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

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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 (i) reduced theta and alpha 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. These features support a non-network-specific framework in which low-frequency theta dynamics are associated with attentional fluctuations, while aperiodic offset relates to attentional state indirectly through its association with theta phase-behavior correlations. 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.

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