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Brain & Development 34 (2012) 806–811

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Original article

EEG characteristics and visual cognitive function of children


with attention deficit hyperactivity disorder (ADHD)
Tongkun Shi a, Xia Li a,b, Jia Song a, Na Zhao a, Caihong Sun a, Wei Xia a,
Lijie Wu a,⇑, Akemi Tomoda c
a
Department of Child and Adolescent Health, Public Health College, Harbin Medical University, Harbin, PR China
b
Department of Sanitarian of Zaozhuang Maternity and Child Care Hospital, 25# East of Wenhua Road, Shizhong District, Zaozhuang,
Shandong 277100, PR China
c
Child Development Research Center, Graduate School of Medicine, University of Fukui, Fukui, Japan

Received 29 August 2011; received in revised form 16 February 2012; accepted 28 February 2012

Abstract

Using visual and auditory continuous performance tests (CPT) and EEG, cognitive function and EEG power were investigated in
patients with attention deficit hyperactivity disorder (ADHD). CPT and EEG were conducted for 44 ADHD children and 44
healthy controls of comparable age and sex. The EEG power tests include relative power of theta, alpha, and beta, and theta/beta
and theta/alpha ratios. ADHD patients showed significantly higher theta relative power, lower beta relative power, and higher
theta/beta ratio (p < 0.05). ADHD patients showed a significantly lower score of auditory CPT (p < 0.05). The EEG power char-
acteristics were correlated significantly with the visual attention function in ADHD children (p < 0.01). Higher-order level cognitive
dysfunction affects ADHD pathogenesis. Cortical hypoarousal effects on several mechanisms including the fronto-striatal circuitry
may be implicated in the inhibition of prepotent and premature responses.
Ó 2012 The Japanese Society of Child Neurology. Published by Elsevier B.V. All rights reserved.

Keywords: Attention deficit hyperactivity disorder (ADHD); Integrated visual and auditory continuous performance test (IVA-CPT); Children;
EEG; Visual cognitive function

1. Introduction of ADHD. Reportedly, 45–90% of ADHD children


show electroencephalographic abnormalities [3].
Attention deficit hyperactivity disorder (ADHD) is Quantitative electroencephalographic recording is a
the most common psychiatric disorder among children noninvasive measurement of the baseline or the underly-
[1]. As defined in DSM-IV, ADHD symptoms include ing brain state before information processing [4]. Elec-
developmentally inappropriate levels of attention, troencephalographic measurements have been regarded
hyperactivity, and impulsive behavior. If untreated, as highly sensitive in distinguishing ADHD patients
ADHD, which has been estimated conservatively as from healthy subjects in many studies [5,6]. An early
affecting 3–5% of school-aged children [2], can influence study that identified EEG abnormalities in children with
children’s studies, family settings, and social life. The ADHD was Jasper’s study [7] (1938) of children with
pathogenesis of this disorder remains unknown, with a behavior problems: the study examined 71 children aged
lack of objective, comprehensive indicator for diagnose 2–16 years, most with IQ above 70. Results show that
over half of the subjects had EEG abnormalities, pre-
⇑ Corresponding author. Tel./fax: +86 451 87502867.
dominantly increased slow wave (2–6 Hz) activity in
E-mail address: wulijie_123@yahoo.com.cn (L. Wu).
one or more regions, and often in frontal regions. With

0387-7604/$ - see front matter Ó 2012 The Japanese Society of Child Neurology. Published by Elsevier B.V. All rights reserved.
http://dx.doi.org/10.1016/j.braindev.2012.02.013
T. Shi et al. / Brain & Development 34 (2012) 806–811 807

