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Resting EEG Theta Activity Predicts Cognitive

Performance in Attention-Deficit
Hyperactivity Disorder
Daniel F. Hermens, BSc*†‡, Eleonore X.C. Soei, BSc*§, Simon D. Clarke, MD*储,
Michael R. Kohn, MD*储, Evian Gordon, PhD*‡¶, and Leanne M. Williams, PhD*†

Quantitative electroencephalography has contributed implications for the role of trait-like biologic deficits in
significantly to elucidating the neurobiologic mecha- attention-deficit hyperactivity disorder predicting per-
nisms of attention-deficit hyperactivity disorder. The formance in information processing. © 2005 by
most consistent and robust electroencephalographic Elsevier Inc. All rights reserved.
disturbance in attention-deficit hyperactivity disorder
Hermens DF, Soei EXC, Clarke SD, Kohn MR, Gordon E,
has been abnormally increased theta band during Williams LM. Resting EEG theta activity predicts cognitive
resting conditions. Separate research using attention- performance in attention-deficit hyperactivity disorder. Pedi-
demanding tests has elucidated cognitive disturbances atr Neurol 2005;32:248-256.
that differentiate attention-deficit hyperactivity disor-
der. This study attempts to integrate electroencepha-
lographic and neuropsychological indices to determine
whether cognitive performance is specifically related to Introduction
increased theta. Theta activity was recorded during a The recent U.S. prevalence of attention-deficit hyperac-
resting condition for 46 children/adolescents with at- tivity disorder (ADHD) (between 6 and 17 years) is within
tention-deficit hyperactivity disorder and their sex- the range 1.7% to 16%, consistent with the 11% estimate
and age-matched control subjects. Accuracy and reac- for Australia [1]. These figures are beyond the potentially
tion time during an auditory oddball and a visual conservative 3-5% estimate based on the Diagnostic and
continuous performance test were then recorded. Com- Statistical Manual of Mental Disorders–Fourth Edition
pared with control subjects, the attention-deficit hy- (DSM-IV) [2] criteria [3]. The DSM-IV-defined symp-
peractivity disorder group manifested significantly in- toms of ADHD include developmentally inappropriate
creased (primarily left) frontal theta. Furthermore, the levels of inattention, hyperactivity, and impulsivity. A
attention-deficit hyperactivity disorder group scored significant number of children diagnosed with ADHD will
significantly delayed reaction time and decreased ac- ultimately be prescribed treatment with stimulant medica-
curacy in both tasks. Correlation analysis revealed a tions [4]. This disorder can also have severe consequences
significant relationship between frontal (primarily left) in social, individual, and family settings, resulting from
theta and oddball accuracy for the attention-deficit financial costs of treatment, psychological implications
hyperactivity disorder group compared with a signifi- due to familial stress and breakdown, difficulties in
cant relationship between posterior (primarily right) academic and vocational areas, and increased risk of drug
theta and reaction time in the continuous performance abuse [5].
test for the control group. These results indicate that Quantitative electroencephalographic recording can
spatial neurophysiologic deficits in attention-deficit provide a noninvasive measure of baseline or the under-
hyperactivity disorder may be related to disturbances lying brain states before information processing [6]. Elec-
in signal detection. This observation has important troencephalographic measures have been observed to have

From *The Brain Dynamics Centre, ¶Division of Psychological Communications should be addressed to:
Medicine, and 储Adolescent Medicine, Westmead Hospital, NSW, Dr. Hermens; The Brain Dynamics Centre, Acacia House, Westmead
Australia; †School of Psychology, University of Sydney, NSW, Hospital, Hawkesbury Road, Westmead, NSW, 2145, Australia.
Australia; §Faculty of Psychology, Heinrich-Heine University of Received May 26, 2004; accepted November 29, 2004.
Düsseldorf, Germany; and ‡The Brain Resource International
Database, Sydney, NSW, Australia.

