Is mild ADHD beneficial? Brain criticality peaks at intermediate ADHD symptom scores across the population

Abstract

Attention-deficit/hyperactivity disorder (ADHD) is characterized by a continuum of symptoms including inattentiveness, hyperfocus, and hyperactivity, that are manifested, e.g., in increased reaction-time variability in continuous performance tasks (CPTs). Framework of brain criticality posits that brains operate in an extended regime of critical-like dynamics where neuronal and behavioral processes exhibit scale-free long-range temporal correlations (LRTCs) across hundreds of seconds. Whether shifts across critical-like brain states and parallel changes in LRTCs underlie ADHD symptoms has remained unexplored. We investigated whether brain-state shifts towards excitation-dominated dynamics and associated changes in LRTCs could explain ADHD symptoms and their continuum across individuals. We measured brain activity with magnetoencephalography (MEG) during resting and two CPTs from adult participants diagnosed with ADHD (N = 34) and neurotypical controls (NC) (N = 36) and characterized criticality with LRTCs of neuronal oscillations. ADHD patients exhibited stronger LRTCs than NC in low (5-20 Hz) and high (30-100 Hz) frequencies and dichotomous task effects. High-frequency LRTCs were positively correlated with ADHD symptoms, while beta-band (20-30 Hz) activity exhibited a quadratic correlation, peaking at moderate scores across the ADHD and NC cohorts being smaller for low and high scores. We demonstrate that ADHD is associated with shifts in brain criticality in resting-and task-state brain dynamics. Individuals with intermediate symptom scores across the NC and ADHD cohorts operated at peak criticality that is associated with a several functional benefits The progressive shift towards the supercritical side of the critical regime becomes detrimental only at moderate and severe symptoms.