Reduced prefrontal hemodynamic response in children with

ADHD during the Go/NoGo task: a NIRS study

Yuki Inoue
a,c
, Kotoe Sakihara
a
, Atsuko Gunji
a
, Hiroshi Ozawa
c
,
Satoshi Kimiya
b
, Haruo Shinoda
d
, Makiko Kaga
a
and Masumi Inagaki
a
The current study examined the hemodynamic response
during the Go/ NoGo t ask in chil dren with/ without att enti on
deficit / hyperactivity disorder (ADHD). Using near-infrared
spectroscopy, oxy-Hb and deoxy-Hb concentrati on
changes in the frontal areas were compared during the
conditi ons with/ without inhi bitory demand. Compared
with typically devel oping chil dren, chil dren with ADHD
showed si gnificantly reduced activati on during the
conditi ons with inhi bitory demand (NoGo-conditi on)
in the front al areas. However, no si gnificant diff erences
in activati on during the conditi ons without inhi bitory
demand (Go-conditi on) were found between the two
groups. The current findings reveal ed that chil dren
with ADHD exhi bit an alt ered hemodynamic response
specifically during response inhi biti on, but not
during response executi on, and suggest ed the clinical
usefulness of near-infrared spectroscopy for the
eval uati on of response inhi biti on deficits in chil dren
with ADHD. NeuroReport 23:5560 c 2012 Wolt ers Kl uwer
Health | Li ppincott Willi ams & Wil kins.
NeuroReport 2012, 23:5560
Keywords: att enti on-deficit / hyperactivity disorder, Go/ NoGo paradi gm,
near-infrared spectroscopy, response inhi biti on
a
Department of Developmental Disorders, National Institute of Mental Health,
National Center of Neurology and Psychiatry (NCNP),
b
Shimada Ryoiku Center,
c
Department of Child Psychiatry, Shimada Ryoiku Center Hachiouji and
d
Faculty
of Psychology, Rissho University, Tokyo, Japan
Correspondence to Dr Yuki Inoue, MD, PhD, Department of Child Psychiatry,
Shimada Ryoiku Center Hachiouji, 4-33-13 Dai-machi, Hachiouji,
Tokyo 193-0931, Japan
Tel: +81 42 634 8511; fax: +81 42 634 8512;
e-mail: [email protected]
Received 21 September 2011 accept ed 20 October 2011
Introduction
Attention-deficit/hyperactivity disorder (ADHD) is a
developmental/behavioral disorder characterized by poor
attention, hyperactivity, and impulsivity that affects 37%
of the pediatric population [1]. A neuro-cognitive model
of ADHD has been based on disrupted behavioral
inhibition. Barkley developed a conceptual model of
ADHD that links behavioral inhibition, which comprises
three inhibitory functions: inhibition of a prepotent
response; stopping of an ongoing response; and inter-
ference control [2]. More recently, Sonuga-Barke [3]
postulated the Dual pathway model, which comprises
two functional pathways: in one, ADHD is a disorder of
executive function dysregulation, and in the other, it is a
motivational deficit with delay aversion. In both models,
the deficit of inhibitory function is regarded as a key
feature of ADHD. Besides these models, working
memory deficit is also considered to be one of the core
deficits of ADHD. Some neuroimaging studies have
examined the neural basis of working memory deficit of
the disorder [4,5].
To evaluate the cognitive features of ADHD, a series of
neurophysiological and neuroimaging studies involving
inhibitory tasks have been reported. The event-related
potential has been repeatedly examined in children with
ADHD, who show attenuated amplitudes of inhibitory
components (NoGo-N200 and P300) [68]. Moreover, a
one-source localization study of inhibitory event-related
potential revealed a group effect in the ADHD and
control groups in the right dorsolateral prefrontal cortex
(PFC) [9]. Also, functional MRI (fMRI) studies revealed
reduced activation in inhibitory trials in the ventrolateral
and dorsolateral prefrontal cortical areas [10,11], the
striatal region [12], and the presupplementary motor
