Functional connectivity dynamics slow with descent from wakefulness to sleep.

Mazen El-Baba,Daniel J Lewis,J Bruce Morton,Zhuo Fang,Adrian M Owen,Stuart M Fogel,Lawrence M Ward

doi:10.1371/journal.pone.0224669

Abstract

The transition from wakefulness to sleep is accompanied by widespread changes in brain functioning. Here we investigate the implications of this transition for interregional functional connectivity and their dynamic changes over time. Simultaneous EEG-fMRI was used to measure brain functional activity of 21 healthy participants as they transitioned from wakefulness into sleep. fMRI volumes were independent component analysis (ICA)-decomposed, yielding 42 neurophysiological sources. Static functional connectivity (FC) was estimated from independent component time courses. A sliding window method and k-means clustering (k = 7, L2-norm) were used to estimate dynamic FC. Static FC in Wake and Stage-2 Sleep (NREM2) were largely similar. By contrast, FC dynamics across wake and sleep differed, with transitions between FC states occurring more frequently during wakefulness than during NREM2. Evidence of slower FC dynamics during sleep is discussed in relation to sleep-related reductions in effective connectivity and synaptic strength.

Highlights

The transition from wakefulness to sleep is highly organized into a continuum of heterogeneous stages that change dynamically over the course of a single night and is associated with marked alterations in brain function and cognition
Consistent with our predictions, qualitative changes in whole-brain functional connectivity occurred less frequently over time when participants were asleep compared to when they were awake. This sleep-related slowing of connectivity dynamics was most clearly reflected by a decrease in the number of transitions between qualitatively distinct connectivity states during sleep relative to wakefulness, and by an increase in the length of time between transitions
This is consistent with differences in the mode of operation of cortico-subcortical circuitry in NREM2 compared to wake, whereby at the cellular level, the brain oscillates between up-states, separated by down-states [23,24,25,26]

Summary

Introduction

The transition from wakefulness to sleep is highly organized into a continuum of heterogeneous stages that change dynamically over the course of a single night and is associated with marked alterations in brain function and cognition. There is, for example, a marked reduction in long-range inter-cortical functional connectivity (FC) in the descent from alert wakefulness to deep, slow-wave sleep [1,2,3], and a dampening of inter-regional effective connectivity dynamics [4]. This reduced connectivity may represent processes which support the known functions of sleep, including reduced sensory processing [5,6], the disengagement of executive control [7], synaptic homeostasis [8], and sleep-dependent memory processes [9,10,11,12]. The method is powerful as EEG provides a gold-standard means of identifying qualitatively distinct sleep stages and fMRI provides a whole-brain, albeit indirect, measure of brain

Methods

Results

Conclusion