the application of computer aided tools, many new or less (Wechsler Intelligence Scale for Children, Third
methods in EEG analysis were applied, including mea- Edition; WISC-III), and those with comorbid epilepsy,
surements of amplitude, relative power, absolute power, progressive neurological and psychiatric disorders were
and analysis of the dominant frequency and average fre- excluded. Control group subjects were also excluded if
quency, each band power percentage, and power ratios. they reported a family history of ADHD, psychiatric
Clarke et al. [8] reported that 20 ADHD children’s rela- disorder, or genetic brain disorder.
tive power and absolute power of alpha and beta waves Both ADHD patients and healthy children were med-
were lower than those of normal controls. The relative ication free (central nervous system stimulant) for at
power and absolute power of theta waves were higher least 48 h before testing. Moreover, for at least 2 h prior
than in the control group. Monastra et al. [9] found that to testing, participants were asked to refrain from caf-
the value of theta/beta ratio was useful to distinguish feine intake and smoking. All subjects or their guardians
ADHD patients from normal ones, and found that the were provided a written informed consent form for par-
respective degrees of sensitivity and specificity reached ticipation in the research at the Child Development and
86% and 98%. Clarke’s et al. [8] research also revealed Behavior Research Center at Harbin Medical Univer-
that the values of theta/alpha ratio and theta/beta ratio sity, in accordance with National Health and Medical
were diverse in normal children and in ADHD children. Research Council guidelines.
In addition, this ratio was useful to distinguish inatten-
tion-type patients and combined-type patients. 2.2. Procedures and tasks
We used a biofeedback system to detect the levels of
relative power of EEG and the values of the relative 2.2.1. Resting electroencephalographic condition
power ratio, along with neuropsychological testing anal- The EEG was recorded in an eyes-closed resting condi-
yses to assess correlation between the visual cognitive tion, with subjects sitting in reclining chair. The test used a
function and the EEG characteristics. Thereby, we were biofeedback system (VBFB 3000; Thought Technology
able to explore the relations between resting-state EEG Ltd., Canada). Electrode placement followed the Interna-
and ADHD behavior symptoms, and to validate the tional 10–20 system, using three electrodes. The Fourier
EEG power in predicting the cognitive activities of transformation was carried out for 600 s consisting of
ADHD children. one EEG record in each patient. According to the interna-
tional 10–20 Electrode Placement System, Cz [10,11] is
2. Methods the standard placement sites, which is the most sensitive
EEG area between ADHD and normal children. Active
2.1. Subjects (record) electrode was placed at site Cz in order to collect
EEG activity signals easily. Reference (A1) and Ground
Subjects included 44 children who were diagnosed (A2) electrode were placed on opposite ear lobes. Sub-
with ADHD (mean age 8.45; SD 2.11; range 6–14 years; jects, who were told that the task would last for 10 min,
36 boys and 8 girls) and 44 age-and-sex-matched (pair- were asked to rest quietly with their eyes closed during
wise) healthy children as a control group (mean age the recording. The record index includes the level of the
8.32; SD 1.99; range 6–14 years). Forty-four ADHD relative power of theta (4–7 Hz) wave, alpha (8–12 Hz)
children included 34 inattentive type (IT) children, seven wave, the beta (13–32 Hz) wave, and the values of the
combined type (CT) children and three hyperactive- theta/beta ratio and theta/alpha ratio.
impulsive type (HI) children. All ADHD children were
recruited from Child Development and Behavior 2.2.2. Cognitive tasks
Research Center of Harbin Medical University; healthy This test mainly adopted the software of Integrated
children were recruited from primary school as volun- Visual and Auditory continuous performance test (IVA-
teers. Both of two groups were residents of Harbin, CPT; Brain Train, USA). Furthermore, information
the capital city of Heilongjiang province. from the tests was collected by computer. The IVA-CPT
All ADHD subjects were selected by two pediatri- principle is mainly to represent repeated auditory and
cians. The ADHD diagnosis was further confirmed with visual stimuli, and to record the response of subjects
a semi-structured interview based on the Diagnostic and (including reaction time, omissions, endurance, repetition
Statistical Manual of Mental Disorders Fourth Edition, frequency, etc.) to assess the attention activity. The IVA-
Text Revision (DSM-IV-TR) diagnostic criteria for CPT results include six full-scale quotients and 12 inde-
ADHD. pendent quotients. The full scale response control quo-
Exclusion criteria for both the ADHD group and the tient (FRCQ) is based on equal weights of the auditory
control group include a personal history of physical response control quotient (ARCQ) and the visual
brain injury, neurological disorder, genetic disorder, or response control quotient (VRCQ), ARCQ and VRCQ
other severe medical condition or a personal history of scores are based on equal weights (1/3) of their respective
substance abuse or dependency. Patients with IQ of 80 prudence, consistency and stamina scales.
808 T. Shi et al. / Brain & Development 34 (2012) 806–811

