Dissociable Oscillatory Alpha and Aperiodic Neural Dynamics Underlie Atypical Attentional Control in Children With Attention-Deficit/Hyperactivity Disorder (ADHD)

Children with attention-deficit/hyperactivity disorder (ADHD) often have difficulty maintaining goal-directed attention when task-relevant and task-irrelevant information compete for processing resources. The present study investigated whether this difficulty reflects distinct abnormalities in demand-related attentional regulation and distractor-related neural responses. We recorded electroencephalography (EEG) signals from 45 children with ADHD and 45 typically developing (TD) children while they performed a visual detection task under low and high visual demands, with simultaneous task-irrelevant standard and deviant sounds. EEG power spectra were parameterized to separate oscillatory alpha activity from aperiodic activity, as putative indices of attentional regulation and cortical excitation/inhibition (E/I) balance, respectively. TD children showed adaptive demand-related alpha modulation, whereas children with ADHD showed an atypical alpha response pattern, including reduced frontal modulation and atypical posterior alpha enhancement; this demand-related group difference was observed in oscillatory alpha activity but not in aperiodic activity. In contrast, ADHD-related abnormalities in responses to auditory distractors were more clearly reflected in the aperiodic slope. Children with ADHD showed atypical distractor-related aperiodic modulation, suggesting reduced stability of neural background activity, potentially reflecting disrupted cortical E/I balance when irrelevant sounds had to be ignored. Furthermore, multivariate machine learning classification demonstrated that relying on these sensitive neural signatures yielded robust discrimination between children with ADHD and TD controls, with significant predictive performance emerging shortly after stimulus onset and sustaining throughout information processing. These findings suggest that oscillatory alpha activity and aperiodic neural dynamics show differential sensitivity to distinct attentional abnormalities in ADHD, with alpha oscillations primarily reflecting demand-related regulatory deficits and aperiodic activity primarily reflecting distractor-related neural instability.