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Review Article
Developing Attention: Behavioral and Brain Mechanisms
Correspondence should be addressed to Michael I. Posner; [email protected] and Mary K. Rothbart; [email protected]
Copyright © 2014 Michael I. Posner et al. This is an open access article distributed under the Creative Commons Attribution
License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly
cited.
Brain networks underlying attention are present even during infancy and are critical for the developing ability of children to
control their emotions and thoughts. For adults, individual differences in the efficiency of attentional networks have been related
to neuromodulators and to genetic variations. We have examined the development of attentional networks and child temperament
in a longitudinal study from infancy (7 months) to middle childhood (7 years). Early temperamental differences among infants,
including smiling and laughter and vocal reactivity, are related to self-regulation abilities at 7 years. However, genetic variations
related to adult executive attention, while present in childhood, are poor predictors of later control, in part because individual
genetic variation may have many small effects and in part because their influence occurs in interaction with caregiver behavior and
other environmental influences. While brain areas involved in attention are present during infancy, their connectivity changes and
leads to improvement in control of behavior. It is also possible to influence control mechanisms through training at any time of life.
The relation between maturation and learning may allow advances in our understanding of human brain development.
Table 1: Correlations between temperament measures at 7 months Table 2: Relating attention networks to dominant modulators and
and ANT scores at 7 years. relevant genes.
to sensory and motor brain areas [31, 32] that would be control through orienting ends with the preschool transition.
targets of the orienting network. While there is evidence that We view adults as having dual control. Looking away from
some of these resting state studies may be confounded by disturbing or highly arousing events is clearly a major
greater movement that can occur in younger subjects [33], coping strategy in adults. However, the growing influence
in our view it seems unlikely that this artifact will change of executive control allows the person’s internally controlled
the conclusions discussed above. However, the problems that goals to become generally dominant.
occur with any one imaging method support the approach of
relating different imaging methods [34] and establishing their 4.2. Control of Emotion and Cognition. The structural con-
connections to behavior as we have sought to do in this paper. nectivity of the anterior cingulate reflects its control functions
We think the relatively slow development of long-term [6, 18]. The ventral portion of the ACC and adjacent orbital
connections to distant brain areas allows the executive net- frontal cortex connects mainly to limbic regions and its
work to provide more control at later ages. Indeed direct function is thought to be related to control of emotions
evidence on this point came from a study of 7-month-old [6, 42]. The more dorsal part of the cingulate connects
infants viewing visual displays [35]. They oriented longer more strongly to cortical areas in the frontal and parietal
when the display was in error [36] and this behavior was lobes. This is reflected in evidence of increased connectivity
associated with a set of scalp electrodes at the frontal midline between the dorsal ACC and auditory areas when attending
which localized to the anterior cingulate, an important node to speech, while a switch to visual input is reflected in
of the executive network. However, the lack of connections of increased connectivity between the ACC and occipital lobe
the cingulate to remote areas was shown in an inability to use [43]. The developmental data cited in the last section [40, 41]
error to control behavior. The most frequent adult response to support separate functions for the ventral and dorsal ACC
a self-made error is to slow down during the next trial [37]. and show they both develop strongly between 5 and 8 years
We traced the evidence for this kind of control and found that of age.
it emerged around three years of age and was not found at the We want to understand the origins of cognitive and
age of 2 [38]. emotional controls in the developing infant and child. As
The growing behavioral influence of executive control is mentioned previously, one important function of the anterior
shown in an MRI study of the resolution of conflict in the cingulate is to play a role in the detection of error [44].
