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Association between sleep slow-wave activity and in-vivo estimates of myelin in healthy young men

Association between sleep slow-wave activity and in-vivo estimates of myelin in healthy young men
Association between sleep slow-wave activity and in-vivo estimates of myelin in healthy young men

Sleep has been suggested to contribute to myelinogenesis and associated structural changes in the brain. As a principal hallmark of sleep, slow-wave activity (SWA) is homeostatically regulated but also differs between individuals. Besides its homeostatic function, SWA topography is suggested to reflect processes of brain maturation. Here, we assessed whether interindividual differences in sleep SWA and its homeostatic response to sleep manipulations are associated with in-vivo myelin estimates in a sample of healthy young men. Two hundred twenty-six participants (18–31 y.) underwent an in-lab protocol in which SWA was assessed at baseline (BAS), after sleep deprivation (high homeostatic sleep pressure, HSP) and after sleep saturation (low homeostatic sleep pressure, LSP). Early-night frontal SWA, the frontal-occipital SWA ratio, as well as the overnight exponential SWA decay were computed over sleep conditions. Semi-quantitative magnetization transfer saturation maps (MTsat), providing markers for myelin content, were acquired during a separate laboratory visit. Early-night frontal SWA was negatively associated with regional myelin estimates in the temporal portion of the inferior longitudinal fasciculus. By contrast, neither the responsiveness of SWA to sleep saturation or deprivation, its overnight dynamics, nor the frontal/occipital SWA ratio were associated with brain structural indices. Our results indicate that frontal SWA generation tracks inter-individual differences in continued structural brain re-organization during early adulthood. This stage of life is not only characterized by ongoing region-specific changes in myelin content, but also by a sharp decrease and a shift towards frontal predominance in SWA generation.

myelin markers, sleep homeostasis, sleep slow-wave activity, semi-quantitative MRI
1053-8119
Deantoni, Michele
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Baillet, Marion
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Hammad, Gregory
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Berthomier, Christian
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Reyt, Mathilde
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Jaspar, Mathieu
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Meyer, Christelle
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Egroo, Maxime Van
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Talwar, Puneet
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Lambot, Eric
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Chellappa, Sarah L.
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Degueldre, Christian
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Luxen, André
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Salmon, Eric
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Balteau, Evelyne
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Phillips, Christophe
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Dijk, Derk-Jan
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Vandewalle, Gilles
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Collette, Fabienne
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Maquet, Pierre
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Muto, Vincenzo
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Schmidt, Christina
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Deantoni, Michele
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Baillet, Marion
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Hammad, Gregory
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Berthomier, Christian
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Reyt, Mathilde
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Jaspar, Mathieu
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Meyer, Christelle
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Egroo, Maxime Van
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Talwar, Puneet
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Lambot, Eric
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Chellappa, Sarah L.
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Degueldre, Christian
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Luxen, André
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Salmon, Eric
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Balteau, Evelyne
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Phillips, Christophe
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Dijk, Derk-Jan
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Vandewalle, Gilles
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Collette, Fabienne
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Maquet, Pierre
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Muto, Vincenzo
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Schmidt, Christina
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Deantoni, Michele, Baillet, Marion, Hammad, Gregory, Berthomier, Christian, Reyt, Mathilde, Jaspar, Mathieu, Meyer, Christelle, Egroo, Maxime Van, Talwar, Puneet, Lambot, Eric, Chellappa, Sarah L., Degueldre, Christian, Luxen, André, Salmon, Eric, Balteau, Evelyne, Phillips, Christophe, Dijk, Derk-Jan, Vandewalle, Gilles, Collette, Fabienne, Maquet, Pierre, Muto, Vincenzo and Schmidt, Christina (2023) Association between sleep slow-wave activity and in-vivo estimates of myelin in healthy young men. NeuroImage, 272, [120045]. (doi:10.1016/j.neuroimage.2023.120045).

