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EEG Differences in ADHD-Combined Type

During Baseline and Cognitive Tasks


Jeffery N. Swartwood, PhD*, Michie O. Swartwood, PhD*, Joel F. Lubar, PhD, and
DeAnna L. Timmermann, PhD

This study examines the relation between neurologic, Introduction


behavioral, and performance indicators of attention-
deficit hyperactivity disorder. Twenty-three males age Among the psychiatric diagnoses of childhood, atten-
nine to 11 years with attention-deficit hyperactivity tion-deficit hyperactivity disorder (ADHD) is one of the
disorder, including symptoms of hyperactivity, and 23 most debated. Establishing a distinct syndrome has been
matched controls served as participants. Differences difficult because of such issues as a lack of differentiation
between groups were investigated using referential from other behavioral and learning disorders, low levels of
19-channel quantitative electroencephalogram, behav- agreement across different measures, and a lack of a single
ioral rating scale data, and continuous performance etiology or a consistent response to treatment [1,2]. Part of
the problem may be that the current descriptors of the
test data. Results from the behavioral data were con-
disorder are too broad, relying heavily on reports of
sistent with previous research. Behavioral ratings for
behavioral symptoms by parents or teachers. The devel-
participants with attention-deficit hyperactivity disor-
opment of more objective measures would enhance the
der were significantly more negative than controls.
validity and reliability of an ADHD diagnosis. Although
Control participants performed significantly better on
ADHD is currently a behaviorally driven diagnosis, re-
the continuous performance test, with fewer errors,
search is beginning to provide evidence for the use of
faster reaction times, and less variability in reaction
neurometric tools to facilitate the diagnosis.
time. Electroencephalogram results indicated differ- One such neurometric that has been actively investi-
ences between participants with attention-deficit hy- gated is quantitative electroencephalogram (EEG). Con-
peractivity disorder and control participants primarily sensus, however, regarding EEG differences in ADHD
in the alpha bandpass, with evidence of increased alpha across different studies has not been reached. Several
in posterior regions during baseline for the group with studies have demonstrated that individuals with ADHD
attention-deficit hyperactivity disorder. Additionally, exhibit increases in slow-wave activity, particularly in the
participants with attention-deficit hyperactivity disor- frontal regions of the brain, which is sometimes accom-
der manifested decreased alpha in left frontal regions panied by a decrease in fast wave activity in the posterior
when reading. The results are discussed in terms of region [3,4]. Other studies have failed to localize the
possible differences in electroencephalographic data as excess in slow-wave activity to the frontal regions [5,6]
a function of degree of hyperactivity, as well as the but have found a diffuse increase in slow-wave activity
impact of task specificity on the electroencephalogram. from recording sites across the entire brain. In addition to
2003 by Elsevier Inc. All rights reserved. these findings, Clarke et al. [6,7] found an increase in
Swartwood JN, Swartwood MO, Lubar JF, Timmermann fast-wave activity in the frontal region of the brain for a
subset of the participants with ADHD. Clarke [5] noted
DL. EEG differences in ADHD-combined type during
that a greater proportion of children with ADHD-com-
baseline and cognitive tasks. Pediatr Neurol 2003;28:
bined type had this increase in fast-wave activity com-
199-204.
pared with participants with ADHD-inattentive type.
It is possible that some of the variability in findings
across studies may be due to differences in the participant

From the *Department of Psychology, State University of New York Communications should be addressed to:
at Cortland, Cortland, New York and theDepartment of Psychology, Dr. Swartwood; SUNY Cortland, Psychology Department,
University of Tennessee at Knoxville, Knoxville, Tennessee. Cortland, NY 13045.
Received April 2, 2002; accepted August 26, 2002.