248 PEDIATRIC NEUROLOGY Vol. 32 No. 4 © 2005 by Elsevier Inc. All rights reserved.
doi:10.1016/j.pediatrneurol.2004.11.009 ● 0887-8994/05/$—see front matter
a high degree of sensitivity in distinguishing patients with in a relatively large sample of young unmedicated ADHD
ADHD from healthy control subjects in a wide range of adolescents. We selected an auditory signal detection
studies [7-12]. Electroencephalographic studies of the (oddball) and a visual continuous performance test, each
“resting state” (i.e., during eyes open or closed conditions) of which elicit substantial and consistent performance
have observed a consistent elevation in low-frequency deficits in ADHD. We predicted that ADHD patients
activity, particularly theta (4-7 Hz), in ADHD subjects would score increased (primarily frontal) resting theta
compared with control subjects [7-14]. Elevated theta activity and poorer performance on both cognitive tasks,
activity has been observed primarily in the frontal brain compared with matched healthy control subjects. More-
region and has been linked to a decrease in attention [12]. over, it was expected that excessive theta would be a
According to Klimesch [15], a decrease in resting or tonic significant predictive correlate of performance (both reac-
theta power is related to improved performance in cogni- tion time delays and errors) on these tasks.
tive and memory performance. In regard to underlying
neurobiologic mechanisms, elevated theta in ADHD has
Methods
been central to theories of maturational lag [10,16],
cortical hypoarousal [17,18], and developmental deviation Patients
[8,19] (see [6] for a review of these models). The frontal
focus of raised theta suggests that cortical hypoarousal Forty-six young adolescents diagnosed with ADHD (mean age 13.78;
may disrupt anterior attentional network function [20]. S.D. 1.7; range 11-17 years; 15 females) and 46 age- and sex-matched
Given that theta activity decreases with age in normal (pair-wise) healthy control subjects (mean age 13.65; S.D. 1.83; range
11-17 yrs) were recruited from the Sydney metropolitan regions as part of
subjects (reflecting neurodevelopment), a complementary the standardized Brain Resource International Database (http://www.
interpretation of excessive theta activity in ADHD is that brainresource.com). Both groups were administered a Spot-the-Word test
it reflects a maturational delay, particularly of the frontal as a measure of verbal intelligence. Univariate analysis of variance
inhibitory networks [7,10-12,18,21-23]. controlling for age found that the ADHD group produced decreased
Convergent evidence from neuroimaging and neuropsy- scores in the Spot-the-Word test compared with control subjects (F1,89 ⫽
14.24, P ⬍ 0.001).
chology points to the central role of the frontal cortices in All ADHD subjects were referred by two pediatricians (S.C., M.K.),
cognitive performance deficits in ADHD [24]. ADHD and diagnosis of ADHD was confirmed using a semi-structured interview
patients manifest equivalent performance deficits to fron- based on DSM-IV criteria for ADHD and Conners Parent Rating Scales
tal lobe lesion patients on neuropsychological tasks such (T-score 1.0 S.D. above the norm in either Inattentive or Hyperactivity/
as sustained attention [25]. Similarly, many studies have Impulsivity indices). Twenty-six individuals met the DSM-IV criteria for
the combined subtype of ADHD (8 females), whereas 20 individuals met
observed slower reaction times and greater false-positive the criteria for ADHD of the predominantly inattentive subtype (7
errors in ADHD compared with healthy subjects, on females).
frontal lobe executive function tasks [26-29]. In previous All ADHD subjects were medication-free (at least 48 hours) at the time
research, results in a continuous performance test were of testing. Nineteen ADHD individuals were medication naïve, and 27
employed to classify (in addition to behavioral ratings) were withdrawn from medication for at least 2 days before testing (15
were withdrawn from methylphenidate and 12 were withdrawn from
ADHD groups who then manifested evidence of electro- dexamphetamine).
encephalographic slowing compared with control subjects Exclusion criteria for both groups included a personal history of
with high levels of specificity [30]. Lubar et al. [31] found physical brain injury, neurologic disorder or other serious medical
that ADHD subjects (8-19 years) who manifested de- condition, or a personal history of drug or alcohol addiction. Control
creased theta after neurofeedback treatment improved subjects were also excluded if they had a family history of ADHD, Axis
1 psychiatric disorder, or genetic brain disorder. ADHD subjects were
their performance in the Test of Variables of Attention, a also excluded if they had an Axis 1 psychiatric disorder or a genetic brain
visual continuous performance test. From the same group, disorder.
Swartwood et al. [32] examined a smaller age range (9-11 All subjects were asked to refrain from drinking caffeine and smoking
years) of ADHD-Combined subtype males and demon- cigarettes 2 hours before the study session. All subjects or their guardians
strated that compared with control subjects they were provided a written informed consent form to participate in the Interna-
tional Brain Resource Database, in accordance with national health and
significantly differentiated by continuous performance test medical research council guidelines.
measures (reaction time and accuracy) and decreased
posterior alpha band activity. Although theta band differ-
ences between the groups were less apparent, they re- Procedure and Tasks
ported a correlation between left frontal theta (during a
Resting Electroencephalographic Condition. After being fitted with a
baseline task) and continuous performance test reaction Quik-Cap (NeuroScan) for electroencephalographic recording (see “Data
time [32]. Acquisition” below), subjects were seated comfortably in a sound and
Despite the promise of both raised theta and poor light attenuated room, set at an ambient temperature of 24°C. Subjects
attentional performance as markers of ADHD, the specific were asked to rest quietly with their eyes open for the duration of the
recording, and were told that the task would last for 3 minutes.
relationship between these measures in the same subjects
Cognitive Tasks. After a standardized interval of 2 minutes, an
requires further examination. The objective of this study auditory oddball signal detection task was presented. It comprised a
was to determine whether resting theta activity is related to series of high and low tones, at 75 dB of 50 ms, with an inter-stimulus
poor performance in attention-demanding cognitive tasks interval of 1.0 second. Rise and fall times of the tones were 5