flanker task [39] by 725 children from 4 to 21 years [40]. From Error detection found at 7 months may reflect either the
4 to 8 years, ability to resolve conflict was positively related cognitive or emotional aspects related to the violation of
to the size of the anterior cingulate. Beyond the age of 8, expectation. However, studies using high density scalp EEG
the connectivity of the anterior cingulate was correlated with at 4–6 years suggest that the resolution of conflict at 4
the speed of response. The brain and behavior correlation in years involves primarily ventral areas of the cingulate [45,
early childhood was similar to our finding that flanker task 46]; later more dorsal areas become involved. In addition,
performance showed a specific improvement in children of studies of resting state MRI in infancy suggest a node in
6–8 years, but reaction time in the task continued to improve the midprefrontal cortex adjacent to emotional parts of the
until adulthood [11]. A different study [41] used emotional ACC [30]. This evidence fits with the idea that emotional
responses to a fear face during a rewarded go/no-go task to control develops more quickly than cognitive control during
explore the role of brain connectivity in regulation of the early life, although there is strong overlap in their later
amygdala from the ventral anterior cingulate. They found development. While the data are not completely clear on this
a significant correlation between age and the efficiency of point, it is of obvious importance to parents in fostering the
connectivity between the ventral ACC and amygdala during development of these controls.
the presentation of fear faces.
The major change in connectivity took place between
ages 5 and 7. These studies show substantial overlap in age 5. Early Temperament Predicts Later Control
between development of purely cognitive and emotional
self- regulation. We do not believe that the flanker task By temperament, we mean constitutionally based individual
and emotional go/no-go tasks index the full development of differences in reactivity and self-regulation [47]. At 7 months,
control mechanisms, since more complex tasks may show we used a parent report scale, the Infant Behavior Question-
longer periods of development, but these studies do provide naire (IBQ), which heavily weighs reactive responses of the
strong confirmation of growing executive system control infant, although it does provide a measure of orienting that
during early childhood and the close correspondence of brain involves an early control network.
connectivity to behavioral performance.
In summary, we have discovered a transition between 5.1. Predicting Attention Networks. We found surprisingly
the brain networks responsible for control at 7 months and high and significant correlations between temperament mea-
those at 4 years and later. At 7 months, control involves sures at 7 months and performance on the attention network
the orienting network, but by 4 years the executive network test at 7 years. Our surprise reflects the fact that these
dominates. Behaviorally, the orienting network involves sen- correlations are found over an extended time course during
sory stimulation and we believe this is a major reason why which there is considerable neural maturation and they
infants show control by external stimulation provided by also involve parent report during infancy and behavior in a
caregivers and sensory events. We also do not believe that cognitive reaction time task (ANT) during childhood. These
Advances in Neuroscience 5
correlations must be regarded as tentative, however, since cognitive tests and parent reported effortful control support
they involve only sixteen of the seventy infants who remained the relation of early reactive emotion in infancy to control
in the study when the ANT was measured at 7 years of age. systems of childhood.
The small remaining samples are partly self-selected (some The correlations found between parent reported temper-
loss resulting from moving away may have been involuntary) ament at 7 months and ANT performance at 7 years were as
from the larger number of infants involved at 7 months. high or higher than those found between temperament at the
Separate aspects of temperament were related to each of two ages. It is possible these high correlations are due to the
the attention networks. For a correlation matrix, see Table 1, unique nature of the 16 families who persisted from 7 months
and in what follow we report significant correlations. Infants’ to 7 years. Comparison of those infants who remained in
perceptual sensitivity to the environment (.56) and duration the study until the age of 7 with those who dropped out
of orienting (.55) were correlated with ANT scores of the did not reveal any striking differences, although there was
alerting network at the age of 7 years. While we did not some evidence that the parents continuing with the study
predict that parent ratings of orienting would be related to were more committed to timely submission of questionnaires
the alerting network rather than the orienting network, this than those who dropped out. Moreover, we found neither
may reflect dependence of orienting on alertness during the significant demographic nor behavioral differences between
infancy state when sleep occupies so much of the day. the 20 persistent families and the 50 who were involved at 7
Infant approach behavior (.76) and soothability (.56) years but not at 7 months.
