Sleep modulates neural timescales and spatiotemporal integration in the human cortex

Abstract

Spontaneous neural dynamics manifest across multiple timescales, which are intrinsic to brain areas and exhibit hierarchical organization across the cortex. In wake, a hierarchy of timescales is thought to naturally emerge from microstructural properties, gene expression, and recurrent connections. A fundamental question is timescales organization and changes in sleep, where physiological needs are different. Here, we describe two coexisting but distinct measures of neural timescales, obtained from broadband activity and gamma power, which display complementary properties. We leveraged intracranial electroencephalography (iEEG) data to characterize timescale changes from wake to sleep across the cortical hierarchy. We show that both broadband and gamma timescales are globally longer in sleep than in wake. While broadband timescales increase along the sensorimotor-association axis, gamma ones decrease. During sleep, slow waves can explain the increase of broadband and gamma timescales, but only broadband ones show a positive association with slow-wave density across the cortex. Finally, we characterize spatial correlations and their relationship with timescales as a proxy for spatiotemporal integration, finding high integration at long distances in wake for broadband and at short distances in sleep for gamma timescales. Our results suggest that mesoscopic neural populations possess different timescales that are shaped by anatomy and are modulated by the sleep/wake cycle. Significance statementUnderstanding the organization of intrinsic neural dynamics is crucial for investigating brain functions in health and disease. A key question is: how do neural dynamics change in the sleeping brain? Here we focus on neural timescales, which measure temporal autocorrelation and are organized hierarchically across the cortex, and spatial correlations. We show that two types of timescales exist in neural populations recorded with intracranial electroencephalography in humans, corresponding to broadband (0.5-80 Hz) and gamma (40-80 Hz) frequency ranges. Both timescales increase in sleep, where slow waves have an important role, but follow opposite hierarchies: broadband timescales increase from sensory to associative areas, while gamma timescales show the reverse pattern. Finally, timescales covary with spatial correlations, suggesting higher spatiotemporal integration over long distances in wake compared to sleep.