Abstract

Recent research has found that the human sleep cycle is characterised by changes in spatiotemporal patterns of brain activity. Yet, we are still missing a mechanistic explanation of the local neuronal dynamics underlying these changes. We used whole-brain computational modelling to study the differences in global brain functional connectivity and synchrony of fMRI activity in healthy humans during wakefulness and slow-wave sleep. We applied a whole-brain model based on the normal form of a supercritical Hopf bifurcation and studied the dynamical changes when adapting the bifurcation parameter for all brain nodes to best match wakefulness and slow-wave sleep. Furthermore, we analysed differences in effective connectivity between the two states. In addition to significant changes in functional connectivity, synchrony and metastability, this analysis revealed a significant shift of the global dynamic working point of brain dynamics, from the edge of the transition between damped to sustained oscillations during wakefulness, to a stable focus during slow-wave sleep. Moreover, we identified a significant global decrease in effective interactions during slow-wave sleep. These results suggest a mechanism for the empirical functional changes observed during slow-wave sleep, namely a global shift of the brain’s dynamic working point leading to increased stability and decreased effective connectivity.

Highlights

  • Recent research has found that the human sleep cycle is characterised by changes in spatiotemporal patterns of brain activity

  • We found that 83% of all the subjects exhibit higher functional connectivity (FC) node strength during wakefulness than during sleep, indicating that the group FC matrices represent the average participant with high accuracy

  • Using the whole-brain model we found a significant shift of the brain’s global working point from the edge of the transition between noisy and sustained oscillatory behaviour during wakefulness to a noisy regime characterised by a stable focus during slow-wave sleep as a possible mechanistic explanation of the observed empirical functional changes between those two brain states

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Summary

Introduction

Recent research has found that the human sleep cycle is characterised by changes in spatiotemporal patterns of brain activity. While the EEG shows clear changes between the two, it is less clear how the brain’s spatiotemporal dynamics supports these different behavioural states From this perspective recent decades’ research has improved our understanding of wakefulness in particular, characterising the organisation of the brain’s spontaneous activity in terms of correlated activity patterns across different brain regions (as measured with functional resonance imaging [fMRI]), www.nature.com/scientificreports/. Combined transcranial magnetic stimulation and electroencephalography (TMS-EEG) studies have shown decreased cortical effective connectivity during deep sleep, with effective connectivity understood here as the capacity for a causal interaction in response to an external perturbation[22,23,24,25] This result suggests a lowering of the capability of the brain to integrate information across different cortical areas and a diminished capacity to amplify local perturbations

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