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Article

Electroencephalographic Alpha Reactivity


on Opening the Eyes in Children With
Attention-Deficit Hyperactivity Disorder

Clinical EEG and Neuroscience


44(1) 53-57
EEG and Clinical Neuroscience
Society (ECNS) 2013
Reprints and permission:
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DOI: 10.1177/1550059412445659
eeg.sagepub.com

Lineu C. Fonseca1, Gloria M. A. S. Tedrus1,


Marilia C. Bianchini2, and Talita F. Silva3

Abstract
The quantification of differences in alpha electroencephalograph (EEG) activity between the eyes-closed and eyes-open resting
conditions could be used as a measure of resting state arousal. The objective of this study was to evaluate the contribution of EEG
alpha reactivity on opening the eyes, to the neurophysiology of children with attention-deficit hyperactivity disorder (ADHD).
Thirty-eight children with ADHD were assessed using quantitative EEG (qEEG) analysis of absolute band power at rest, with eyes
open and closed. Alpha reactivity index was calculated on opening the eyes, defined from the relationship between the absolute
powers in the respective bands in the periods with the eyes open and closed. EEG data of 38 sex- and age-matched controls, with no
neurological or psychiatric problems, were collected for comparison. There was a significant reduction in absolute alpha power at all
electrodes for both ADHD and control groups with eyes open, indicating an increase in the arousal level. However, the alpha
reactivity index was greater, corresponding to less reactivity, in the frontal regions of the children with ADHD (P < .01). Such a
finding suggests alterations in arousal mechanisms in ADHD. This research suggests that alpha reactivity on opening the eyes, allied
with other variables from the qEEG, may improve diagnostic accuracy in ADHD.
Keywords
attention-deficit hyperactivity disorder, EEG, children, arousal
Received June 6, 2011; accepted September 8, 2011.

Introduction
A diagnosis of ADHD is based on the Diagnostic and
Statistical Manual of Mental Disorders (Fourth Edition
Text Revision {DSM-IV-TR}) criteria,1 of which the basic
characteristic is the persistence of a standard of lack of
attention and/or hyperactivity impulsivity, more frequent,
and serious than that typically observed in individuals at
an equivalent developmental level. Currently, there is no
laboratory examination that can serve as a marker for
ADHD. Thus, the assessment procedure should consist of a
review of the medical, developmental and family histories,
as well as an examination of intellectual function and
academic performance.
There is wide agreement that ADHD occurs as the result of a
dysfunction in the central nervous system, but the mechanisms
are still not well known. Zentall and Zentall2 raised the hypothesis that ADHD symptoms, such as restlessness and hyperactivity, could be associated with chronic underarousal.
However, a number of researchers have suggested different
mechanisms by which there would be a compromise of arousal,
alertness and activation in ADHD.3-5

Since it is functional, simple and accessible, EEG has


been widely used to study normal cognitive mechanisms, as
well as the nature of brain dysfunction in ADHD. The most
frequent alterations in ADHD are greater interhemispheric
coherence in the theta and delta bands, less in the alpha band,6
increased absolute and relative theta and delta,7-11 and lower
relative alpha and beta.8,10,12,13 Absolute theta/beta power ratio
showed high discriminatory power between ADHD and
controls.14,15

1
School of Medicine, Pontifcia Universidade Catolica de Campinas (PUCCampinas), Campinas, Sao Paulo, Brazil
2
Scholarship holder, School of Psychology (PUC-Campinas); FAPESP, The
State of Sao Paulo Research Foundation
3
Scholarship holder, School of Psychology (PUC-Campinas); FAPIC/Reitoria
(PUC-Campinas)

Corresponding Author:
Lineu C. Fonseca, Rua Sebastiao de Souza 205, cj 122, CEP 13.013.173,
Campinas, Sao Paulo, Brazil.
Email: lineu.fonseca@uol.com.br

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54

Clinical EEG and Neuroscience 44(1)

Recent studies have tried to characterize concepts of arousal


and activation in normal individuals from physiology and neural
correlations. By using measurement of electrochemical skin
conductance (SCL), the classical correlation of arousal level, it
was shown that during eyes-closed resting the arousal level was
negatively correlated with the alpha brain electrical activity
(8-12 Hz range), and that opening the eyes was associated
with an increase in SCL and reduction in alpha activity.16,17
Thus, the quantification of alpha activity could be used as a measure of resting-state arousal under eyes-closed and eyes-open
conditions.
In a recent work, Barry et al18 failed to encounter a significant correlation between theta/beta ratio and SCL, contradicting the supposed linkage between this index and arousal in
ADHD. Instead, they found a negative correlation between
SCL and alpha activity, suggesting its importance as a marker
of arousal.
The objective of the present work was to evaluate the relationship between alpha activity, with eyes open and closed, in
ADHD. Although a state of hypoarousal is considered to be an
important mechanism in ADHD, no research of alpha reactivity
on opening the eyes in children could be found.

