ADHD symptoms across the population are explained by individual variability in brain criticality

Attention-deficit/hyperactivity disorder (ADHD) is characterized by a continuum of symptoms, including inattentiveness, impulsiveness, and hyperactivity, which can negatively impact daily life. In laboratory settings, these deficits are manifested as increased reaction-time variability in continuous performance tasks (CPTs) over several minutes. Although considerable work has elucidated neural mechanisms associated with ADHD, less is known about how these mechanisms vary across the continuum of symptom severity. We investigated whether symptom severity could be explained in the Extended Brain Criticality framework. Brains operate in an extended critical regime between disorder (asynchronous) and order (synchronous) at balanced excitation-inhibition which is characterized by moderate synchronization and scale-free long-range temporal correlations (LRTCs) across hundreds of seconds. We hypothesized that differences in brain operating points (brain states) along the critical-like regime and paralleled changes in LRTCs could predict ADHD symptom continuum. We measured brain activity with magnetoencephalography (MEG) during rest and two CPTs from adult ADHD and control participants and assessed criticality with LRTCs of neuronal oscillations. LRTCs showed high variability, but overall ADHD patients exhibited stronger LRTCs than NC in low (5-20 Hz) and high (30-100 Hz) frequencies as well as stronger task effects. ADHD symptom severity was predicted by individual variability in LRTCs and i.e., by the individual's position in the critical phase with both linear and quadratic correlations such that the severity of symptoms were predicted by shifts of the operating point toward the supercritical direction in a frequency dependent manner. Our study thus proposes a novel complex systems-level framework to explain the emergence of ADHD symptoms and their continuum across the population.