may be due to the greater levels of stress
cents have enhanced sensitivity to social stressors. This during the TSST in adolescents with excess weight.
is manifested both at subjective and physiological levels. Stress negatively affects abilities that require conscious
Subjectively, the greater increase in stress levels indicates attention and effortful information processing, reduc-
that adolescents with excess weight perceive the situation ing therefore cognitive efficiency [38]. Greater cortisol
as more stressful than do adolescents with normal weight. responses to the TSST were found in the previous study
At the physiological level, results indicate a greater mobi- [27], and results of the present study showed higher HR
lization of physiological resources and autonomic reac- and electrodermal reactivity to the social stress task in
tivity during social stress, particularly during negative adolescents with excess weight. Furthermore, auto-
social evaluation, in adolescents with excess weight. The nomic reactivity after TSST, specifically electrodermal
most common motivation for using a public speaking response, correlated inversely with working memory
task is that it elicits a social evaluation–related threat [34]. performance in the whole sample. Therefore, the greater
The inclusion of the two phases of the TSST as a func- autonomic and stress response in adolescents with excess
tion of feedback from the audience (positive vs. negative) weight can increase stress interference in this group and
allowed for a more specific analysis of social evaluation, therefore lead to a deficit in learning from the repeated
making our results more innovative. Taken together, these administration of the tasks.
results support the utility of differentiating between posi- Executive functioning may have multiple direct and
tive versus negative social evaluation during the TSST for indirect influences on obesity in adolescence. Although
the study of the impact of social stress on autonomic and available evidence links executive functioning and obe-
cognitive functions. sity [24, 39], the specific mechanisms mediating this asso-
The observed negative impact of social stress on ciation are less well-known. Some studies have found that
executive functioning in adolescents with excess weight executive dysfunction is associated with obesity-related
is consistent with a previous study that showed impaired behaviors in childhood and adolescence via increasing
attention after TSST in adolescents with excess weight intake, disinhibiting eating, and reducing physical activ-
compared with adolescents with normal weight [27]. ity. The inability to inhibit impulses predicted higher
Negative emotional states in adults are known to impair food intake, a higher body weight and less weight loss
cognitive capacity; for example, depressive symptoms after a weight reduction intervention [40]. Deficits in
in people with obesity impair executive function [35]. inhibition can affect impulse control and thus the cap-
Furthermore, emotional eating patterns, which are acity to restrict intake of appetizing foods (high fat/
more prevalent in this population [15], may addition- sugar). Impairments in shifting may influence the cap-
ally affect executive functioning. Specifically, socially acity to regulate and modify eating behaviors to prevent

