Global neural oscillations underlie performance variability and attentional state fluctuations in humans

Abstract

Fluctuations in attentional states, such as mind-wandering (MW), are associated with critical variability in task performance. While fMRI studies highlight the opposing roles of task-positive (e.g., dorsal attention network) and task-negative (e.g., default mode network) systems, the electrophysiological mechanisms underlying these dynamics remain poorly understood. Using intracranial electrocorticography in humans performing a sustained attention task, we identified global oscillatory dynamics linked to attentional shifts. MW was characterized by (1) reduced theta (θ) and alpha (α) power, (2) decreased aperiodic signal components, indicating a shift toward cortical inhibition, (3) enhanced phase synchronization across networks, and (4) strengthened θ phase-behavior correlations (ρ). These features support a non-network-specific framework in which low-frequency θ dynamics—captured by both θ power and ρ—are associated with attentional fluctuations, while aperiodic offset relates to attentional state indirectly through its association with ρ (structural equation modeling: power → state β = − 0.118, p = 0.002; ρ → state β = 0.246, p < 0.001; offset → ρ β = − 0.222, p < 0.001). Our study provides a unified neurophysiological framework for understanding how spontaneous neural activity can drive attentional fluctuations and performance variability, with implications for research on attention, learning, and neuropsychiatric disorders.