area [13] of children with ADHD. Suskauer et al. [13]
also reported that these activation differences between
the ADHD and the control groups were not observed
for Go-stimuli, showing that this activation difference for
NoGo-stimuli is associated with response inhibition, not
the motor response.
Also, previous near-infrared spectroscopy (NIRS) studies
have investigated the frontal lobe function in chil-
dren [1416] and adults with ADHD [5]. Negoro et al.
and Jourdan Moser et al. reported that the prefrontal
hemodynamic response was altered in children with
ADHD [14,16] during the Stroop task, which involves
interference control [2]. However, to our knowledge, no
NIRS studies of children with ADHD have ever involved
the Go/NoGo task, which involves inhibition of the
prepotent response [2]. However, Herrmann et al. [17]
succeeded in detecting frontal lobe activation in normal
adults engaging with the Go/NoGo task by NIRS
measurement. They found significantly higher increase
in [oxy-Hb] and decrease in [deoxy-Hb] in the bilateral
inferior frontal cortex during the inhibition phase of the
Go/NoGo task. In the current study, we examined the
hemodynamic response during the Go/NoGo task in
children with and without ADHD. If we could detect the
Cognitive neuroscience and neuropsychology 55
0959-4965 c 2012 Wolters Kluwer Health | Lippincott Williams & Wilkins DOI: 10.1097/WNR.0b013e32834e664c
Copyright Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
altered NIRS finding in the prefrontal area of ADHD
children, which would be consistent with previous fMRI
studies, the current study would increase the possibility
of the clinical usefulness of NIRS measurement for the
evaluation of inhibitory function in children with ADHD.
Methods
Participants
Forty children, inclusive of 20 with ADHD (six females
and 14 males; eight with predominantly inattentive type
and 12 with combined type; mean age, 9 years 7 months;
range, 614 years) and 20 with typical development (six
females and 14 males; mean age, 9 years 9 months; range,
614 years), participated in this study. Children with
ADHD were recruited from among patients who were
referred to the Department of Child Neurology, National
Center Hospital, National Center of Neurology and
Psychiatry, Kodaira, Tokyo, Japan, and the Shimada
Ryoiku Center, Tama, Tokyo, Japan. The diagnosis was
confirmed by two child neurologists and one child
psychiatrist according to the Diagnostic and Statistical
Manual of Mental Disorders, fourth edition criteria [1].
Paid volunteers were recruited from neighboring ordinary
elementary and junior high schools as typically developing
children (TDC). The intelligence quotients of the
ADHD children were determined by means of the
Wechsler Intelligence Scale for Children, third edition [18].
Raven Colored Progressive Matrices [19] were used in
both groups. No participants exhibited significant sensory
or neurological limitation, epilepsy, mental retardation
(FIQ<70, Wechsler Intelligence Scale for Children, third
edition), or a pervasive developmental disorder. No
ADHD children had undergone pharmacotherapy before
the NIRS experiment. The research protocols were
approved by the ethical committees of the National
Center of Neurology and Psychiatry and the Shimada
Ryoiku Center. Written informed consent was obtained
from the children and their parents following a full
explanation of the experiment.
Task procedure
We used the Go/NoGo task software MOGRAZ
(NoruPro Light Systems Inc., Tokyo, Japan) [20]. Every
stimulus picture (a mole with/without sunglasses), with a
visual angle of 101, appeared in the center of a 21-inch
CRT monitor. The stimulus duration was 500 ms and the
interstimulus interval was randomly varied between 750
and 1250 ms. Each participant was instructed to respond
