Abstract

Sleep has beneficial effects on brain function and learning, which are reflected in plastic changes in the cortex. Early childhood is a time of rapid maturation in fundamental skills—e.g., language, cognitive control, working memory—that are predictive of future functioning. Little is currently known about the interactions between sleep and brain maturation during this developmental period. We propose coherent electroencephalogram (EEG) activity during sleep may provide unique insight into maturational processes of functional brain connectivity. Longitudinal sleep EEG assessments were performed in eight healthy subjects at ages 2, 3 and 5 years. Sleep EEG coherence increased across development in a region- and frequency-specific manner. Moreover, although connectivity primarily decreased intra-hemispherically across a night of sleep, an inter-hemispheric overnight increase occurred in the frequency range of slow waves (0.8–2 Hz), theta (4.8–7.8 Hz) and sleep spindles (10–14 Hz), with connectivity changes of up to 20% across a night of sleep. These findings indicate sleep EEG coherence reflects processes of brain maturation—i.e., programmed unfolding of neuronal networks—and moreover, sleep-related alterations of brain connectivity during the sensitive maturational window of early childhood.

Highlights

  • Across childhood and adolescence the brain undergoes massive morphological changes such as cortical refinement, synapse growth, pruning, and white matter myelination [1,2]

  • Major connectivity growth is assumed to contribute to neuronal network maturation, resulting in refinement of brain functions and behavioral skills

  • Connectivity was assessed with sleep EEG coherence, which provides insight into temporal synchrony of distinct brain regions during sleep [3] and allows for the tracking of subtle dynamical changes of functional brain connectivity across development

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Summary

Introduction

Across childhood and adolescence the brain undergoes massive morphological changes such as cortical refinement, synapse growth, pruning, and white matter myelination [1,2]. Major connectivity growth is assumed to contribute to neuronal network maturation, resulting in refinement of brain functions and behavioral skills. The well-established EEG marker of deep sleep, slow-wave activity (SWA, EEG power in the 1–4.5 Hz frequency range), undergoes maturation in parallel with cortical morphology [7,8] and might be interdependent with structural changes [9]. Connectivity was assessed with sleep EEG coherence, which provides insight into temporal synchrony of distinct brain regions during sleep [3] and allows for the tracking of subtle dynamical changes of functional brain connectivity across development. We tested the hypothesis that sleep EEG coherence changes across a night of sleep in early childhood

Results and Discussion
Connectivity Changes across Development
Connectivity Changes across the Night
Sleep EEG Coherence and Neuronal Networks
Regional Variation in Coherence
Neuronal Network Refinement
Experimental Section
Conclusions
Full Text
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