Differential oscillatory electroencephalogram between attention-deficit/hyperactivity disorder subtypes and typically developing adolescents

Abstract

Background: A neurobiological-based classification of attention-deficit/hyperactivity disorder (ADHD) subtypes has thus far remained elusive. The aim of this study was to use oscillatory changes in the electroencephalogram (EEG) related to informative cue processing, motor preparation, and top-down control to investigate neurophysiological differences between typically developing (TD) adolescents, and those diagnosed with predominantly inattentive (IA) or combined (CB) (associated with symptoms of inattention as well as impulsivity/hyperactivity) subtypes of ADHD.

Methods: The EEG was recorded from 57 rigorously screened adolescents (12 to 17 years of age; 23 TD, 17 IA, and 17 CB), while they performed a cued flanker task. We examined the oscillatory changes in theta (3-5 Hz), alpha (8-12 Hz), and beta (22-25 Hz) EEG bands after cues that informed participants with which hand they would subsequently be required to respond.

Results: Relative to TD adolescents, the IA group showed significantly less postcue alpha suppression, suggesting diminished processing of the cue in the visual cortex, whereas the CB group showed significantly less beta suppression at the electrode contralateral to the cued response hand, suggesting poor motor planning. Finally, both ADHD subtypes showed weak functional connectivity between frontal theta and posterior alpha, suggesting common top-down control impairment.

Conclusions: We found both distinct and common task-related neurophysiological impairments in ADHD subtypes. Our results suggest that task-induced changes in EEG oscillations provide an objective measure, which in conjunction with other sources of information might help distinguish between ADHD subtypes and therefore aid in diagnoses and evaluation of treatment.

Keywords: Attention-deficit/hyperactivity disorder; EEG oscillations; connectivity; cue-processing; response preparation; top-down control.

Copyright © 2014 Society of Biological Psychiatry. Published by Elsevier Inc. All rights reserved.

Figures

Figure 1

Task figure. Participants were required to respond by button press to the centrally-presented arrow in a horizontal array of five arrows, while ignoring the surrounding or “flanking” arrows. Participants pressed with the right hand to a rightward facing arrow and the left hand to a leftward facing arrow. All stimuli were surrounded by a white border. Participants were instructed to restrict their gaze within the confines of the white border. The central arrow could be facing in either the same (congruent) or opposite (incongruent) direction to the flanking arrows. Neutral trials consisted of a centrally-presented arrow surrounded by flanking plus signs. Each stimulus was preceded by a cue which consisted of two colored cartoon hands. The figure shows the Null cue, which provided no information about the subsequent stimulus and the RP cue, which informed the participants with 84% certainty as to the motor response (left or right hand button press) that would be required for the subsequent stimulus. Trials were separated by a variable inter-trial interval (ITI; 2,400–10,400 ms). This was indicated by a color change of the surrounding border from white to green. Participants were instructed to relax their eyes during this ITI.

Figure 2

Alpha suppression after the response preparation (RP) cues. A) The topography of the post-cue alpha power reduction collapsed across the three groups. B) The time-frequency spectra locked to cue-onset, at the occipital electrode ‘Oz’, collapsed across the three groups. C) The time-course of alpha activity in the three groups of adolescents. The TD adolescents showed the greatest amount of alpha suppression 0–500 ms after the cue, whereas the IA had the least amount of alpha suppression.

Figure 3

Attentional benefit of the RP cue and alpha suppression. In the TD adolescents, the amount of alpha suppression was significantly correlated with the behavioral benefit (i.e. RT differences between null cued and RP cued correct targets) of the RP cue. Alpha suppression was not correlated with behavioral benefits of the cue in either sub-types of ADHD.

Figure 4

Trial-by-trial correlations between the frontal theta increase and the posterior alpha decrease. A) The grand-average time-frequency spectra of RP cue collapsed across groups and electrodes. B) The increase in theta activity at 50–300 ms post-cue was greatest over frontal-midline electrodes. The subsequent alpha suppression that followed occurred over occipital electrodes. C) For TD adolescents, there was a strong anti-correlation between midline fronto-central theta power and occipital alpha. This correlation was not significant in either of the ADHD subtypes.

Figure 5

The suppression of beta activity is diminished in the CB group. A) The topography of the post-cue beta activity, collapsed across the three groups. The RP cues resulted in a suppression of beta activity centered on electrodes over the motor cortex. B) The time course of post-cue beta power over the electrode contra-lateral to the cued hand in the three groups of adolescents (smoothed using a 5 point moving average method). From 800–1300 ms after cue onset, TD adolescents had the largest amount of beta suppression whereas CB adolescents showed the least. On a trial-by-trial basis, the beta activity after the cue was found to be significantly correlated with reaction times to targets.