with the index finger of his/her dominant hand as soon as
possible whenever he/she saw a mole with sunglasses
(Go-stimulus) and not to respond to a mole without
sunglasses (NoGo-stimulus).
The current task involved two conditions (Fig. 1). In the
Go-condition, all stimuli were Go-stimuli throughout the
2-min task. In the NoGo-condition, Go-stimuli appeared
with a probability of 50% throughout the 2-min task. The
participants were asked to focus on the CRT monitor with
their minds blank while a 15-s baseline recording was
performed. Then, after completion of a certain condition
(Go-condition or NoGo-condition), they were told to focus
on the CRT again for another 30s. The order of the two
conditions of the task was counter-balanced. Four behavioral
variables [reaction time (RT, ms), reaction time variability
(RTV, ms), omission error rate (OE, %), and commission
error rate (CE, %)] were automatically recorded.
NIRS measurements
We used a 16-channel NIRS device cognoscope (NIM
Inc., Philadelphia, Pennsylvania, USA) to measure the
relative changes in [oxy-Hb] and [deoxy-Hb]. The NIRS
probe consisted of four light sources and ten detectors. The
detectors covered an area of 14 3.5cm on the forehead.
The probe was positioned as it was in the previous
study [21], which involved the same type of NIRS
equipment as that in the current study. The line of four
light sources was set on the FP1FP2 line (International
1020 System). Also, the very center of the probe was
positioned on Fpz (Fig. 2). The setup was designed to
image the PFC including the frontal pole, orbitofrontal
cortex, and the ventromedial-prefrontal and ventrolateral-
prefrontal cortices [22].
Each light source contained two LEDs (wavelengths: 730
and 850 nm; sampling rate: 3 Hz). The measurement
principles were based on the modified BeerLambert law,
for which the [oxy-Hb] and [deoxy-Hb] changes are
calculated from the change in light attenuation at a given
measured point. The sourcedetector distance was
2.5 cm. To correct a drift change of [Hb] over time,
baseline correction by linear fitting was performed for
each channel based on the two baseline data: the mean of
10-s periods before/after the task section. For statistical
analysis, we averaged all the time points of [oxy-Hb] and
[deoxy-Hb] changes during the task section. Then, as
performed in a previous NIRS study on children [23],
[oxy-Hb] and [deoxy-Hb] data from 16 channels were
averaged into four regions. The four regions were named
as left lateral (channel 14), left medial (channel 58),
right medial (channel 912), and right lateral (channel
1316) (Fig. 2).
Statistical analysis
Behavioral variables (RT, RTV, OE, and CE), age, and the
Raven score were compared between the TDC and the
ADHD groups by means of an unpaired t-test. For
statistical analysis of the NIRS data, the mean [oxy-Hb]
and [deoxy-Hb] changes detected in the four regions (left
lateral, left medial, right medial, and right lateral) during
the two task conditions (Go-conditions and NoGo-condi-
tions) were included. These NIRS measures were analyzed
using a mixed analysis of variance (ANOVA) design
(Diagnosis Region Task Condition), with repeated
measures over the latter two factors. Post-hoc analysis
56 NeuroReport 2012, Vol 23 No 2
Copyright Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
was conducted using an unpaired t-test (between-group
comparison: Diagnosis) and a paired t-test (within-group
comparison: Region and Task Condition), when main
effects or significant interactions were found. Bonferroni
correction was used for multiple post-hoc tests.
Finally, Pearsons correlation coefficients were calculated
for the relationship between the mean [oxy-Hb] (or
[deoxy-Hb]) changes and all demographic and behavioral
