REM sleep reconfigures large-scale network dynamics: a link to its suppressive role in epilepsy

Abstract

Converging evidence suggests that human brain activity operates near a critical-like regime in which balanced excitation and inhibition support efficient large-scale communication. The brains proximity to criticality may be dynamically reset across the sleep-wake cycle and altered by epilepsy, leading to aberrant oscillatory dynamics. Building on recent work demonstrating a tripartite interaction between networks synchronization, oscillatory amplitude bistability, and cross-frequency coupling in the human brain that seems to favour epileptic activity, we examined how this interaction, and its underlying large-scale dynamics are modulated across vigilance states. We analyzed overnight recordings from 20 patients with drug-resistant epilepsy undergoing presurgical evaluation and selected overall 20 minutes of continuous, artifact free stereo-electroencephalography (SEEG) spanning REM sleep, NREM stages N2 and N3, and eyes-closed resting wakefulness. Across states, we quantified phase synchronization, phase-amplitude coupling, bistability and their correlation. REM sleep was consistently associated with a reduction of these dynamics relative to NREM sleep and wakefulness. Importantly, the canonical correlation between these measures -- reflecting the strength of the tripartite interaction -- was significantly weaker during REM sleep. These findings indicate that vigilance states modulate this previously identified multiscale interaction in human brain networks and suggest that the reduced epileptogenicity of REM sleep can be associated with a disruption of coordinated synchronization, coupling, and bistable dynamics at the large-scale network level.