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

Abstract

Attention-deficit/hyperactivity disorder (ADHD) is characterized by involuntary fluctuations of attention in continuous performance tasks (CPTs) wherein attention must be sustained over long periods of time. The neuronal basis underlying aberrant attentional fluctuations in time scales from seconds to minutes have remained poorly understood. Neuronal alpha- and gamma-band oscillations are thought to implement attentional and top-down control of sensorimotor processing. We hypothesized that aberrant behavioral fluctuations in ADHD would be caused by aberrant endogenous brain dynamics in alpha and gamma-band oscillations and specifically by their aberrant long-range temporal correlations (LRTCs). We measured brain activity with magnetoencephalography (MEG) from adult participants diagnosed with ADHD (N = 19) and from healthy control subjects (N = 20) during resting state and two CPTs; a threshold stimulus detection task and a Go/NoGo task. We then estimated LRTCs of neuronal oscillations and behavioral fluctuations with detrended fluctuation analysis (DFA). ADHD was associated with aberrant LRTCs in both behavioral performance and of neuronal oscillations. LRTCs were correlated with symptom severity with a U-shaped correlations indicating that the LRTCs were largest with moderate symptom scores. These data demonstrate the presence of aberrant temporal dynamics of neuronal oscillations in adult ADHD patients, which may underlie involuntary attentional fluctuations in ADHD. Taken that LRTCs are a hallmark of brain critical dynamics, these data show that moderate ADHD symptoms scores maximize brain criticality which is thought to be beneficial for performance.