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Sleep deprivation leads to a loss of functional connectivity in frontal brain regions

BACKGROUND: The restorative effect of sleep on waking brain activity remains poorly understood. Previous studies have compared overall neural network characteristics after normal sleep and sleep deprivation. To study whether sleep and sleep deprivation might differentially affect subsequent connecti...

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Autores principales: Verweij, Ilse M, Romeijn, Nico, Smit, Dirk JA, Piantoni, Giovanni, Van Someren, Eus JW, van der Werf, Ysbrand D
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4108786/
https://www.ncbi.nlm.nih.gov/pubmed/25038817
http://dx.doi.org/10.1186/1471-2202-15-88
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author Verweij, Ilse M
Romeijn, Nico
Smit, Dirk JA
Piantoni, Giovanni
Van Someren, Eus JW
van der Werf, Ysbrand D
author_facet Verweij, Ilse M
Romeijn, Nico
Smit, Dirk JA
Piantoni, Giovanni
Van Someren, Eus JW
van der Werf, Ysbrand D
author_sort Verweij, Ilse M
collection PubMed
description BACKGROUND: The restorative effect of sleep on waking brain activity remains poorly understood. Previous studies have compared overall neural network characteristics after normal sleep and sleep deprivation. To study whether sleep and sleep deprivation might differentially affect subsequent connectivity characteristics in different brain regions, we performed a within-subject study of resting state brain activity using the graph theory framework adapted for the individual electrode level. In balanced order, we obtained high-density resting state electroencephalography (EEG) in 8 healthy participants, during a day following normal sleep and during a day following total sleep deprivation. We computed topographical maps of graph theoretical parameters describing local clustering and path length characteristics from functional connectivity matrices, based on synchronization likelihood, in five different frequency bands. A non-parametric permutation analysis with cluster correction for multiple comparisons was applied to assess significance of topographical changes in clustering coefficient and path length. RESULTS: Significant changes in graph theoretical parameters were only found on the scalp overlying the prefrontal cortex, where the clustering coefficient (local integration) decreased in the alpha frequency band and the path length (global integration) increased in the theta frequency band. These changes occurred regardless, and independent of, changes in power due to the sleep deprivation procedure. CONCLUSIONS: The findings indicate that sleep deprivation most strongly affects the functional connectivity of prefrontal cortical areas. The findings extend those of previous studies, which showed sleep deprivation to predominantly affect functions mediated by the prefrontal cortex, such as working memory. Together, these findings suggest that the restorative effect of sleep is especially relevant for the maintenance of functional connectivity of prefrontal brain regions.
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spelling pubmed-41087862014-07-25 Sleep deprivation leads to a loss of functional connectivity in frontal brain regions Verweij, Ilse M Romeijn, Nico Smit, Dirk JA Piantoni, Giovanni Van Someren, Eus JW van der Werf, Ysbrand D BMC Neurosci Research Article BACKGROUND: The restorative effect of sleep on waking brain activity remains poorly understood. Previous studies have compared overall neural network characteristics after normal sleep and sleep deprivation. To study whether sleep and sleep deprivation might differentially affect subsequent connectivity characteristics in different brain regions, we performed a within-subject study of resting state brain activity using the graph theory framework adapted for the individual electrode level. In balanced order, we obtained high-density resting state electroencephalography (EEG) in 8 healthy participants, during a day following normal sleep and during a day following total sleep deprivation. We computed topographical maps of graph theoretical parameters describing local clustering and path length characteristics from functional connectivity matrices, based on synchronization likelihood, in five different frequency bands. A non-parametric permutation analysis with cluster correction for multiple comparisons was applied to assess significance of topographical changes in clustering coefficient and path length. RESULTS: Significant changes in graph theoretical parameters were only found on the scalp overlying the prefrontal cortex, where the clustering coefficient (local integration) decreased in the alpha frequency band and the path length (global integration) increased in the theta frequency band. These changes occurred regardless, and independent of, changes in power due to the sleep deprivation procedure. CONCLUSIONS: The findings indicate that sleep deprivation most strongly affects the functional connectivity of prefrontal cortical areas. The findings extend those of previous studies, which showed sleep deprivation to predominantly affect functions mediated by the prefrontal cortex, such as working memory. Together, these findings suggest that the restorative effect of sleep is especially relevant for the maintenance of functional connectivity of prefrontal brain regions. BioMed Central 2014-07-19 /pmc/articles/PMC4108786/ /pubmed/25038817 http://dx.doi.org/10.1186/1471-2202-15-88 Text en © Verweij et al.; licensee BioMed Central Ltd. 2014 This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Verweij, Ilse M
Romeijn, Nico
Smit, Dirk JA
Piantoni, Giovanni
Van Someren, Eus JW
van der Werf, Ysbrand D
Sleep deprivation leads to a loss of functional connectivity in frontal brain regions
title Sleep deprivation leads to a loss of functional connectivity in frontal brain regions
title_full Sleep deprivation leads to a loss of functional connectivity in frontal brain regions
title_fullStr Sleep deprivation leads to a loss of functional connectivity in frontal brain regions
title_full_unstemmed Sleep deprivation leads to a loss of functional connectivity in frontal brain regions
title_short Sleep deprivation leads to a loss of functional connectivity in frontal brain regions
title_sort sleep deprivation leads to a loss of functional connectivity in frontal brain regions
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4108786/
https://www.ncbi.nlm.nih.gov/pubmed/25038817
http://dx.doi.org/10.1186/1471-2202-15-88
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