The full scale attention quotient (FSAQ) is based on Table 1


equal weights of the auditory attention quotient (AAQ) Power of EEG between ADHD children and the control group (x  s).
and the visual attention quotient (VAQ). The AAQ and Items AD/HD Control t p
VAQ in turn are based on equal weights (1/3) of their Theta % 21.75 ± 2.94 20.49 ± 1.85 2.402 .021*
respective vigilance, focus and speed scales. Alpha % 14.53 ± 3.84 14.01 ± 4.01 0.481 .634
During the test, subjects were asked to press the Beta % 5.44 ± 1.24 6.41 ± 1.16 4.302 .001**
mouse left key once if they saw or heard the number Theta/beta 4.22 ± 1.23 3.41 ± 0.57 4.194 .001**
“1”, and not to click if they saw or heard the number Theta/alpha 1.62 ± 0.49 1.54 ± 0.34 0.667 .765
“2”. Participants were asked to remember the following
four rules: see “1” press mouse; hear “1” press mouse;
see “2” do not press the mouse left key; hear “2” do
for ADHD subjects and control subjects across scalp
not press the mouse left key. The computer recorded
sites during eyes-closed resting activity. Using paired t-
the statistical analysis feedback of subjects.
tests, significant differences were found between two
groups in theta relative power, beta relative power,
2.3. Statistical analysis
and the theta/beta ratio (t = 2.402, p < 0.05;
t = 4.302, p < 0.05; t = 4.194, p < 0.05). In the ADHD
2.3.1. Statistical method
group, the level of relative power of theta and the value
A paired t-test was used to compare the results of the
of theta/beta ratio were significantly higher than in the
ADHD group to those of the control group. A correla-
control group, and the level of relative power of beta
tion analysis was used to measure the relative power
was significantly lower than in the control group.
between the brain electrical level and cognitive task
grades in two groups. Furthermore, as a secondary anal-
3.2. Cognitive task analyses
ysis, a Pearson correlation matrix was computed to
ascertain whether the power of EEG for each band
Tables 2 and 3 present differences between the
was related to the cognitive function in the IVA-CPT,
ADHD group and the control group in the result of
with the significance cutoff set at p < 0.05. All statistical
IVA-CPT for the response control quotient and atten-
analyses were processed using software (SPSS 13.0;
tion control quotient.
SPSS Inc., USA).
For the response control quotient, the ADHD group
scores were significantly lower in seven quotients of
2.3.2. Quality control
response control: the full scale response control quo-
All testers were strictly trained to be familiar with the
tient, auditory response control quotient, visual
use of test instruments, and to adopt a unified standard.
response control quotient, auditory prudence quotient,
Testers ensured the completion of the whole process for
visual prudence quotient, auditory consistency quotient,
each subject. The test environment was quiet, with no
and visual consistency quotient (p < 0.05).
magnetic interference, thereby ensuring the reliability
Regarding the attention control quotient, the ADHD
of data collection.
group scores were significantly lower in nine quotients of
attention control: the full scale attention quotient, audi-
3. Results
tory attention control quotient, visual attention control
quotient, auditory vigilance quotient, visual vigilance
3.1. Electroencephalographic analyses
quotient, auditory focus quotient, visual focus quotient,
auditory speed quotient, and visual speed quotient
Table 1 presents the relative power in theta, alpha,
(p < 0.05).
and beta, and the theta/beta ratio and theta/alpha ratio
Table 2
Results of IVA-CPT of the response control quotient for ADHD children and the control group (x  s).

Items AD/HD Control t p


FRCQ 80.60 ± 21.55 97.34 ± 18.72 3.274 .002**
ARCQ 83.74 ± 18.95 98.24 ± 17.60 3.436 .001**
VRAQ 81.65 ± 22.28 97.70 ± 17.06 2.996 .005**
Auditory prudence quotient 91.84 ± 20.75 102.92 ± 18.95 2.456 .019*
Visual prudence quotient 87.97 ± 17.92 98.78 ± 15.16 2.932 .006**
Auditory consistency quotient 75.37 ± 15.63 93.92 ± 16.68 5.125 .001**
Visual consistency quotient 80.08 ± 23.22 99.49 ± 18.37 3.849 .001**
Auditory stamina quotient 99.89 ± 22.82 99.50 ± 12.52 .094 .926
Visual stamina quotient 93.51 ± 19.55 98.05 ± 12.24 1.130 .266
Note: FRCQ, full scale response control quotient; ARCQ, auditory response control quotient; VRCQ, visual response control quotient.
T. Shi et al. / Brain & Development 34 (2012) 806–811 809

Table 3
Result of IVA-CPT of the attention quotient for ADHD children and the control group (x  s).