2003 by Elsevier Inc. All rights reserved. Swartwood et al: EEG Differences in ADHD 199
doi:10.1016/S0887-8994(02)00514-3 0887-8994/03/$see front matter
population that are revealed by EEG data but not neces- ADDES rating scale norms was not included in the study. Additionally,
sarily discriminated by using standard diagnostic criteria. subjects in the control group were not diagnosed with other learning or
behavior disorders.
Other sources of interstudy variability may be due to
procedural differences during the process of EEG collec-
tion. Some researchers record EEG data from the partici-
pants during an eyes closed baseline condition [5,6], Materials
whereas others have examined participants during en-
Participants were tested using several neurological and psychological
gaged tasks (reading, listening, and drawing) in addition to test materials. The McCarney Attention Deficit Disorder Evaluation
baseline conditions [4,8]. General conclusions regarding Scale (ADDES) [9] was used to collect behavior ratings from parents
research in this area depends on these participant and regarding their child. The Wide Range Achievement Test-Revised
procedural differences. For example, although the Mann et (WRAT-R) [10] was used to screen academic performance and to
determine appropriate materials for the EEG conditions. The Test of
al. [4] study investigated EEG changes during both base-
Variables of Attention (TOVA) [11], a normed continuous performance
line and cognitive tasks in children with ADHD-inatten- test, was used as a measure to assess performance differences between
tive type, whether or not the same results would be groups. During the TOVA, visual stimuli were briefly presented every 2
observed in those children diagnosed as ADHD-combined seconds for 22.5 minutes. Participants followed standardized instructions
type is not known. to watch the screen and click a button whenever a colored square
appeared at the top portion of an outer square (target stimulus). If the
The present study compares the EEGs of children with
square appeared at the bottom portion of the outer square (nontarget
ADHD-combined type on a variety of baseline and cog- stimulus), participants were told to refrain from clicking. Scores derived
nitive tasks with the EEGs of typically developing chil- from the TOVA provided measures of errors of omission, errors of
dren. Given the results of research with nonhyperactive commission, mean correct response time, and response variability.
children with ADHD during cognitive tasks [4,7], it is Referential electroencephalographic data were recorded through the use
expected that children with ADHD-combined type will of the Lexicor NRS-24 (Lexicor Health Systems: Boulder, CO) equip-
ment and software.
exhibit increased theta activity, possibly localized in
frontal areas. Additionally, research from Clarke [5,6]
indicates that participants with ADHD-combined type
may exhibit increases in beta. This study seeks to integrate Procedure
and expand previous EEG diagnostic research and to The process for administering neurologic and physiologic tests was the
further develop an electrophysiologic profile in children same for both the ADHD and control groups. Testing took approximately
with ADHD-combined type. 3 hours on a single day. Parents completed the McCarney Attention
Deficit Disorder Evaluation Scale (ADDES) while the children were
tested. Data were collected in the same order for all participants. The
WRAT-R was administered first, followed by the TOVA, and finally the
Method referential 19-channel EEG was recorded. Individual scores on the
WRAT-R were used to determine appropriate materials for the child
Participants during the reading and story conditions.
The quantitative referential 19-channel EEG data were collected using
Participants for this study were 23 male children diagnosed with the International 10-20 system for electrode placement, including the
attention-deficit hyperactivity disorder (ADHD-combined type) and 23 central locations. Electrode placements were made using an electrode cap
male control children. The age range of the participants was from 9 to 11 (Electro Cap Co.: Eaton, OH) and Electrogel conductive gel (Weaver and
years. Participation was voluntary, and participants were recruited Co.: Aurora, CO). An electrode was placed at Oz using a discrete
through either the local school system, Children and Adults with electrode to provide an additional recording site. Linked ear electrodes
Attention Deficit/Hyperactivity Disorder (C.H.A.D.D.) group, or a neu- were used as the reference. A cotton ball was placed behind the ear
rology clinic. Participants were not known to the investigators before electrodes to isolate the referent from potential sources of contamination.
their participation in the study. No monetary payment was used to recruit Data were collected under six conditions: eyes open baseline, reading,
the participants; however, parents did receive results from the neurophys- drawing, the Ravens Progressive Matrices [12], listening to a story, and
iological and behavioral test batteries. the coding task from the WISC-R [13]. The EEG was recorded for 2
Participants were included in the ADHD group if they met the minutes for each condition.
following criteria: (1) they had been diagnosed by a physician as having
ADHD according to the Diagnostic and Statistical Manual and had
complaints of hyperactivity, inattention, and impulsivity; (2) they were
currently being treated with methylphenidate; (3) they had not been Data management
diagnosed as having a learning disability; (4) they were rated by a parent
as having symptoms of ADHD (greater than one standard deviation from All EEG data were visually inspected and artifact rejected before any
the mean) on the McCarney Attention Deficit Disorder Evaluation Scale statistical analyses were performed. Segments of EEG that involved
(ADDES); and (5) they scored in the average range on the Wide Range obvious ocular or excessive muscle activity were deleted. Each partici-
Achievement Test (WRAT). All participants in the ADHD group had pants total amount of artifact free EEG used for analyses varied, but at
medication administration suspended for at least 48 hours before testing. least 1 minute of data were analyzed for each condition. Artifact rejection
Participants in the control group were age matched to participants in was completed by two extensively trained researchers with an inter-rater
the ADHD group. Control participants were not rated on any subscale of reliability coefficient of 0.92. Bandpasses were defined as follows: delta
the ADDES as having symptoms consistent with a diagnosis of ADHD. 1 (D1) 0.75-1.75 Hz, delta 2 (D2) 2-3.75 Hz, theta (TH) 4-7.75
Any individual who volunteered for the study as a control participant Hz, alpha (AL) 8-12.75, beta 1 (B1) 13-21.75, and beta 2 (B2)
who was rated as one standard deviation or more from the mean on the 22-31 Hz.