as rated by parents were correlated with ANT scores for However, the 16 children who had participated at 7
the orienting network at the age of 7. As we have seen months were faster in ANT performance than the new
previously, orienting as reported by parents and measured in recruits. Since faster speed of responding is frequently related
the laboratory can be used to control emotional reactivity in to better overall performance, this finding suggests that the
infancy, and this aspect seems to predict the skill of taking 20 children who persisted from time 1 were relatively high
in sensory information later in life. Soothability as reported performing children. This effect was probably not due to
by the parent may reflect both the child’s propensity and practice, since a direct comparison of performance on the
the parent’s skill. This could mean that the parents’ ability ANT at the age of 7 of children who had also taken the test
to provide emotional soothing to the child is an important at the age of 6 and those who had not practiced it previously
determinant of cognition via the orienting network. showed no differences in speed. The speed differences may
The scales of infant smiling and laughter (−.60), vocal have reflected recruitment of lower SES families at the age of
reactivity (−.64), and cuddliness (−.64) were negatively cor- 7 years than we had previously recruited or other unknown
related with the ability to resolve conflict and, in addition, the characteristics of the persistent families. A more interesting
higher order factor of positive affect that contains these scales possibility is that early positive emotional reactivity reflects
was also negatively correlated with ANT conflict at 7 years. particularly predictive long-lasting feature of child behavior.
Multiple regression indicates that these factors could account One possible mechanism for the strong influence of early
for about 50 percent of the variance in the difference between positive emotion on later control is that more reactive
reaction time in incongruent and congruent flankers. children in infancy come to control their positive emotions
In addition, negative affect measured in infancy is corre- more strongly and that this transfers to cognitive control as
lated with the total errors found in the ANT at the age of 7. It is measured by the ANT.
interesting that positive affect was related to the speed of the
children’s response, which may largely reflect the efficiency of
white matter connections [40], while negative affect predicted 5.2. Role of Genetic Variation. We have pursued two strategies
the errors that arise due to competition from the incompatible to help understand how genes are related to the individual
flankers. efficiency of attention networks. One approach involves
Many older ideas of temperament are based on stability adults and uses the association of attentional networks with
between childhood and adults traits. However, Rothbart and particular neuromodulators. These associations have led to
Derryberry [47] suggested that we should expect tempera- identification of candidate genes that relate to each network.
ment to change as new neural systems come on line. They The results were summarized by Green et al. [28] and are
recognize that there is stability, but change is be expected as shown in Table 2. A number of other results have qualified the
a consequence as neural systems and connections are estab- view of Green et al. somewhat. It seems clear that serotonin
lished. A number of the temperament correlations between as well as dopamine can influence the executive atten-
infancy and childhood in the previous literature support the tion network [50] and that there are interactions between
ability to predict control in children from infant emotion. dopaminergic and cholinergic genes at the molecular level
Putnam et al. [48] found that positive emotion in infancy is that modify the degree of independence between them [51].
related to later parent reports of their child’s effortful control Nonetheless, the scheme in Table 2 provides a degree of
and that infant surgency (smiling and laughter and approach) organization and prediction that is often lacking in studies
predicted high effortful control in toddlers. Komsi et al. [49] of genetic influences on cognition and behavior.
also found that infant smiling and laughter predicted effortful In our longitudinal study, we examined genetic variation
control in children when they were 5 years old. In addition, in twelve genes that had been related to attention in adult
the overall orienting measure in infancy predicted 7-year-old studies (see Table 2 and [52]). The children had been evalu-
soothability, effortful control, and interest. Thus, both ANT ated when they were 7 months old, and genotyping took place
6 Advances in Neuroscience
when they returned to the laboratory at 18–20 months. We The developmental process through which attention net-
also genotyped all of the children at 7 years. We compared works and self-regulation mature is very complex. There
the results at two ages to be sure of high replication of our are many changes in brain structure and function that may
classifications. We found supportive evidence for some of be related to the multiple changes in voluntary behavior in
the genes discussed in Table 2. The COMT gene was related early development. As discussed previously, an increasingly
to number of anticipatory looks at 7 and 18 months [53]. popular way of tracing brain changes is to use resting state
The DRD4 7 repeat allele was not related to our attention MRI to characterize how the brain changes in development
measures in infancy or among toddlers but did relate to [30, 59]. In our recent work, we have tried to relate behavior
effortful control at the age of 4 [54]; [55]. This discontinuity changes to changes in functional connectivity [4].