Hermens et al: EEG Theta Predicts Performance in ADHD 249


milliseconds. “Background” tones were low (500 Hz), to which the Statistical Analysis
subject was asked not to respond. “Target” (signal detection) tones were
high (1000 Hz), to which the subject was asked to press buttons with the A one-way multivariate analysis of variance with “group” as the
index finger of each hand. Speed and accuracy of response were equally between-subjects factor and within-subjects factor of “quadrant” was
stressed. The 280 background and 60 target tones were presented in a undertaken for theta power. The “quadrant” factor had four levels: (left
quasi-random order, with the further constraint that two targets could not frontal: [F3, FC3, F7]; right frontal: [F4, FC4, F8]; left posterior: [CP3,
appear consecutively. Subjects were told that the duration of this task is T5, P3]; and right posterior: [CP4, T6, P4]). While the groups were
approximately 6 minutes. matched for age, young adolescence is a period of rapid neurodevelop-
The continuous performance test (sustained attention task was pre- mental change; for this reason, additional multivariate analyses of
sented after a further standardized interval of 10 minutes) consisted of a covariance were conducted with age as the covariate. Mean reaction time
series of letters (white single capital Arial font letters B, C, D, and G to targets and mean number of errors for both cognitive tasks were
were presented in pseudo-random order on a black background) pre- submitted to one-way analyses of variance (ADHD vs control subjects)
sented to the subject on the computer screen for 200 milliseconds with an and analyses of covariance to control for age effects. A Pearson
interstimulus interval (ISI) of 2.5 seconds. Subjects were instructed to correlation matrix was computed to assess whether theta power for each
simultaneously press two buttons with each index finger, if the same electrode site (three per quadrant) was related to reaction time and errors
letter appears twice in a row. Speed and accuracy of response were again in the two cognitive tasks, with the significance cutoff set at P ⬍ 0.05.
stressed equally. There were 125 stimuli in total; 85 nontarget letters and A secondary analysis was performed to assess the effect of ADHD
20 randomly presented target letters (i.e., repetitions of the previous subtype. Similar statistical tests (see above) were employed; however,
letter). Subjects were told that this task would last for 8 minutes. control subjects were omitted from the analysis and a new between-
subjects factor of “subtype” was used. Furthermore, due to case-to-
variable issues in the analyses of electroencephalographic power across
Data Acquisition the scalp sites used in the primary analysis (see above), data were
transformed into z scores and collapsed into each quadrant (thereby
Electroencephalographic Data. A Quik-Cap was used to acquire data reducing the number of dependent variables used).
from the F3, Fc3, F7, F4, Fc4, F8, Cp3, T5, P3, Cp4, T5, and P4 electrode Before statistical testing, individual variables were assessed for outli-
sites (NuAmps; 10-10 International system). Data were recorded relative ers, defined a priori using stringent criterion of beyond 3.5 standard
to the average of A1 and A2 (mastoids) electrodes sites. Horizontal eye deviations from the group means for each electrode site. New group
movements were recorded with electrodes placed 1.5 cm lateral to the mean replacement was undertaken for each outlier. The range of outliers
outer canthus of each eye. Vertical eye movements were recorded with across variables for both ADHD and control groups did not exceed 5%.
electrodes placed 3 mm above the middle of the left eyebrow and 1.5 cm All statistical analyses were performed using the Statistical Package for
below the middle of the left bottom eyelid. Skin resistance was the Social Sciences (SPSS 11.0.1).