Record type: Article

Abstract

Sleep has been suggested to contribute to myelinogenesis and associated structural changes in the brain. As a principal hallmark of sleep, slow-wave activity (SWA) is homeostatically regulated but also differs between individuals. Besides its homeostatic function, SWA topography is suggested to reflect processes of brain maturation. Here, we assessed whether interindividual differences in sleep SWA and its homeostatic response to sleep manipulations are associated with in-vivo myelin estimates in a sample of healthy young men. Two hundred twenty-six participants (18–31 y.) underwent an in-lab protocol in which SWA was assessed at baseline (BAS), after sleep deprivation (high homeostatic sleep pressure, HSP) and after sleep saturation (low homeostatic sleep pressure, LSP). Early-night frontal SWA, the frontal-occipital SWA ratio, as well as the overnight exponential SWA decay were computed over sleep conditions. Semi-quantitative magnetization transfer saturation maps (MTsat), providing markers for myelin content, were acquired during a separate laboratory visit. Early-night frontal SWA was negatively associated with regional myelin estimates in the temporal portion of the inferior longitudinal fasciculus. By contrast, neither the responsiveness of SWA to sleep saturation or deprivation, its overnight dynamics, nor the frontal/occipital SWA ratio were associated with brain structural indices. Our results indicate that frontal SWA generation tracks inter-individual differences in continued structural brain re-organization during early adulthood. This stage of life is not only characterized by ongoing region-specific changes in myelin content, but also by a sharp decrease and a shift towards frontal predominance in SWA generation.

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Accepted/In Press date: 17 March 2023
e-pub ahead of print date: 29 March 2023
Published date: 6 April 2023
Additional Information: Funding Information: M.D., M.B., C.S., F.C., C.P., and G.V. are supported by the Fonds National de la Recherche Scientifique-FNRS-Belgium (F.R.S.-FNRS) . M.B., M.R., G.H. and V.M. are supported by the European Research Council (COGNAP-GA-757763). D.J.D. is supported by the UK Dementia Research Institute (DRI). S.L.C. is supported by the Alexander Von Humboldt Foundation. M.V.E. is supported by BrightFocus Foundation (A20211016F). The study was supported by the Wallonia-Brussels Federation (Actions de Recherche Concertées-ARC-09/14-03) , WELBIO/Walloon Excellence in Life Sciences and Biotechnology Grant ( WELBIO-CR-2010-06E ), FNRS-Belgium ( F.R.S-FNRS - F.4513.17 & T.0242.19 & 3.4516.11 ), Fondation Recherche Alzheimer ( SAO-FRA 2019/0025 ), University of Liège (ULiège), Fondation Simone et Pierre Clerdent, European Regional Development Fund (Radiomed project), Fonds Léon Fredericq . D.J.D. is supported by the UK Dementia Research Institute (DRI) . S.L.C. is supported by the Alexander Von Humboldt Foundation . M.B., M.R., G.H. and V.M. are supported by the European Research Council ( COGNAP-GA-757763 ). M.V.E. is supported by BrightFocus Foundation ( A20211016F). DJDC. is supported by the Alexander Von Humboldt Foundation. M.R., G.H. and V.M. are supported by the European Research Council (COGNAP-GA-757763). M.V.E. is supported by BrightFocus Foundation (A20211016F).
Keywords: myelin markers, sleep homeostasis, sleep slow-wave activity, semi-quantitative MRI

Identifiers

Local EPrints ID: 480054
URI: http://eprints.soton.ac.uk/id/eprint/480054
ISSN: 1053-8119
PURE UUID: ec581375-15c0-447d-b24b-6b6fb859fd3a
ORCID for Sarah L. Chellappa: ORCID iD orcid.org/0000-0002-6190-464X

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Date deposited: 01 Aug 2023 16:40
Last modified: 17 Mar 2024 04:21

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Contributors

Author: Michele Deantoni
Author: Marion Baillet
Author: Gregory Hammad
Author: Christian Berthomier
Author: Mathilde Reyt
Author: Mathieu Jaspar
Author: Christelle Meyer
Author: Maxime Van Egroo
Author: Puneet Talwar
Author: Eric Lambot
Author: Sarah L. Chellappa ORCID iD
Author: Christian Degueldre
Author: André Luxen
Author: Eric Salmon
Author: Evelyne Balteau
Author: Christophe Phillips
Author: Derk-Jan Dijk
Author: Gilles Vandewalle
Author: Fabienne Collette
Author: Pierre Maquet
Author: Vincenzo Muto
Author: Christina Schmidt

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