on 22 June 2018
harmful health consequences. Furthermore, this deficit and normal weight individuals [15]. This discrepancy
may lead to adolescents with excess weight persisting in may be due to the noninclusion of specific positive–neg-
their unhealthy eating habits. Impairments in working ative evaluation phases in their TSST, or may reflect a
memory could affect the ability to maintain cognitive greater vulnerability to social stress in adolescents than
control, making it more difficult to engage in healthy adults. In line with the greater autonomic response found
activities and intervention programs. Finally, disinhibited in our study, a greater cortisol response after the TSST
eating in obese adolescents was associated with reduced has been previously found in excess weight than in ado-
orbitofrontal volume and executive dysfunctions, which lescents with normal weight [27].
were most pronounced in terms of working memory and Executive functioning is still developing during ado-
inhibition [41]. Conversely, executive function skills were lescence, as prefrontal areas reach full development at
positively associated with healthy eating habits, such as maturity [45]. A growing body of literature suggests an
fruit and vegetable intake, and physical activity [42, 43]. altered balance between the earlier-developing limbic
We observed group differences before social stress only system and the later-developing frontal/executive system
in the “inhibition score” (FDT), with lower performance [46] during adolescence. Furthermore, in this period,
in excess weight adolescents. However, no differences the opinions of peers and general social evaluation
were found in shifting or working memory. These results become a central aspect for self-image development [47].
are concordant with a previous study reporting selective Adolescents with excess weight frequently suffer from
alterations in inhibition in adolescents with obesity ver- negative social evaluations and social stressors during
sus normal weight adolescents [43]. Another study found their everyday lives, which may lead to greater vulnera-
selective alterations in inhibition and shifting, but not bility to social stress, especially if a negative social evalu-
working memory, in excess weight and obese adolescents ation component is included. It would be reasonable to
[24]. In contrast, other authors found significant differ- assume that adolescents with excess weight would show
ences between obese and normal adolescents in working a blunted stress response due to habituation to repeated
memory as well as attention, but not in intelligence or stress exposure. However, previous studies using this
verbal fluency [44]. Discrepancies between studies may same TSST protocol found greater increases in salivary
be due to differences in testing methods, samples, and cortisol in excess weight than in normal weight adoles-
levels of BMI. cents [27]. These results suggest the development of a
As expected, the change in subjective stress was posi- sensitization process to social stress in adolescents with
tively associated with the change in HR, SC, and “inhibi- excess weight.
tion errors” (FDT). This suggests that levels of subjective Therefore, due to all of the factors listed above, ado-
stress may modulate both psychophysiological responses lescents with excess weight are an important target group
and executive-inhibition functions. In this way, negative for cognitive interventions based on stress regulation
social evaluations may induce a greater increase in stress strategies, executive function improvement and preven-
levels and autonomic responsiveness, and a reduction tion of harmful eating behaviors. In this regard, some
of inhibition capacity, in excess weight adolescents rela- evidence already suggests that executive functioning
tive to those with normal weight. The deleterious influ- training for obese children can improve working mem-
ence of negative social evaluation on executive control ory, inhibition, and shifting, being useful in weight-loss
in adolescents with excess weight may exacerbate diffi- maintenance [48].
culties in eating behavior control, eventually triggering Regarding its strengths, our study used an innovative
overconsumption. strategy to evaluate the impact of social stress, particu-
The change in HR during social evaluation was pos- larly negative social evaluation, on adolescents with excess
itively associated with the change in “shifting errors,” weight, as well as the inclusion of autonomic variables
“inhibition errors,” and “shifting score” in the whole as objective indices of stress. Among the limitations, we
sample. The change in SC was negatively associated with used a virtual reality audience in our TSST instead of the
the change in Letter-Number Sequencing performance actual public, which might have decreased the realism of
(i.e., greater habituation of SC was associated with bet- the situation and the stress-elicited responses. However,
ter working memory). These results suggest that modula- this version of the TSST was validated in previous stud-
tion of autonomic activity by social stress may index, or ies and produced a reliable stress response [26, 27, 31].
additionally influence, executive functioning in adoles- Furthermore, the inclusion in future studies of a non-
cents with excess weight. This harmful effect on execu- stress control condition (also with two cognitive evalua-
tive functioning may lead to problems in real life, such tions) is recommended to rule out more possible general
as poor regulation of eating habits. However, studies in disruption of cognitive processes in excess weight ado-
adults also using the TSST did not find differences in lescents. Regarding the study design, the absence of
HR, blood pressure, or cortisol responses between obese any counterbalancing of the order of presentation of

on 22 June 2018
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Ethical Approval All procedures performed in this study involv- P. Peer victimization during adolescence: Concurrent and
ing human participants were in accordance with the ethical stand- prospective impact on symptoms of depression and anxiety.
ards of the Ethics Committee of the Universidad de Jaén and with Anxiety Stress Coping. 2015;28:105–120.
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19. Puhl RM, Luedicke J, Heuer C. Weight-based victimization
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20. Cramer P, Steinwert T. Thin is good, fat is bad: How early
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Standards The authors declare no conflicts of interest. 21. Gunnarsdottir T, Njardvik U, Olafsdottir AS, Craighead L,
Bjarnason R. Childhood obesity and co-morbid problems:
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Exceso de peso en adolescentes: inﬂuencia del estrés social en el rendimiento

Thesis · October 2018

Maria Moreno Padilla

The user has requested enhancement of the downloaded file.

