NREM sleep brain networks modulate cognitive recovery from sleep deprivation

Abstract

Decrease in cognitive performance after sleep deprivation and its recovery following sleep suggests the key role of sleep, especially non-rapid eye movement (NREM) sleep, in maintaining cognition. It remains unknown whether brain network reorganization in NREM sleep stages N2 and N3 can uniquely be mapped onto individual differences in cognitive performance after a recovery nap following sleep deprivation. Using resting state functional magnetic resonance imaging (fMRI), we quantified the integration and segregation of brain networks during N2 and N3 sleep in a 1-hour nap following 24-hour sleep deprivation, compared to well-rested wakefulness. Here, we introduce a new analytic framework called the hierarchical segregation index (HSI) to quantify network segregation across spatial scales, from whole-brain to the voxel level, by identifying spatio-temporally overlapping large-scale networks and the corresponding voxel-to-region hierarchy. We found that network segregation increased in the posterior cingulate cortex during both N2 and N3 sleep compared to wakefulness. In contrast, increased segregation in the visual cortex and decreased segregation in the posterior ventromedial prefrontal cortex during N2 returned to levels comparable to wakefulness during N3. More segregation during N3 sleep was associated with worse recovery of working memory, executive attention, and psychomotor vigilance after the nap. Sleep-related changes in network segregation emerged at different spatial scales, with regional- and voxel-level alterations being associated with different cognitive tasks. Finally, we demonstrated the sensitivity and reliability of voxel-level HSI to provide key insights into within-region variation, suggesting a mechanistic understanding of how NREM sleep replenishes cognition after sleep deprivation.