likely reflected the change in networks of control from The changes in connectivity during development
orienting to executive control that we found between 2 and reported in resting state MRI studies involve functional
4 years of age. connectivity based upon correlations between BOLD activity
In addition, parenting quality at 18–20 months was exam- in separated brain areas. There is also evidence of actual
ined through observation of caregiver-child interactions in physical changes in the white matter thought to underlie
which the children played with toys in the presence of one of these correlations [34]. Our recent training work with adults
their caregivers. Raters reviewed videotapes of the caregiver- using diffusion tensor imaging (DTI) has uncovered white
child interaction and rated the parent on five dimensions matter changes that have some similarities to those found
of parenting quality according to a schedule developed in development. Changes in connectivity surrounding the
by NICHD [56]: support, autonomy, stimulation, lack of ACC have been shown to be critical to improved reaction
hostility, and confidence in the child. According to their time in the flanker task during development [40]. Training
scores, parents were divided at the median into two groups: adults might thus allow us to uncover how connections
one showing a higher quality of parenting and the other a developing during childhood support the changes in self-
lower quality. control between infancy and adulthood.
We reported previously (Sheese et al., 2009 [57]) that During development, there is a large change in the
variations in COMT, SNAP25, CHRNA4, and DRD4 were physical connections between brain areas. The density of
related to elements of emotion during infancy (age of 7 axons in pathways connecting brain areas increases, followed
months) and during the toddler period (18–20 months). by an increase in the myelin sheath that surrounds the axons
COMT was related to positive affect including smiling and and provides insulation. Together, these changes result in
laughter and high intensity pleasure at 7 months. SNAP 25 more efficient connections [60]. Fractional anisotropy (FA)
was related to negative affect, mainly distress at 7 and 18 is the main index for measuring the integrity of white matter
months. CHRNA 4 was related to effortful control at 18 fibers when using DTI.
months and DRD4 was related to sensation seeking at 18 In our work, we studied FA in college students before
months. and after a form of mindfulness meditation called integrated
However, unlike the temperament measure of emotion body mind training (IBMT) in comparison to a control
to which the genetic variations were often related, there group given the same amount of relaxation training. We
was, little evidence that the genetic variations by themselves found clear improvement in the executive attention network
predicted behavior at 7 years on the ANT. A recent meta- after only five days of training [61]. After two to four weeks
analysis of studies of twins indicates that genetic factors that of training, we found significantly greater change in FA
influence cognition at one point are largely different from following meditation training than following the relaxation
those at later times (see, [58], p. 19). Our studies suggest training control. This change was found in all white matter
that shifts in control networks and gene X environment tracts surrounding the ACC, but not in other brain areas [62].
interactions may be among the reasons for this lack of This was particularly striking because one of these pathways,
prediction in early life. the anterior corona radiata, has previously been reported
to be correlated with individual differences in the ability to
resolve conflict using the ANT [15].
These alterations in FA could originate from several
6. Simulating Development through Training factors, such as changes in myelination, axon density, axonal
membrane integrity, axon diameter, intravoxel coherence
Development in the title of this paper refers both to changes of fiber orientation, and others. Several DTI studies have
in attention through the natural maturation of the brain and examined axial diffusivity (AD) and radial diffusivity (RD),
to our efforts to develop attention through training. Below we the most important indices associated with FA, to understand
discuss similarities between the development of white matter the mechanisms of FA change [63, 64]. Changes in AD are
pathways between infancy and childhood with the influence associated with axon morphological changes, with lower AD
of meditation training on adult white matter. It is our hope value indicating higher axonal density. In contrast, RD relates
that efforts to train attention may help us to better understand to the myelin insulation surrounding the axons. Decreases
the process of infant and child development. As we have in RD imply increased myelination, while increases represent
seen, parenting influences this development, and we hope to demyelination.
better inform parents about what can be done to improve this In our study [65], we investigated AD and RD where FA
process. indicated that integrity of white matter fibers was enhanced
Advances in Neuroscience 7
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