⬍10 kOhms. A continuous acquisition system was employed, and
electrooculogram correction was carried out using a technique based on
Gratton et al. [33]. The sampling rate was 500 Hz, and a low pass filter Results
with attenuation of 40 dB per decade above 100 Hz was employed before
digitization. Electroencephalographic Analyses
Cognitive Test Data. Both accuracy and reaction time to targets (tones
or letters) were recorded in each task via a computer linked to the button Figure 1 depicts the mean theta power for ADHD and
press response box. control subjects across scalp sites during eyes open resting
activity. There was a significant group by quadrant inter-
action for theta power (F ⫽ 4.53, df ⫽ 3,270, P ⬍ 0.01).
Data Reduction
Planned contrasts revealed that this finding was due to
Electroencephalographic Data: The electroencephalographic data increased left frontal theta in ADHD subjects relative to
were screened visually for artefacts, normal variants, and changes in control subjects (F ⫽ 4.18, df ⫽ 1,90, P ⬍ 0.05; see Fig
alertness (the technician screening these data was unaware of whether 1). The subsequent analysis, controlling for age, confirmed
a subject was in the control or ADHD group). There were no
the group by quadrant interaction for theta. In this case
significant differences between ADHD and control groups (indepen-
dent samples t test) in the reported number of hours slept the night planned contrasts not only revealed the increased left
before the testing or the number and frequency of eye blinks recorded frontal theta for ADHD subjects (F ⫽ 6.56, df ⫽ 1,89,
during the task, suggesting they did not differ in alertness (spontane- P ⬍ 0.02), but also revealed significantly greater right
ous eye blinks have been demonstrated to be associated with alpha frontal theta for ADHD compared with control subjects
activity and can be used as an index of alertness [34]). Average power
(F ⫽ 4.10, df ⫽ 1,89, P ⬍ 0.05).
spectra were computed for 28 epochs during the eyes open paradigm;
2 minutes of electroencephalography were divided into adjacent
intervals of 4 seconds. Power spectral analysis was performed on each Cognitive Task Analyses
4-second interval by first applying a Welch window to the data, and
then performing a Fast Fourier Transform. Epochs were rejected Figure 2 depicts (a) mean reaction time and (b) accuracy
if the signal at three or more sites exceeded 100 ␮V for that particular
epoch. The power spectra were averaged for each electrode position, (number of errors) for both the oddball and continuous
and power was then calculated for the theta (4-7.5 Hz) frequency performance test for ADHD and control groups.
band. Theta power data were square root transformed in order that Oddball. The ADHD group scored significantly de-
they might better approximate the normal distributional assumptions layed reaction times to correctly detected oddball targets
required by parametric statistical methods. (F ⫽ 18.67, df ⫽ 1,90, P ⬍ 0.001) and more errors overall
Cognitive Tasks: The mean number of errors (total of incorrectly
pressed nontargets or false-positive and missed targets or false-negative)
(F ⫽ 22.57, df ⫽ 1,90, P ⬍ 0.001). Within the errors, the
and reaction time were calculated for each subject for both oddball and ADHD group produced more false-positive (F ⫽ 17.72,
continuous performance tests. df ⫽ 1,90, P ⬍ 0.001) and more false-negative errors (F ⫽

250 PEDIATRIC NEUROLOGY Vol. 32 No. 4


Figure 1. Mean theta (4-7.5 Hz) power (square root transformed) for ADHD and age- and sex- matched control subjects across electrode sites during
eyes open resting activity. Electrodes sites from left to right ordered according to “quadrant”: left frontal (F7, F3, FC3); right frontal (FC4, F8, F4);
left posterior (T5, P3, CP3); right posterior (CP4, P4, T6). ADHD subjects manifested significantly increased theta power in the left frontal quadrant
compared with control subjects.