interconnected ear lobe electrodes served as the reference. The


data were recorded while awake during about 5 periods, alternating 2 minutes with the eyes closed and 2 minutes with the
eyes open. The individual was stimulated to remain awake
when symptoms of somnolence appeared. Stretches of somnolence or sleep were excluded from the quantitative analysis.
For the qEEG analyses, 18 to 26 of artifact-free epochs, each
lasting 2.56 seconds, were selected under 2 conditions; awake
but resting (eyes closed) and awake (eyes open). After applying
Fast Fourier Transform, the absolute powers (mV2/Hz) were
studied in the following frequency bands: delta (up to
3.9 Hz), theta (4.9-7.8 Hz), alpha (8.2-12.5 Hz), and beta
(12.9-36.3 Hz). To obtain a normal distribution, the values for
absolute power were substituted by their logarithms.
The absolute power averages were calculated for the centrotemporal regions (C4, C3, T4, T3, T6, and T5), occipital
regions (O1 and O2), and frontal regions (F3 and F4).
Alpha reactivity index, calculated on opening the eyes, was
defined as the ratio between the absolute alpha power with eyes
open and eyes closed. The greater the reduction in alpha activity
with eyes open (alpha reactivity), the smaller the value of this
index.
The formula for the alpha index is as follows:

Materials and Methods

Alpha reactivity index

Thirty-eight school children, aged 8 to 11, diagnosed with ADHD


according to DSM-IV-TR, and referred by the outpatients
departments of the Infancy & Adolescence Psychiatry Department and the Pediatric & Neurological Pediatric Department
(HMCP PUC-Campinas), were studied. Thirty-eight children,
with no neurological or psychiatric problems, comprised the sexand age-matched control group, which was also matched for
maternal scholastic level. All the children were free of medication at the time of testing, and those taking methylphenidate were taken off this medication for at least 12 hours
prior to the assessment, longer than its serum and behavioral
half-lives.19 The following procedures were carried out: medical history, psychiatric evaluation, neurological examination;
Conner Parent and Teacher Rating Scales; Child Behavior
Checklist 4-18, Wechsler Intelligence Scale for Children; and
digital and quantitative EEG (qEEG).

EEG
EEG was recorded with a resolution of 12 bits, 0.5 and 35 Hz
filters, and 200 samples/second, using the BrainNet BNT 36
equipment (EMSA Equipamentos Medicos), with impedance
maintained below 10 kO. The examination was carried out with
the patients lying on their backs in a silent environment with
low-intensity lighting. The electrodes were placed according
to the International 10-20 System, with the use of an additional
2 electrodes placed 1 cm below (left side) and above (right
side) the external angle of the eyelid, with the objective of evaluating eye movements. The data referring to the electrodes
Fp1, Fp2, F8, and F7 were not computed due to frequent contamination by artifacts related to eye movements. The

Absolute alpha power; eyes open


Absolute alpha power; eyes closed

The Statistical Packages for Social Sciences (SPSS 10.0.1) statistical program was used, applying both parametric and nonparametric tests, according to the data distribution. In order
to minimize the possibility of errors due to multiple comparisons, means of measurements involving various electrodes
positions were used instead of individual electrode position
measurements, and the level of significance was P  .01.

Ethical aspects
The Ethics Commission for Research with Human Beings of
PUC-Campinas, Brazil, approved the project, and the participants signed an informed consent.

Results
Table 1 shows the data for age, sex, maternal scholastic level,
and school grade of the 38 children with ADHD and of the control group (CG). Table 2 shows the mean obtained for the logarithms of the absolute alpha powers, with eyes closed and open,
by location of electrodes and by groups. There was no statistically significant difference between the ADHD and CG for
absolute alpha power, whether eyes were closed or open (T test,
P > .05, values for P not presented in table).
A decrease in the absolute alpha power occurred with the
eyes open for all the regions studied, with a significance level
below .001. Table 3 shows the alpha reactivity indices obtained
at the various locations of the electrodes for ADHD and CG. The
alpha indices were greater (less reactivity) for ADHD, but statistically significant only in the frontal regions (T test, P < .01).

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Table 1. Data for Age, Gender, School Grade, and Maternal Scholastic Level for the ADHD and Control Groups.a

Participants
Age (years)
Gender (male/female)
School grade (years)
Maternal scholastic level (years)

ADHD

CG

P Value

38
8.97 (1.15)
(28/10)
3.05 (1.11)
2.74 (1.62)

38
8.97 (1.15)
(28/10)
2.87 (1.07)
2.63 (1.62)

1.00 b
1.0 c
.510 b
.772 b

ADHD: attention-deficit/hyperactivity disorder; CG, control group.


a
Data are expressed as means, and the standard deviations (SDs) are within parentheses.
b
t test.
c
Chi-square test.