200 PEDIATRIC NEUROLOGY Vol. 28 No. 3


Results Table 1. Significant t tests on log transformed data

Psychometric measures ADHD Control t-Test


Frequency/Condition Location Mean Mean Value
There were no significant differences in age or grade
Delta 1/Story
between the ADHD group and the normal control Fp1 0.35 0.48
group. Results from the ADDES, which were used to 2.78
establish the groups of children with and without ADHD, Fp2 0.38 0.45 2.15*
F8 0.38 0.44 2.2*
indicated significantly lower scores (poorer perfor- Fz 0.43 0.50 2.44*
mance) for the ADHD group on all subscales: inattention Alpha/Baseline
[t(44) 9.53, P 0.0005], impulsivity [t(44) 7.50, P O2 0.46 0.60 2.02*
T5 0.56 0.70 2.16*
0.0005], and hyperactivity [t(44) 7.97, P 0.0005]. T6 0.52 0.69 2.44*
Results from the TOVA continuous performance test Alpha/Reading
revealed that the ADHD group had significantly poorer F3 0.90 0.83 2.07*
performance on scores of omissions [t(44) 2.40, P F7 0.98 0.92 2.16*
Alpha/Coding
0.021)], reaction time [t(44) 4.49, P 0.0005], and T5 0.78 0.87
variability [t(44) 3.48, P 0.001]. Academic perfor- 2.84
mance as measured by the WRAT-R indicated signifi-
Note: Percentage EEG activity at a particular location increases as the
cantly lower scores for the ADHD group on spelling mean of the log transformed data becomes less negative.
[t(44) 5.72, P 0.0005], reading [t(44) 4.26, P * P 0.05
0.0005], and mathematics [t(44) 3.09, P 0.003]
P 0.01
sub-tests; however, standard scores for the children with
ADHD were all average and ranged from 90-105. Stan-
Correlations among EEG, ADDES, and TOVA
dard scores for the normal control group ranged from
107-119, which placed them between one and two stan- To assess possible relationships among EEG, ADDES,
dard deviations from the mean. and TOVA for the participants with ADHD, a Pearson
Product Moment correlation coefficient matrix was com-
puted. Only the EEG measures that significantly differed
EEG measures according to the initial multiphase analysis were correlated
with the three subscales of the ADDES and the four
Data analyses were conducted using a multiphase ap- measures generated from the TOVA. The significant
proach [4,14] that limits what portion of the data is results from this correlational matrix are presented in
analyzed, thereby reducing experiment-wise error. This Table 2.
approach uses a combination of data reduction techniques
and traditional parametric statistics. First, the total number Discussion
of data points to be compared was reduced using a Psychometric measures
principle component analysis (PCA) on the 19 recording
locations. This analysis reduced the data to a smaller set The TOVA results, excluding the commissions score,
of linear combinations that accounted for the majority of revealed significant differences between the children with
variance in the original data. Then, individual t tests on and without ADHD. For number of omissions, reaction
the actual data from all 19 recording sites were performed time, and reaction time variability measurements, the
for those factors from a given condition demonstrating a ADHD group had poorer performance compared with the
significant difference between groups. Raw data were log normal control group. These findings, in conjunction with
transformed to address the naturally skewed distribution the significant differences on the ADDES that were
initially used to establish group membership, provide
of the EEG.
support that the two groups of participants in this study
The significant findings from the PCA are summar-
demonstrated distinct patterns of behavior.
ized in Table 1 and graphically illustrated in Figure 1.
Analyses were based on percent power. Figure 1 reveals
increased right frontal delta 1 activity in the ADHD EEG measures
group during the story condition, increased alpha The EEG data revealed significant differences between
activity in the ADHD group in the posterior regions children with and without ADHD; these differences were
during the baseline condition, increased alpha activity task and bandpass specific. Differences were seen in the
in the normal control group during the reading condi- alpha band pass during the eyes open baseline condition.
tion in the left frontal region, and increased alpha Significantly more alpha was identified in the participants
activity in the ADHD group during the coding task at with ADHD at T5, T6, and O2. These findings may
T5 only. indicate that the participants with ADHD failed to sup-