13.09, df ⫽ 1,90, P ⬍ 0.001) compared with control contrast, the control group had an association only be-
subjects. Follow-up analysis controlling for age confirmed tween right frontal theta and oddball errors (see Table 1
this pattern of results. for the correlation coefficients across sites). Partial corre-
Continuous Performance Test. The ADHD group again lations (controlling for age) indicated no changes in these
produced significantly delayed reaction times to correctly results. The scatter plots depicted in Figure 3 exemplify
detected targets (F ⫽ 24.65, df ⫽ 1,90, P ⬍ 0.001) and the differential pattern of left and right frontal theta
more errors overall (F ⫽ 21.132, df ⫽ 1,90, P ⬍ 0.001). associations with oddball errors for control and ADHD
Within the errors, the ADHD group scored more false- groups.
positive (F ⫽ 12.86, df ⫽ 1,90, P ⬍ 0.001) and more The inclusion of the error types (false- positive or
false-negative (F ⫽ 36.33, df ⫽ 1,90, P ⬍ 0.001) errors false-negative) revealed that for control subjects the sig-
compared with control subjects. Similarly, follow-up anal- nificant relationship found between (overall) errors and
ysis controlling for age did not change the pattern of these (right frontal) theta may be the result of false-positive and
results. not false-negative errors. For ADHD, however, the asso-
ciation observed between left frontal theta and errors could
Correlation Analyses be attributed to the combination of false-positives and
false-negatives, because both error types produced rela-
Table 1 summarizes the Pearson correlation matrices tively high correlation coefficients with left frontal sites
conducted for each group. ADHD and control groups were (note: only F7 and FN reached significance). There was a
distinguished by clearly distinct patterns of associations in similar pattern for ADHD in continuous performance test
these measures. In control subjects, there was a significant errors and theta, with false-negative and left frontal theta
positive association between theta at (primarily) posterior (F3) reaching significance. Partial correlations (controlling
sites and reaction in the continuous performance test (the for age) yielded no changes in the overall error type results
oddball reaction time did not reach significance). The for both groups.
ADHD group did not manifest any patterns of association
between theta and reaction time. A secondary correlation Subtype Analyses
analysis controlling for age indicated that the association
between continuous performance test reaction time and Secondary analyses indicated that ADHD subtypes
theta for control subjects failed to reach significance. were significantly different in false-negative errors during
For the ADHD group, theta power revealed a significant the continuous performance test, with ADHD-Combined
positive relationship with errors on the oddball (but not producing increased false-negative errors compared with
continuous performance test) for left frontal sites. In ADHD-Inattentive (F ⫽ 5.98 df ⫽ 1,44, P ⬍ 0.05), and

Hermens et al: EEG Theta Predicts Performance in ADHD 251


Figure 2. (a) Mean reaction time to correctly detected targets during auditory oddball and visual continuous performance test (CPT) for ADHD and
age- and sex- matched control subjects. (b) Mean total number of errors committed during auditory oddball and visual CPT for ADHD and age- and
sex-matched control subjects. ADHD subjects manifested significantly increased reaction time and made more errors in both tasks compared with
matched control subjects.

continuous performance test reaction time was of border- larly in (left) frontal regions. They also manifested both
line significance with ADHD-Combined revealing de- delayed reaction time and increased errors in subsequent
layed reaction time compared with ADHD-Inattentive signal detection and continuous performance tests. Nota-
(F ⫽ 4.03, df ⫽ 1,44, P ⬍ 0.05). These results were bly, abnormally elevated (primarily left) frontal resting
unchanged when controlling for age. There were no other theta activity correlated with poorer performance in the
differences between the ADHD subtype groups for per- signal detection (oddball) task for the ADHD group.
formance and theta measures. ADHD and control groups were distinguished most clearly
by two patterns of associations between theta and perfor-
Discussion mance measures. For ADHD, there was a positive associa-
tion between frontal (primarily left) resting theta and errors in
This study undertook a direct examination of the rela- the oddball task. This association was virtually absent for
tionship between elevated electroencephalographic theta control subjects (with one right frontal electrode site yielding
(particularly in frontal sites) and poorer cognitive perfor- a significant relationship with oddball errors). The different
mance in ADHD children/adolescents compared with pattern of association between frontal theta and oddball errors
control subjects. Although previous studies of electroen- for ADHD and control groups is exemplified in Figure 3. For
cephalographic and cognitive measures have each impli- control subjects, reaction time for the continuous perfor-
cated the importance of frontal brain dysfunction in mance test was predicted positively by (primarily right)
ADHD, a direct association between these measures and posterior theta; there was no evidence of this pattern in the
concomitant recording in the same subjects has rarely been ADHD group. This pattern did not reach significance (in
addressed. To our knowledge, one other study [32] has control subjects) when the correlations controlled for the
examined the association between baseline electroen- effects of age.
cephalographic measures and cognitive tasks in ADHD Swartwood et al. [32] also found a left frontal theta
Combined subtype males. The current study adds to these relationship with poorer performance in ADHD; however,
previous findings by examining a larger and older ADHD this was in relation to a reaction time measure during the
group (containing both sexes) with Combined and Inatten- test of variables of attention. They did not report correla-
tive subtypes. This study has focused on theta (because it tions between these measures for control subjects. In the
is the most robust electroencephalographic finding in current study, the ADHD group appears to be manifesting
ADHD) and examined relationships with performance signs of “pervasive ADHD” described by Oades [35],
measures in auditory and visual attention-demanding tests. which is highlighted by impairment in left frontal func-
Consistent with predictions, ADHD subjects manifested tion; that is, a deficit relating to detailed stimulus identi-
excessive theta power during resting conditions, particu- fication or decision-making, possibly over and above a