Items AD/HD Control t p


FAQ 68.86 ± 23.89 98.51 ± 17.75 5.747 .001**
AAQ 69.34 ± 24.45 97.05 ± 18.84 5.028 .001**
VAQ 74.95 ± 23.86 100.62 ± 15.48 5.428 .001**
Auditory vigilance quotient 66.34 ± 32.99 94.21 ± 20.58 4.039 .001**
Visual vigilance quotient 78.11 ± 22.21 99.49 ± 13.57 4.660 .001**
Auditory focus quotient 82.92 ± 16.53 98.68 ± 14.01 4.745 .001**
Visual focus quotient 85.62 ± 18.07 99.73 ± 17.16 3.252 .002**
Auditory speed quotient 94.63 ± 14.79 102.00 ± 12.34 2.174 .036*
Visual speed quotient 94.38 ± 17.49 101.73 ± 13.31 2.125 .041*
Note: FAQ, full scale attention quotient; AAQ, auditory attention quotient; VAQ, visual attention quotient.

Table 4
Correlation between IVA-CPT and the relative power of EEG in ADHD children.

Item Theta % Alpha % Beta % Theta/beta Theta/alpha


FRCQ .050 .303 .094 .043 .261
ARCQ .03 .302 .097 .059 .243
VRAQ .061 .233 .189 .093 .189
Auditory prudence quotient .045 .238 .112 .109 .193
Visual prudence quotient .544** .104 .069 .293 .349
Auditory consistency quotient .040 .127 .090 .093 .007
Visual consistency quotient .078 .150 .238 .156 .030
Auditory stamina quotient .044 .191 .080 .033 .186
Visual stamina quotient .177 .212 .148 .042 .184
FAQ .322 .441* .066 .114 .184
AAQ .227 .302 .016 .097 .159
VAQ .267 .294 .016 .145 .034
Auditory vigilance quotient .102 .406* .027 .035 .246
Visual vigilance quotient .718** .042 .096 .411* .213
Auditory focus quotient .522** .142 .230 .062 .107
Visual focus quotient .074 .104 .281 .235 .010
Auditory speed quotient .647** .079 .039 .358* .291
Visual speed quotient .524** .003 .290 .050 .126
*
p < 0.05.
**
p < 0.01.

3.3. Correlation analyses studies, can distinguish the normal group from the case
group. Particularly, EEG recording under eyes-closed
The Pearson correlation matrix between indexes of conditions is an extremely reliable method [12,13]. In
EEG characteristics and scores of cognitive tasks in 1996, Chabot and Serfontein [6] reported that the
ADHD group is shown in Table 4. For ADHD subjects, EEG of the children with ADHD differed from those
a significant negative linear relation was found between of normal children, results showed that the theta abso-
the level of theta relative power and each of the visual lute power and the relative power of electrical was
prudence quotient, visual vigilance quotient, auditory increased, mainly concentrated in the frontal lobe, espe-
focus quotient, auditory speed quotient, and visual cially in prefrontal regions. Furthermore, alpha waves
speed quotient. Statistically significant positive linear and beta waves changed. In 1998, Clarke et al. [14] first
correlation was found between the level of alpha relative applied the DSM-IV diagnosis of ADHD and analyzed
power and each of the full scale attention quotient and the brain electrical power of all subjects, revealing that
the auditory vigilance quotient. In addition, a significant test electrode parts of the theta relative power and abso-
negative linear relation was found between the level of lute power are significantly higher than those of the con-
the theta/beta ratio and the scores of the visual vigilance trol group. The brain electrical power of alpha and beta
and the auditory speed quotient. are decreased significantly. A previous study also sup-
ports the results presented above [15].
4. Discussion This study found that the theta relative electrical
power of ADHD children was statistically significantly
The method of recording the relative power of EEG higher than that of the control group. The beta relative
in detection analysis, which is used widely in ADHD electrical power was lower than that of the control
810 T. Shi et al. / Brain & Development 34 (2012) 806–811