Table 2. EEG Absolute Alpha Power With the Eyes Both Closed and Open for the ADHD and Control Groups.
ADHD
Average
(Log-Transformed)
Frontal
Occipital
Centrotemporal

Comparing ADHD  CG, P Value

CG

Eyes Closed

Eyes Open

Eyes Closed

Eyes Open

Eyes Closed

Eyes Opened

52.6 (6.9)
69.5 (9.8)
53.4 (7.5)

50.1 (5.9)
58.4 (8.9)
48.7 (6.9)

.000 a
.000 a
.000 a

52.2 (6.1)
71.7 (9.1)
53.1 (6.9)

47.9 (5.4)
58.0 (9.0)
47.8 (6.4)

.000 a
.000 a
.000 a

.783
.328
.854

.101
.841
.548

ADHD, attention-deficit hyperactivity disorder; CG, control group.


a
t test, P < .001.

Table 3. Alpha Reactivity Indices on the qEEG for the ADHD and
Control Groups.
Alpha Indices
Electrodes
Frontal
Occipital
Centrotemporal

ADHD

CG

P Value

0.96 (0.05)
0.84 (0.08)
0.91 (0.05)

0.92 (0.04)
0.81 (0.07)
0.90 (0.05)

0.002 a
0.060
0.273

ADHD, attention-deficit/hyperactivity disorder; CG, control group; qEEG,


quantitative electroencephalograph.
a
t test, P < .01.

Discussion
No significant differences were found between ADHD and CG
in absolute alpha power, in agreement with the literature, since
increases in absolute power occur predominantly in delta and
theta bands7-11 and are expressed in a relevant way in the
theta/beta index.14,15
Opening of the eyes, from the eyes-closed resting state, is
classical practice in conventional EEG.20 It results in desynchronization of electrical brain activity, and the alpha rhythm
is reduced, giving rise to rapid rhythms. Alpha reactivity to
visual stimuli is well known; however, it is not exclusively
related to visual information, since it has connections with
memory and cognition in general.21 This is traditionally evaluated by visual analysis of the EEG, although with the advances
in computer technology, it may be the object of multiple quantitative analyses of qEEG.
Alpha reactivity can be quantified by indices such as the
alpha power index, obtained by dividing the values obtained

eyes open by the corresponding values obtained eyes closed.


In qEEG studies, a reduction in alpha power reactivity has been
found in diverse clinical conditions such as age-related cognitive decline22 and Alzheimer disease23,24 and has been considered as an indicator of brain disorder.24
In the present study, a significant reduction in absolute alpha
power was observed with eyes open compared with eyes closed
for both ADHD and CG, and for all the derivations, providing
evidence of clear reactivity of the alpha rhythm, as expected in
this age group.25,26 Such alpha desynchronization to visual
input could occur due to widespread communication of cortical
and thalamocortical interactions, in order to aid information
processing.21,27 On comparing the reactivity indexes between
ADHD and CG in the present research, values were found to
be higher (less alpha reactivity) in the ADHD group at the various electrode positions, although the difference was only statistically significant in frontal regions.
Since quantification of alpha activity can be used as a
measure of resting-state arousal under both eyes-closed and
eyes-open conditions,16-18 the findings of the present research
suggest alterations in the state of alertness of the children
with ADHD. This finding in children is original in the use
of EEG, since the authors have no knowledge of a similar
study. Mechanisms connected to cortical hypoarousal were
reported by Lubar28 as being due to the increase in theta
activity, decrease in beta, and eventually in alpha activities.
This suggestion is supported by research with skin conductance tests,29 regional cerebral blood flow and positron emission tomography.30
van Dongen-Boomsma et al31 found a greater reduction in
alpha power from eyes closed to eyes open in adults with
ADHD as compared with controls, which appears inconsistent

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Clinical EEG and Neuroscience 44(1)

with the results of the present study. However, there are relevant differences between the findings of EEG at rest in children
with ADHD as compared to those of adults with ADHD, since in
the latter the data are scarce, disparate, and less consistent, 31-33
suggesting neurophysiologic modifications during the development of the individuals into adult life. Earlier research on ADHD
was directed essentially at evaluating brain activation, that is,
making recordings during different tasks. The researchers did
not search for a characterization of the state of arousal.15,32-37
The fact that in the present study the difference in alpha reactivity was only observed in a significant way in the frontal regions
is supported by various other evidences of dysfunction in the
frontal cortex. In the study of ADHD in children, alterations in
coherence6,38,39 and an increase in theta activity40 in the frontal
regions were found. Frontal alterations have been found in studies with positron emission tomography39 and single photon
emission computed tomography.41
In summary, elements suggesting alterations in the arousal
mechanisms that probably involve the frontal regions were
found in the present research. On the other hand, this research
opens opportunities for the use of alpha reactivity on opening
the eyes, obtained using different evaluation methods,42 and
allied to other variables of the qEEG, with the objective of providing an increment in diagnostic accuracy of ADHD.
Declaration of Conflicting Interests
The authors declared no potential conflicts of interest with respect to
the research, authorship, and/or publication of this article.

Funding
The authors received no financial support for the research, authorship,
and/or publication of this article.

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