Abstract

Frontal and parietal regions are associated with some of the most complex cognitive functions, and several frontoparietal resting-state networks can be observed in wakefulness. We used functional magnetic resonance imaging data acquired in polysomnographically validated wakefulness, light sleep, and slow-wave sleep to examine the hierarchical structure of a low-frequency functional brain network, and to examine whether frontoparietal connectivity would disintegrate in sleep. Whole-brain analyses with hierarchical cluster analysis on predefined atlases were performed, as well as regression of inferior parietal lobules (IPL) seeds against all voxels in the brain, and an evaluation of the integrity of voxel time-courses in subcortical regions-of-interest. We observed that frontoparietal functional connectivity disintegrated in sleep stage 1 and was absent in deeper sleep stages. Slow-wave sleep was characterized by strong hierarchical clustering of local submodules. Frontoparietal connectivity between IPL and superior medial and right frontal gyrus was lower in sleep stages than in wakefulness. Moreover, thalamus voxels showed maintained integrity in sleep stage 1, making intrathalamic desynchronization an unlikely source of reduced thalamocortical connectivity in this sleep stage. Our data suggest a transition from a globally integrated functional brain network in wakefulness to a disintegrated network consisting of local submodules in slow-wave sleep, in which frontoparietal inter-modular nodes may play a role, possibly in combination with the thalamus.

Highlights

  • IntroductionThese functionally comprehensive networks of regions are consistently observed throughout multiple time-series analyses, such as correlation against the timecourse of a particular seed region (Biswal et al, 1995; Fox et al, 2005; Fox and Raichle, 2007) or spatiotemporal independent component analysis (ICA; Beckmann et al, 2005; Damoiseaux et al, 2006)

  • Ultraslow fluctuations (

  • We used functional magnetic resonance imaging data acquired in polysomnographically validated wakefulness, light sleep, and slow-wave sleep to examine the hierarchical structure of a low-frequency functional brain network, and to examine whether frontoparietal connectivity would disintegrate in sleep

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Summary

Introduction

These functionally comprehensive networks of regions are consistently observed throughout multiple time-series analyses, such as correlation against the timecourse of a particular seed region (Biswal et al, 1995; Fox et al, 2005; Fox and Raichle, 2007) or spatiotemporal independent component analysis (ICA; Beckmann et al, 2005; Damoiseaux et al, 2006) These networks are typically analyzed in so-called “resting-state fMRI” without subject’s engagement in a particular task, their neural circuitry matches fMRI-activations in specific sensory, motor, and cognitive tasks (Fox and Raichle, 2007). Horovitz et al (2008) found an increase in BOLD signal fluctuations in the visual and auditory cortices and the precuneus, while an increase of activity in the left precuneus and bilateral IPL has been observed in early sleep stage 1 (Picchioni et al, 2008) These results are largely in line with EEG studies, which reported increased neocortical connectivity

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