group to a statistically significant degree. These findings The results of correlation analyses revealed theta
revealed that the EEG characteristics of ADHD chil- power improvement and the scores of signal detection
dren are abnormal, which may imply that the average tasks significantly correlated to the error rate, which
excitation of the brain is decreased, and that the inhibi- implied that abnormal theta activities affect ADHD chil-
tion of the cortical nervous system is decreased. Conse- dren’s performance of cognitive tasks, especially the level
quently, the ADHD children can not maintain an of attention. Some earlier studies identified that a signifi-
appropriate degree of attention. They may not be able cant increase of theta is consistent with decreased white
to specifically examine many things, engendering behav- matter, glucose metabolism, and total brain capacity
ior such as inattention in class and hyperactivity. The [19–22]. Increased theta wave activity of ADHD children
dysfunction of specific brain areas associated with these can engender changes in attention, inability to concen-
abnormalities might explain characteristics of clinical trate, and other defects of behavior in class. Normal
symptoms observed in ADHD patients. experiments also revealed a correlation between increased
In recent years, with the development of the quantita- theta activity and sleep [23]. The theta activity level,
tive electroencephalogram technology for ADHD study, reflecting a person’s cognitive level, also decreased [24].
it has been recognized that the ratio of theta/beta can Additionally, correlation between alpha activity and
forecast the ADHD group and the control group well. attention defects has been shown in go/no go out of task
Monastra et al. [9] research showed that theta/beta [25]. The alpha activity level reflects a certain arousal
ratios can differ between ADHD patients and others, state. The results of the present study showed that the
with specificity and sensitivity reaching 86% and 98%, level of alpha activities and full scale attention quotient
respectively. Many scholars have analyzed multiple share a significant positive correlation, implying that the
quantitative EEGs and have reported an increase in alpha level affects brain resource allocation.
the value of theta/beta ratio among ADHD children The results of correlation analyses conducted for brain
as a common property, with further conclusions show- electrical power and cognitive function of ADHD chil-
ing that when the value of theta/beta power is 3.08, spec- dren show that improvement of the theta/beta ratio is sig-
ificity and sensitivity both reached 94% [16]. Our results nificantly and negatively related to performance of visual
demonstrate that the mean of theta/beta ratio in ADHD memory and the visual vigilance quotient. Many
children (age: 6–14) is 4.22 (SD = 1.26), which was sig- researchers have reported a significant and positive corre-
nificantly higher than that of the control group. lation between the level of EEG power and error rate in
Cognitive testing tasks, which include the prudence signal stop task [26]. Martine [27] reported that the
quotient, consistency quotient, and stamina quotient, theta/alpha ratio and theta/beta ratio are negatively cor-
reflect the subjects’ auditory and visual response control related to response speed in a signal-to-stop task. The
ability, especially the prudence quotient. It can measure result of the survey also showed that the level of theta/
the omission of ADHD children in auditory and visual. beta ratio has a significant negative correlation with audi-
The vigilance quotient, focus quotient, and speed quotient tory speed. This result is inconsistent with that reported
reflect auditory and visual attention abilities of subjects, above. The increase of the theta/beta ratio might have
especially the vigilance quotient. It can measure the error certain relations with hyperactivity and impulsive behav-
of ADHD children in auditory and visual tasks. The sub- iors [28]. A unified account of our findings is provided by
ject is inferred to have cognitive function disorder if the a biophysical model presented by Rowe et al. [29].
score is less than 85. These results demonstrate that the This preliminary study includes some limitations: the
“omission” of the ADHD group was significantly higher samples are small, and we did not carry out stratified
than that of the control group, and that the number of analysis including the age and sub-type of ADHD chil-
“errors” in the ADHD group was significantly greater dren. Moreover, we did not analyze the electrical activ-
than that for the control group, thereby revealing that ity characteristics of various brains areas because of the
ADHD children might have cognitive function disorder. limited number of brain electrodes. We suggest that
The results of Pearson correlation analysis showed future studies can use an electrode cap, comparing dif-
that the visual prudence quotient and visual vigilance ferent changes of EEG among various brain areas.
quotient each shared a significantly negative linear cor-
relation with the level of theta relative power when the
level of theta relative power raised the levels of omission Acknowledgments
and numbers of errors. This result is consistent with
results of other studies. Swartwood et al. [17] reported The work was supported by the Child Development
a significant linear correlation between the left forehead Behavioral Research Center, Harbin Medical
theta band change and the results of continuous opera- University.
tion test. Daniel [18] found the power of theta and Funding support from NSFC (30571576) is gratefully
response delayed error were significantly higher than acknowledged, in addition to the support of Yi Fu Pri-
in the control group. mary School, Harbin, for data collection.
T. Shi et al. / Brain & Development 34 (2012) 806–811 811

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