An altered balance of integrated and segregated brain activity is a marker of cognitive deficits following sleep deprivation

Sleep deprivation (SD) leads to impairments in cognitive function. Here, we tested the hypothesis that cognitive changes in the sleep-deprived brain can be explained by information processing within and between large-scale cortical networks. We acquired functional magnetic resonance imaging (fMRI) s...

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Autores principales:	Nathan E. Cross, Florence B. Pomares, Alex Nguyen, Aurore A. Perrault, Aude Jegou, Makoto Uji, Kangjoo Lee, Fatemeh Razavipour, Obaï Bin Ka’b Ali, Umit Aydin, Habib Benali, Christophe Grova, Thien Thanh Dang-Vu
Formato:	article
Lenguaje:	EN
Publicado:	Public Library of Science (PLoS) 2021
Materias:	Biology (General) QH301-705.5
Acceso en línea:	https://doaj.org/article/c3e289d074804da89090e1740075bb4d
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spelling	oai:doaj.org-article:c3e289d074804da89090e1740075bb4d2021-11-11T05:36:24ZAn altered balance of integrated and segregated brain activity is a marker of cognitive deficits following sleep deprivation1544-91731545-7885https://doaj.org/article/c3e289d074804da89090e1740075bb4d2021-11-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC8568176/?tool=EBIhttps://doaj.org/toc/1544-9173https://doaj.org/toc/1545-7885Sleep deprivation (SD) leads to impairments in cognitive function. Here, we tested the hypothesis that cognitive changes in the sleep-deprived brain can be explained by information processing within and between large-scale cortical networks. We acquired functional magnetic resonance imaging (fMRI) scans of 20 healthy volunteers during attention and executive tasks following a regular night of sleep, a night of SD, and a recovery nap containing nonrapid eye movement (NREM) sleep. Overall, SD was associated with increased cortex-wide functional integration, driven by a rise of integration within cortical networks. The ratio of within versus between network integration in the cortex increased further in the recovery nap, suggesting that prolonged wakefulness drives the cortex towards a state resembling sleep. This balance of integration and segregation in the sleep-deprived state was tightly associated with deficits in cognitive performance. This was a distinct and better marker of cognitive impairment than conventional indicators of homeostatic sleep pressure, as well as the pronounced thalamocortical connectivity changes that occurs towards falling asleep. Importantly, restoration of the balance between segregation and integration of cortical activity was also related to performance recovery after the nap, demonstrating a bidirectional effect. These results demonstrate that intra- and interindividual differences in cortical network integration and segregation during task performance may play a critical role in vulnerability to cognitive impairment in the sleep-deprived state. Can the cognitive changes that result from sleep deprivation be explained by information processing within and between large-scale networks in the brain? This study shows that the ratio of within- vs between-network integration is tightly associated with deficits in cognitive performance.Nathan E. CrossFlorence B. PomaresAlex NguyenAurore A. PerraultAude JegouMakoto UjiKangjoo LeeFatemeh RazavipourObaï Bin Ka’b AliUmit AydinHabib BenaliChristophe GrovaThien Thanh Dang-VuPublic Library of Science (PLoS)articleBiology (General)QH301-705.5ENPLoS Biology, Vol 19, Iss 11 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Biology (General) QH301-705.5
spellingShingle	Biology (General) QH301-705.5 Nathan E. Cross Florence B. Pomares Alex Nguyen Aurore A. Perrault Aude Jegou Makoto Uji Kangjoo Lee Fatemeh Razavipour Obaï Bin Ka’b Ali Umit Aydin Habib Benali Christophe Grova Thien Thanh Dang-Vu An altered balance of integrated and segregated brain activity is a marker of cognitive deficits following sleep deprivation
description	Sleep deprivation (SD) leads to impairments in cognitive function. Here, we tested the hypothesis that cognitive changes in the sleep-deprived brain can be explained by information processing within and between large-scale cortical networks. We acquired functional magnetic resonance imaging (fMRI) scans of 20 healthy volunteers during attention and executive tasks following a regular night of sleep, a night of SD, and a recovery nap containing nonrapid eye movement (NREM) sleep. Overall, SD was associated with increased cortex-wide functional integration, driven by a rise of integration within cortical networks. The ratio of within versus between network integration in the cortex increased further in the recovery nap, suggesting that prolonged wakefulness drives the cortex towards a state resembling sleep. This balance of integration and segregation in the sleep-deprived state was tightly associated with deficits in cognitive performance. This was a distinct and better marker of cognitive impairment than conventional indicators of homeostatic sleep pressure, as well as the pronounced thalamocortical connectivity changes that occurs towards falling asleep. Importantly, restoration of the balance between segregation and integration of cortical activity was also related to performance recovery after the nap, demonstrating a bidirectional effect. These results demonstrate that intra- and interindividual differences in cortical network integration and segregation during task performance may play a critical role in vulnerability to cognitive impairment in the sleep-deprived state. Can the cognitive changes that result from sleep deprivation be explained by information processing within and between large-scale networks in the brain? This study shows that the ratio of within- vs between-network integration is tightly associated with deficits in cognitive performance.
format	article
author	Nathan E. Cross Florence B. Pomares Alex Nguyen Aurore A. Perrault Aude Jegou Makoto Uji Kangjoo Lee Fatemeh Razavipour Obaï Bin Ka’b Ali Umit Aydin Habib Benali Christophe Grova Thien Thanh Dang-Vu
author_facet	Nathan E. Cross Florence B. Pomares Alex Nguyen Aurore A. Perrault Aude Jegou Makoto Uji Kangjoo Lee Fatemeh Razavipour Obaï Bin Ka’b Ali Umit Aydin Habib Benali Christophe Grova Thien Thanh Dang-Vu
author_sort	Nathan E. Cross
title	An altered balance of integrated and segregated brain activity is a marker of cognitive deficits following sleep deprivation
title_short	An altered balance of integrated and segregated brain activity is a marker of cognitive deficits following sleep deprivation
title_full	An altered balance of integrated and segregated brain activity is a marker of cognitive deficits following sleep deprivation
title_fullStr	An altered balance of integrated and segregated brain activity is a marker of cognitive deficits following sleep deprivation
title_full_unstemmed	An altered balance of integrated and segregated brain activity is a marker of cognitive deficits following sleep deprivation
title_sort	altered balance of integrated and segregated brain activity is a marker of cognitive deficits following sleep deprivation
publisher	Public Library of Science (PLoS)
publishDate	2021
url	https://doaj.org/article/c3e289d074804da89090e1740075bb4d
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An altered balance of integrated and segregated brain activity is a marker of cognitive deficits following sleep deprivation

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