Swartwood et al: EEG Differences in ADHD 201


Figure 1. Significant differences in EEG
data by cognitive condition.

Table 2. Significant correlations between ADDES, TOVA, and press alpha activity during an eyes open baseline relative
EEG for the ADHD group
to normal controls. This finding is consistent with previous
Correlation Probability research [3] using baseline measures in individuals with
Test Subscale/EEG data Coefficient Level ADHD and symptoms of impulsivity/hyperactivity. In
normal individuals, alpha activity in the posterior regions
ADHD Group
TOVA reaction time/F7-TH(drawing) 0.4687 0.024 of the brain attenuates when the eyes open [15]. Reviews
TOVA reaction time/FZ-AL(ravens) 0.5346 0.009 of alpha-related activity have generally supported the
TOVA reaction time/T5-TH(story) 0.5203 0.011 relation of this desynchronization in the posterior regions
TOVA variability/FZ-AL (ravens) 0.5066 0.014
ADDES impulsivity/T5-B1(coding) 0.4359 0.038
of the brain to engagement of the occipital lobes in the
processing of incoming visual stimuli [15]. The failure of
Note. EEG data is in the following format: location-frequency participants with ADHD to suppress alpha during a base-
(condition). Bandpasses were defined as follows: delta 1 (D1)
line condition supports the behavioral research findings
0.751.75 Hz, delta 2 (D2) 23.75 Hz, theta (TH) 4 7.75 Hz,
alpha (AL) 8 12.75, beta 1 (B1) 1321.75, and beta 2 (B2) that children with ADHD are not able to attend to and
2231 Hz. process visual stimuli as efficiently as children without
ADHD. It should also be noted that research has demon-
Abbreviations:
strated that alpha activity is impacted by anxiety [16] and
ADDES Attention Deficit Disorders Evaluation Scale increased during certain meditative states [17]; both of
TOVA Test of Variables of Attention which involve attentional processes.