252 PEDIATRIC NEUROLOGY Vol. 32 No. 4


Table 1. Correlation coefficients between (a) oddball and (b) continuous performance task measures (reaction time, false-positives, false-
negatives, and errors) for each site*

Reaction Time False-Positives False-Negatives Errors


a. Oddball Control ADHD Control ADHD Control ADHD Control ADHD

F7 0.24 0.25 0.11 0.32‡ ⫺0.14 0.24 0.05 0.34‡


LF F3 0.23 0.23 0.18 0.28 ⫺0.04 0.28 0.15 0.41§
FC3 0.25 0.14 0.15 0.15 ⫺0.09 0.23 0.10 0.24
FC4 0.25 0.18 0.16 0.17 ⫺0.06 0.15 0.12 0.26
RF F4 0.19 0.09 0.23 0.08 0.07 0.19 0.23 0.26
F8 0.08 0.21 0.34‡ 0.27 0.10 0.25 0.35‡ 0.22
T5 0.06 0.15 0.14 0.20 0.07 0.28 0.16 0.16
LP P3 0.18 ⫺0.03 0.12 0.08 ⫺0.17 0.16 0.04 ⫺0.01
CP3 0.18 ⫺0.08 0.10 0.03 ⫺0.15 0.12 0.03 0.00
CP4 0.25 0.01 0.17 0.03 ⫺0.08 0.23 0.12 0.04
RP P4 0.23 0.01 0.13 ⫺0.03 ⫺0.13 0.02 0.07 0.10
T6 0.17 0.06 0.14 0.08 0.00 0.11 0.13 0.06
Reaction Time False-Positives False-Negatives Errors
b. CPT Control ADHD Control ADHD Control ADHD Control ADHD

F7 0.19 0.12 0.14 0.02 ⫺0.09 0.24 0.00 0.22


LF F3 0.28 0.05 0.21 0.17 ⫺0.03 0.35‡ 0.11 0.26
FC3 0.29† 0.03 0.22 0.00 ⫺0.01 0.23 0.10 0.06
FC4 0.27 0.07 0.28 0.03 0.00 0.23 0.16 0.12
RF F4 0.26 0.13 0.24 0.04 0.00 0.24 0.16 0.11
F8 0.18 0.08 0.20 0.00 0.03 0.21 0.10 0.18
T5 0.17 0.19 0.13 0.01 0.06 0.17 0.07 0.05
LP P3 0.30† 0.13 0.16 ⫺0.11 0.01 0.12 0.07 ⫺0.03
CP3 0.29† 0.07 0.12 ⫺0.13 ⫺0.07 0.12 0.02 ⫺0.04
CP4 0.35‡ 0.07 0.21 ⫺0.10 0.01 0.19 0.14 ⫺0.01
RP P4 0.33† 0.03 0.15 ⫺0.15 0.00 ⫺0.07 0.09 ⫺0.12
T6 0.25 0.09 0.21 ⫺0.07 0.04 0.03 0.15 0.01

* Categorized into regions: left frontal (LF), right frontal (RF), left posterior (LP), right posterior (RP) for eyes open theta power for control subjects
(left columns) and ADHD patients (right columns).
Coefficients are highlighted when significant at † P ⬍ 0.05, ‡ P ⬍ 0.025, § P ⬍ 0.005.