parameters in the ADHD and TDC groups.
Results
Behavioral and demographic data
There were no significant differences in age (t = 0.3,
P=0.80) or the total Raven Colored Progressive Matrices
score (ADHD vs. TDC; 28.6 vs. 29.6, t =0.56, P=0.58)
between the ADHD and the TDC groups. Regarding the
performance data, the ADHD group showed a signifi-
cantly larger RTV (98.4 vs. 72.7 ms, t =2.5, P<0.05) and
a higher CE (16.1% vs. 2.8%, t =3.9, P<0.001) during
the NoGo-condition and a larger RTV (115.5 vs. 64.4 ms,
t =2.4, P<0.05) during the Go-condition compared with
the TDC group.
NIRS data
On mixed-ANOVA analysis of the [oxy-Hb] changes, a
significant interaction (Diagnosis Task condition) was
observed [F(1,38) =7.0, P<0.05]. Within-group compari-
son revealed that [oxy-Hb] changes were significantly
Fig. 2
RL RM LM LL
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
Fpz
Near-infrared spectroscopy probe placement onto a participants
forehead. The very middle of the probe was placed at the Fpz position.
Small squares represent emitters, whereas white circles represent
detectors. Each number represents a channel. The 16 channels were
averaged into four regions; left lateral (LL) in orange, left medial (LM) in
yellow, right medial (RM) in green, and right lateral (RL) in blue.
Fig. 1
Go-probability=100%
NoGo-condition
(a)
(b)
Go-probability=50%
Go-condition
At rest
(15s)
At rest
(30s)
Task block
(120s)
Two task conditions in the current study. Moles with sunglasses (Go-stimuli) appeared with a 50% probability in (a) the NoGo-condition and a 100%
probability in (b) the Go-condition.
Reduced hemodynamic response in ADHD chil dren Inoue et al. 57
Copyright Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
larger during the NoGo-condition versus the Go-condition
in the TDC group (0.83 vs. 0.37 mmol; t =2.2, P<0.05),
whereas such an effect was not observed in the ADHD
group (0.20 vs. 0.32 mmol; t = 1.5, P=0.15). Between-
group comparison revealed that [oxy-Hb] changes during
the NoGo-condition were significantly lower in the
ADHD group than in the TDC group (0.20 vs. 0.83 mmol;
t = 3.1, P<0.01), whereas such an effect was not ob-
served during the Go-condition (ADHD vs. control; 0.32
vs. 0.37 mmol; t =0.27, P=0.78) (Figs 3 and 4).
On mixed-ANOVA analysis of the [deoxy-Hb], main ef-
fects and significant interactions were not observed, except
for the main effect of the Task condition [F(1,38) =14.5,
P<0.001], which revealed that the [deoxy-Hb] change
was significantly smaller during the NoGo-condition versus
in the Go-condition across the diagnostic groups ( 0.21 vs.
0.14mmol).
As a main effect of Region was not found on NIRS data
analysis, the mean [oxy-Hb] and [deoxy-Hb] changes during
the NoGo-condition/Go-condition were averaged across the
regions and then subjected to correlational analysis. The
mean [oxy-Hb] and [deoxy-Hb] changes during the NoGo-
condition/Go-condition were not significantly correlated
with age (NoGo-[oxy-Hb] r =0.132, P=0.411; NoGo-
[deoxy-Hb] r =0.01, P=0.95; Go-[oxy-Hb] r =0.019,
P=0.906; Go-[deoxy-Hb] r = 0.171, P=0.286), Raven
score (NoGo-[oxy-Hb] r =0.117, P=0.568; NoGo-[deoxy-
Hb] r =0.078, P=0.706; Go-[oxy-Hb] r = 0.035,
P=0.864; Go-[deoxy-Hb] r = 162, P=0.4), RT (NoGo-
[oxy-Hb] r = 0.16, P=0.308; NoGo-[deoxy-Hb] r =
0.135, P=0.401; Go-[oxy-Hb] r = 0.225, P=0.157; Go-
[deoxy-Hb] r = 0.087, P=0.588), RTV (NoGo-[oxy-Hb]
r = 0.291, P=0.065; NoGo-[deoxy-Hb] r =0.131, P=
0.416; Go-[oxy-Hb] r = 0.044, P=0.783; Go-[deoxy-Hb]
r =0.191, P=0.232), OE (NoGo-[oxy-Hb] r = 0.45,
P=0.782; NoGo-[deoxy-Hb] r =0.099, P=0.539), or CE
(NoGo-[oxy-Hb] r = 0,299, P=0.057 ; NoGo-[deoxy-Hb]
r =0.164, P=0.307).
Fig. 3
[oxy-Hb]_Control
2.0
(a)
(b)
NoGo-condition
[deoxy-Hb]_Control
[oxy-Hb]_ADHD
[deoxy-Hb]_ADHD
0.0
LL LM
RM RL
[
H
b
]
c
h
a
n
g
e

