Linking alpha oscillations, attention and inhibitory control in adult ADHD with EEG neurofeedback

Marie-Pierre Deiber, Roland Hasler, Julien Colin, Alexandre Dayer, Jean-Michel Aubry, Stéphanie Baggio, Nader Perroud, Tomas Ros, Marie-Pierre Deiber, Roland Hasler, Julien Colin, Alexandre Dayer, Jean-Michel Aubry, Stéphanie Baggio, Nader Perroud, Tomas Ros

Abstract

Abnormal patterns of electrical oscillatory activity have been repeatedly described in adult ADHD. In particular, the alpha rhythm (8-12 Hz), known to be modulated during attention, has previously been considered as candidate biomarker for ADHD. In the present study, we asked adult ADHD patients to self-regulate their own alpha rhythm using neurofeedback (NFB), in order to examine the modulation of alpha oscillations on attentional performance and brain plasticity. Twenty-five adult ADHD patients and 22 healthy controls underwent a 64-channel EEG-recording at resting-state and during a Go/NoGo task, before and after a 30 min-NFB session designed to reduce (desynchronize) the power of the alpha rhythm. Alpha power was compared across conditions and groups, and the effects of NFB were statistically assessed by comparing behavioral and EEG measures pre-to-post NFB. Firstly, we found that relative alpha power was attenuated in our ADHD cohort compared to control subjects at baseline and across experimental conditions, suggesting a signature of cortical hyper-activation. Both groups demonstrated a significant and targeted reduction of alpha power during NFB. Interestingly, we observed a post-NFB increase in resting-state alpha (i.e. rebound) in the ADHD group, which restored alpha power towards levels of the normal population. Importantly, the degree of post-NFB alpha normalization during the Go/NoGo task correlated with individual improvements in motor inhibition (i.e. reduced commission errors) only in the ADHD group. Overall, our findings offer novel supporting evidence implicating alpha oscillations in inhibitory control, as well as their potential role in the homeostatic regulation of cortical excitatory/inhibitory balance.

Keywords: Adult ADHD; Alpha oscillations; EEG; Inhibition control; Neurofeedback.

Conflict of interest statement

Declaration of Competing Interest None of the authors has any conflict of interest to disclose.

Copyright © 2019 The Author(s). Published by Elsevier Inc. All rights reserved.

Figures

Fig. 1
Fig. 1
Timeline of the experimental procedure. EO: eyes opened; CPT: Continuous Performance Task; Q: self-rated questionnaires (Spielberger's and Thayer's).
Fig. 2
Fig. 2
Relative alpha power for ADHD (black solid line) and healthy controls HC (red dashed line) in each condition (average over the 64 electrodes). Bars represent confidence intervals. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)
Fig. 3
Fig. 3
Top: EEG relative power spectrum at baseline (EO1) in ADHD patients (red) and healthy subjects (HC, green). Solid lines: mean relative value over the 64 electrodes, highlighted areas: confidence interval. Bottom: Topographic plots of relative alpha amplitude in EO1 for the ADHD and HC groups, and unpaired permutation test (binomial corrected, p < .05). (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)
Fig. 4
Fig. 4
Top: EEG relative power spectrum during EO2 (green), EO3 (red) and NFB (gray) in ADHD (left) and HC (right). Solid lines: mean relative value over the 64 electrodes, highlighted areas: confidence interval. Bottom, first row: Topographic plots of relative alpha amplitude in NFB and EO2, and paired permutation test (binomial corrected, p < .05). Bottom, second row: Topographic plots of relative alpha amplitude in EO3 and EO2, and paired permutation test (binomial corrected, p < .05). (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)
Fig. 5
Fig. 5
Top: EEG relative power spectrum during CPT1 (green) and CPT2 (red) in ADHD (left) and HC (right). Solid lines: mean relative value over the 64 electrodes, highlighted areas: confidence interval. Bottom: Topographic plots of relative alpha amplitude in CPT2 and CPT1, and paired permutation test (binomial corrected, p < .05). (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)
Fig. 6
Fig. 6
Correlation between commission differences and A. CPT2-CPT1 relative alpha power differences, B. CPT2-CPT1 NoGo trials ERD differences in ADHD.
Fig. 7
Fig. 7
Theoretical model linking alpha oscillations, cortical E/I balance and behavioral performance. U-relationship between elevated response inhibition (i.e. commission) errors, alpha amplitude and cortically hyper- or hypo- activated ADHD biotypes.

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