Large-scale brain functional modularity is reflected in slow electroencephalographic rhythms across the human non-rapid eye movement sleep cycle

Enzo Tagliazucchi, Frederic von Wegner, Astrid Morzelewski, Verena Brodbeck, Sergey Borisov, Kolja Jahnke, Helmut Laufs

Research output: Contribution to journalArticlepeer-review

84 Scopus citations

Abstract

Large-scale brain functional networks (measured with functional magnetic resonance imaging, fMRI) are organized into separated but interacting modules, an architecture supporting the integration of distinct dynamical processes. In this work we study how the aforementioned modular architecture changes with the progressive loss of vigilance occurring in the descent to deep sleep and we examine the relationship between the ensuing slow electroencephalographic rhythms and large-scale network modularity as measured with fMRI. Graph theoretical methods are used to analyze functional connectivity graphs obtained from fifty-five participants at wakefulness, light and deep sleep. Network modularity (a measure of functional segregation) was found to increase during deeper sleep stages but not in light sleep. By endowing functional networks with dynamical properties, we found a direct link between increased electroencephalographic (EEG) delta power (1-4. Hz) and a breakdown of inter-modular connectivity. Both EEG slowing and increased network modularity were found to quickly decrease during awakenings from deep sleep to wakefulness, in a highly coordinated fashion. Studying the modular structure itself by means of a permutation test, we revealed different module memberships when deep sleep was compared to wakefulness. Analysis of node roles in the modular structure revealed an increase in the number of locally well-connected nodes and a decrease in the number of globally well-connected hubs, which hinders interactions between separated functional modules. Our results reveal a well-defined sequence of changes in brain modular organization occurring during the descent to sleep and establish a close parallel between modularity alterations in large-scale functional networks (accessible through whole brain fMRI recordings) and the slowing of scalp oscillations (visible on EEG). The observed re-arrangement of connectivity might play an important role in the processes underlying loss of vigilance and sensory awareness during deep sleep.

Original languageEnglish
Pages (from-to)327-339
Number of pages13
JournalNeuroImage
Volume70
DOIs
StatePublished - 15 Apr 2013
Externally publishedYes

Keywords

  • EEG-fMRI
  • Functional networks
  • Modularity
  • Resting state
  • Sleep
  • Wakefulness

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