MARÍA MORENO PADILLA

Dr. Gustavo. A Reyes del Paso

JAÉN, 5 JULIO DE 2018

María Moreno Padilla

Gustavo A. Reyes del Paso, Catedrático de Personalidad, Evaluación y Tratamiento

Psicológico de la Universidad de Jaén (España), María José Fernández Serrano,

Profesora de Metodología de las Ciencias del Comportamiento de la Universidad de

Jaén (España) y Antonio Verdejo García, Profesor en School of Psychological Sciences

en la Universidad de Monash (Australia)

en el rendimiento neuropsicológico y efecto de la visualización de imágenes de

alimentos en la activación cerebral y toma de riesgos.”, realizada por la doctoranda

de calidad, originalidad y rigor científico necesarias para que se proceda a su defensa

pública de acuerdo con la legislación vigente.

Fdo. Gustavo. A Reyes del Paso

Fdo. María José Fernández Serrano

Fdo. Antonio Verdejo García

Jaén, a 5 de Julio de 2018.

Caminante, son tus huellas

dar. Porque al final el aprendizaje es precisamente eso, equivocarte, volver un poco

nuestras decisiones las que van construyendo nuestro propio sendero.

que sigas caminando.

que hicieron más fácil recorrer este camino.

En primer lugar, quería agradecer a mis directores de tesis el brindarme la oportunidad

de aprender de ellos y realizar este trabajo bajo su tutela. A Gustavo, porque no he

lo he necesitado. Te estaré siempre agradecida por todo lo que me has enseñado. A

Antonio, por permitirme adentrarme en un mundo desconocido como era para mí el

Deseo también expresar mi agradecimiento a la Universidad de Jaén por haber facilitado

que componen este trabajo.

Gracias también a mi supervisor de Estancia Pre-doctoral Robert Whelan, por darme la

oportunidad de visitarles y acogerme durante 3 meses en el Instituto de Neurociencias

y por hacerme sentir afortunada de tener su amistad.

aprendido de mis clases al igual que yo lo he hecho de la experiencia tan gratificante

Mar. La conocí en mi primer congreso, en Cádiz, y desde ahí compartimos experiencias

ha unido, pero ya caminemos siempre juntas.

siempre. Todavía nos quedan muchas aventuras por vivir amiga.

levantarme, siempre me han querido de manera incondicional y eso, en un mundo en el

conmigo desde el origen del camino, no hubiera sido posible. Os quiero.

el camino, GRACIAS. Te quiero.

El aumento en la prevalencia de la obesidad se ha convertido en las últimas décadas,

según la Organización Mundial de la Salud, en uno de los principales problemas de

salud pública a nivel mundial. La obesidad es una condición compleja en la que

intervienen multitud de factores.

En la antigüedad, las personas regulaban su ingesta según sus estados metabólicos de

comer se ha convertido en una cuestión de toma de decisiones. Estudios recientes

apuntan a que el cambio en el estilo de vida actual, basado en el sedentarismo y hábitos

alimenticios no saludables, es el responsable del drástico aumento de la prevalencia de

El exceso de peso y la obesidad también han aumentado exponencialmente en la

infancia y la adolescencia, etapas críticas en el desarrollo del individuo. La adolescencia

es una etapa en la que el individuo es especialmente vulnerable debido a sus

peculiaridades comportamentales. En esta etapa son frecuentes los comportamientos

dirigidos a la búsqueda de recompensa y propensión al riesgo, así como una

disminución del control ejecutivo y la capacidad de regulación efectiva del

comportamiento. En este sentido, distintos estudios confirman la existencia de

alteraciones en el funcionamiento ejecutivo en adolescentes con exceso de peso

una mejor regulación del comportamiento, y específicamente, del comportamiento