(

M
)
2.0
2.0
Go-condition
0.0
[
H
b
]
c
h
a
n
g
e

(

M
)
2.0
LL LM
RM RL
The averaged near-infrared spectroscopy waveforms of [oxy-Hb] and [deoxy-Hb] elicited during (a) NoGo-condition and (b) Go-condition. Two
vertical lines represent the task block (2-min duration). ADHD, attention deficit/hyperactivity disorder; LL, left lateral; LM, left medial; RL, right lateral;
RM, right medial.
Fig. 4
1
0.8
AD/HD
TDC
0.6
0.4
0.2
0
NoGo-condition
M
e
a
n

[
o
x
y
-
H
b
]

c
h
a
n
g
e

(

M
)
Go-condition
The average [oxy-Hb] changes in children with attention-deficit/
hyperactivity disorder (ADHD) and the group of typically developing
children (TDC) across the four regions.
58 NeuroReport 2012, Vol 23 No 2
Copyright Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
Discussion
In the current study, the hemodynamic response of
prefrontal regions during a Go/NoGo task was compared
between TDC and children with ADHD. The mean
change in [oxy-Hb] was clearly reduced in the ADHD
group compared with that in the TDC group. This char-
acteristic change was confined to the NoGo-condition,
for which prepotent inhibition is involved. Our NIRS data
for TDC indicated that activation of the prefrontal area
during an inhibitory task could be detected on NIRS
measurement even in children 614 years of age. As the
current and previous study [17] compared two task
conditions (Go-conditions and NoGo-conditions), in
both, the condition-specific brain activity in healthy
participants (children and adults) caused by inhibitory
demand but not by simple response execution could be
detected. Therefore, the current results overcome the
methodological limitations in the early NIRS study
involving a Go/NoGo task [24], in which the hemody-
namic response without an adequate control condition
equivalent to the Go-condition used in the current study
was measured.
Therefore, the mean [oxy-Hb] and [deoxy-Hb] changes
were not influenced by the regions of NIRS probes,
suggesting that bilateral PFC regions were equally
involved in the response inhibition. Tamm et al. [25]
conducted an fMRI study on children/adolescents,
showing that significant activation during a Go/NoGo
task was observed in the right superior/inferior frontal gyri
and the left middle frontal gyrus, which indicates
activation in more confined areas compared with the
currently described one. This may be due to the higher
mean age of the participants in the fMRI study (14 years
5 months) than in the current study (9 years 9 months),
which implies that younger participants show more
extensive brain activity than older participants because
of inefficient recruitment of brain regions. Moreover, the
[oxy-Hb] changes observed in the current study may
reflect activation in broader brain areas compared with
that in the former fMRI study, which was based on the
BOLD signal [25].
Thus, the reduced [oxy-Hb] response across PFC regions
in ADHD children observed in the current study is
consistent with the former fMRI studies involving an
inhibitory task [10,11], which showed a significant
reduction in brain activity in the bilateral PFC of children
with ADHD. These NIRS/fMRI findings during the
Go/NoGo task presumably reflect the deficit of inhibi-
tion of a prepotent response in children with ADHD [2].
Considering the characteristic findings in the previous
NIRS studies on ADHD children involving the task of
interference control [14,16], the clinical usefulness of
NIRS measurement for investigation of the inhibitory
function in ADHD patients is indicated.
Conclusion
The current study showed that NIRS measurement is a
powerful and handy tool for evaluation of the inhibitory
function in children with ADHD. Future NIRS studies on
ADHD children should include investigation of the
effects of pharmacotherapy on the inhibitory function
and clinical outcome.
Acknowledgements
This study was supported in part by a grant from the
Hayao Nakayama Foundation for Science & Technology
and Culture and a Grant for Research on Psychiatric and
Neurological Diseases and Mental Health (H19-Kokoro-
Ippan-006), and a Research Grant (19A-8) for Nervous
and Mental Disorders from the Ministry of Health,
Labour, and Welfare.
Conflicts of interest
There are no conflicts of interest.
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