Large-scale structure and individual fingerprints of locally coupled sleep oscillations

Abstract

Slow oscillations and sleep spindles, the canonical electrophysiological oscillations of nonrapid eye movement sleep, are thought to gate incoming sensory information, underlie processes of sleep-dependent memory consolidation, and are altered in various neuropsychiatric disorders. Accumulating evidence of the predominantly local expression of these individual oscillatory rhythms suggests that their cross-frequency interactions may have a similar local component. However, it is unclear whether locally coordinated sleep oscillations exist across the cortex, and whether and how these dynamics differ between fast and slow spindles, and sleep stages. Moreover, substantial individual variability in the expression of both spindles and slow oscillations raises the possibility that their temporal organization shows similar individual differences. Using two nights of multichannel electroencephalography recordings from 24 healthy individuals, we characterized the topography of slow oscillation-spindle coupling. We found that while slow oscillations are highly restricted in spatial extent, the phase of the local slow oscillation modulates local spindle activity at virtually every cortical site. However, coupling dynamics varied with spindle class, sleep stage, and cortical region. Moreover, the slow oscillation phase at which spindles were maximally expressed differed markedly across individuals while remaining stable across nights. These findings both add an important spatial aspect to our understanding of the temporal coupling of sleep oscillations and demonstrate the heterogeneity of coupling dynamics, which must be taken into account when formulating mechanistic accounts of sleep-related memory processing.