Global Neural Oscillations Underlie Performance Variability and Attentional State Fluctuations in Humans

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 (i) reduced theta ({theta}) and alpha ({square}) power, (ii) decreased aperiodic signal components, indicating a shift toward cortical inhibition, (iii) enhanced phase synchronization across networks, and (iv) strengthened {theta} phase-behavior correlations ({rho}). These features support a non-network-specific framework in which low-frequency {theta} dynamics--captured by both {theta} power and {rho}--are associated with attentional fluctuations, while aperiodic offset relates to attentional state indirectly through its association with {rho} (Structural Equation Modeling: power[->]state {beta} = -0.118, p = 0.002; {rho}[->]state {beta} = 0.246, p < 0.001; offset[->]{rho} {beta} = -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.