Abbreviations:
ADHD ⫽ Attention-deficit hyperactivity disorder
CPT ⫽ Continuous performance test

general deficit in global attention function governed by tasks may also be a factor, which should be tested in future
right frontal control [35]. The relationship between pri- studies.
marily left frontal theta and oddball errors may reflect a For the ADHD group, theta power was a significant
lateralization unlike normal control subjects (or lack positive predictor (correlate) of oddball task errors across
thereof). However, the association documented in control both left and right frontal sites. In contrast to control
subjects of right frontal theta and oddball errors accords subjects, the most robust positive associations were ob-
with the broader implication of right frontal networks in served for left frontal theta and oddball errors. In this
novelty detection, and the role of theta in determining regard, we speculate that an excess of frontal theta makes
salient sensory input for incorporation into memory. This a central contribution to ADHD decrements in signal
observation is consistent with functional neuroimaging detection. The combination of relatively greater left frontal
studies, which reveal preferential right inferior frontal theta, and the more consistent association between left
engagement in oddball and continuous performance tests frontal theta and oddball performance in ADHD, may
[36-38]. The relatively greater association of theta with reflect a related disturbance in the normal right frontal
errors for the oddball task (in ADHD) compared with lateralization of task-relevant signal discrimination.
reaction time for the continuous performance test (in Our findings provide preliminary evidence to suggest
control subjects) may reflect the differential processing that abnormal frontal theta activity in ADHD is related
demands of these tasks, namely: accuracy for the oddball specifically to difficulties with signal detection, given that
task (in which a nontarget must be ignored), and speed for the oddball task taps the ability to extract task-relevant
the continuous performance test (which requires sustained signals from task-irrelevant background “noise”. This
vigilance for a changing target, rather than selection of proposal accords with reports that left frontal lesion
targets vs nontargets). Furthermore, the modality of these patients have similar performance decrements on attention

Hermens et al: EEG Theta Predicts Performance in ADHD 253


Figure 3. Scatter plots depicting the different pattern of associations between theta power at frontal sites and oddball errors. (a) Control subjects (left
frontal); (b) control subjects (right frontal); (c) ADHD (left frontal); (d) ADHD (right frontal) vs number of errors. For ADHD, associations were
significant primarily for left frontal theta, exemplified by F7 electrode (c) and (to a lesser extent) for right frontal theta, exemplified by F8 electrode (d),
whereas control subjects manifested only right frontal theta associations, F8 electrode (b), revealing a different pattern from ADHD.

to task-relevant signals, tapped by choice reaction tasks mental deviation [8], and cortical hypoarousal [17] by
[39]. Clinically, the findings suggest that inattention is a incorporating tasks that demand an increasing attentional
fundamental characteristic of ADHD, in terms of under- load.
lying brain disturbances and their behavioral manifestation A correspondence in the disturbances (increased theta
in “signal vs noise” discrimination deficits. Indeed, resting coupled with poorer performance) across age suggests that
theta has previously been interpreted as an index of a developmental deviation, rather than a maturational lag,
inattention in this disorder [12,32], and increased errors in model may more precisely account for ADHD. Further
discriminating targets (predicted by raised theta) also point light might be shed on this issue in future research by the
to inattention (within both Combined and Inattentive analysis of additional electroencephalographic frequency
subtypes). In this regard, normal baseline theta might be bands and the inclusion of electrodermal indices, given
conceptualized as a prelude to good performance in that the cortical hypoarousal model has been conceptual-
attention-demanding tasks. In healthy subjects, enhanced ized as a specific version of the developmental deviation
theta has been related to sleepiness [40] and predicts model [6]. Clinically, the inclusion of a hyperactive/
similarly poor cognitive performance [15], possibly via impulsive subgroup would be valuable in differentiating
enhanced activity in cortico-hippocampal feedback loops these models, given that these symptoms are thought to be
[15]. The role of theta activity in indexing attention should more susceptible to maturational changes [13,41]. As
be further addressed in electroencephalography-based Barry et al. [6] have pointed out, these models may prove
models of ADHD such as maturational lag [16], develop- to be too simplistic and a profile of information across data

254 PEDIATRIC NEUROLOGY Vol. 32 No. 4


modalities (from performance to physiologic and brain measures in adolescent attention deficit hyperactivity disorder. Int
imaging) may in the longer term provide the most com- J Psychophysiol 1999;34:123-34.
[12] Mann CA, Lubar JF, Zimmerman AW, Miller CA, Muenchen
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