202 PEDIATRIC NEUROLOGY Vol. 28 No. 3


Alpha production was also found to differ during the General conclusions
coding condition at T5; participants with ADHD produced
Results from the present study indicate few EEG dif-
significantly more alpha at this location. Since the ADHD
ferences between male children with ADHD-combined
group also had significantly more alpha-wave production at
type and matched control participants. The significant
T5 during the baseline condition, the higher alpha seen
differences that were indicated by this study depended on
during the coding condition could represent a persistence of
the task presented to the participants. Mann et al. [4] found
the abnormally high alpha waves observed during the base-
consistent differences between ADD participants without
line. Alpha persistence in the left parietal region may be hyperactivity and control participants on baseline and
indicative of parietal underactivation during the coding task. cognitively engaged tasks. The majority of these differ-
The parietal lobes are involved in writing [18], language [19], ences were associated with increased theta in the central
and drawing [20], all of which are factors that could be regions and decreased beta in posterior regions. The
expected to be active during the coding condition. current findings differ in that there were not only fewer
The finding of increased left frontal alpha activity in the significant differences overall, but those differences that
normal control group during the reading condition is were found appeared to center in the alpha frequency. The
difficult to interpret. Researchers typically interpret the most likely explanation for this discrepancy lies in the
presence of alpha activity in a particular region to signify participant selection process. In the Mann et al. study the
inactivation of that region [21]. It is interesting to note, participants were specifically chosen because they were
however, that increases in frontal alpha were also found free from complaints of hyperactivity. The present study
during a reading condition by Swartwood [14] in children specifically chose participants that experienced hyperac-
with ADHD while they were on methylphenidate. Perhaps tivity and impulsivity; therefore, the different results
methylphenidate normalized the participants frontal alpha obtained in the two studies may be due to inherent
similar to the effect seen in the control participants in the neurologic differences between children with and without
present study. Additional research is necessary to further hyperactivity.
elucidate the importance of frontal alpha during reading. It may also be the case that the cognitive tasks chosen in
Results during the story condition indicate significant this particular study did not maximize potential differ-
differences in the delta 1 bandpass at FP1, FP2, FZ, and ences between participants with ADHD-combined type
F8. For each of these locations, the mean percent power and those children not diagnosed as ADHD. Differences
for the ADHD group was significantly higher than the between children with and without ADHD are often
normal control group. These differences cluster around elusive, and they are often observable only when elicited
frontal regions (FP1, FP2, FZ) with an asymmetrical by environmental demands or consequences [1]. Future
location on the right (F8). It is possible that control research exploring differences between children with and
participants followed the instructions to visually fixate on without ADHD during tasks specifically designed to tap
a point better than the participants with ADHD, since this executive functions, such as the ability to learn from
is a common problem for children with ADHD [22]. consequences, to self-monitor behavior, and to inhibit
Alternatively, this finding may have its origin in a possible unsuccessful behaviors, may yield more consistent find-
delay in the functional maturity of the brain in children ings, as these behaviors represent fundamental problems
with ADHD, as suggested by Matsuura et al. [23]. for individuals with this disorder. Furthermore, studies
could make additional within participant comparisons,
examining how a participants baseline EEG differs from
Correlations among EEG, TOVA, and ADDES
their task-related EEG and how regional patterns vary
Correlations were conducted to assess possible relations according to task (i.e., left/right or frontal/occipital).
among the EEG, TOVA, and the ADDES for the partici- As a final note, future studies need to highlight meth-
pants with ADHD. The standard score for reaction time on odologic differences when comparing experimental results
the TOVA was negatively related to theta activity for left across studies. Differences in participant population, EEG
frontal and temporal regions during story and drawing quantification, and statistical analyses are likely to impact
tasks (Table 2). That is, higher percent power in theta was results and may be a factor in the apparent conflicting
associated with lower standard scores in reaction time on results in ADHD research regarding EEG and cognitive
the TOVA. This is consistent with suggestions by Mann activity. A meta-analysis of the existing research in this
[4] that attention decreases as theta power increases. This area would help to clarify our present understanding of the
decrease in attention probably made it more difficult for disorder and provide insight into directions for future
the ADHD group to respond promptly to the target stimuli, research.
resulting in the lower reaction time scores. The other
significant correlations for the ADHD group were between
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