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Sleep cycle-dependent vascular dynamics in male mice and the predicted effects on perivascular cerebrospinal fluid flow and solute transport

Perivascular spaces are important highways for fluid and solute transport in the brain enabling efficient waste clearance during sleep. However, the underlying mechanisms augmenting perivascular flow in sleep are unknown. Using two-photon imaging of naturally sleeping male mice we demonstrate sleep...

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Autores principales: Bojarskaite, Laura, Vallet, Alexandra, Bjørnstad, Daniel M., Gullestad Binder, Kristin M., Cunen, Céline, Heuser, Kjell, Kuchta, Miroslav, Mardal, Kent-Andre, Enger, Rune
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9941497/
https://www.ncbi.nlm.nih.gov/pubmed/36806170
http://dx.doi.org/10.1038/s41467-023-36643-5
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author Bojarskaite, Laura
Vallet, Alexandra
Bjørnstad, Daniel M.
Gullestad Binder, Kristin M.
Cunen, Céline
Heuser, Kjell
Kuchta, Miroslav
Mardal, Kent-Andre
Enger, Rune
author_facet Bojarskaite, Laura
Vallet, Alexandra
Bjørnstad, Daniel M.
Gullestad Binder, Kristin M.
Cunen, Céline
Heuser, Kjell
Kuchta, Miroslav
Mardal, Kent-Andre
Enger, Rune
author_sort Bojarskaite, Laura
collection PubMed
description Perivascular spaces are important highways for fluid and solute transport in the brain enabling efficient waste clearance during sleep. However, the underlying mechanisms augmenting perivascular flow in sleep are unknown. Using two-photon imaging of naturally sleeping male mice we demonstrate sleep cycle-dependent vascular dynamics of pial arteries and penetrating arterioles: slow, large-amplitude oscillations in NREM sleep, a vasodilation in REM sleep, and a vasoconstriction upon awakening at the end of a sleep cycle and microarousals in NREM and intermediate sleep. These vascular dynamics are mirrored by changes in the size of the perivascular spaces of the penetrating arterioles: slow fluctuations in NREM sleep, reduction in REM sleep and an enlargement upon awakening after REM sleep and during microarousals in NREM and intermediate sleep. By biomechanical modeling we demonstrate that these sleep cycle-dependent perivascular dynamics likely enhance fluid flow and solute transport in perivascular spaces to levels comparable to cardiac pulsation-driven oscillations.
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spelling pubmed-99414972023-02-22 Sleep cycle-dependent vascular dynamics in male mice and the predicted effects on perivascular cerebrospinal fluid flow and solute transport Bojarskaite, Laura Vallet, Alexandra Bjørnstad, Daniel M. Gullestad Binder, Kristin M. Cunen, Céline Heuser, Kjell Kuchta, Miroslav Mardal, Kent-Andre Enger, Rune Nat Commun Article Perivascular spaces are important highways for fluid and solute transport in the brain enabling efficient waste clearance during sleep. However, the underlying mechanisms augmenting perivascular flow in sleep are unknown. Using two-photon imaging of naturally sleeping male mice we demonstrate sleep cycle-dependent vascular dynamics of pial arteries and penetrating arterioles: slow, large-amplitude oscillations in NREM sleep, a vasodilation in REM sleep, and a vasoconstriction upon awakening at the end of a sleep cycle and microarousals in NREM and intermediate sleep. These vascular dynamics are mirrored by changes in the size of the perivascular spaces of the penetrating arterioles: slow fluctuations in NREM sleep, reduction in REM sleep and an enlargement upon awakening after REM sleep and during microarousals in NREM and intermediate sleep. By biomechanical modeling we demonstrate that these sleep cycle-dependent perivascular dynamics likely enhance fluid flow and solute transport in perivascular spaces to levels comparable to cardiac pulsation-driven oscillations. Nature Publishing Group UK 2023-02-20 /pmc/articles/PMC9941497/ /pubmed/36806170 http://dx.doi.org/10.1038/s41467-023-36643-5 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Bojarskaite, Laura
Vallet, Alexandra
Bjørnstad, Daniel M.
Gullestad Binder, Kristin M.
Cunen, Céline
Heuser, Kjell
Kuchta, Miroslav
Mardal, Kent-Andre
Enger, Rune
Sleep cycle-dependent vascular dynamics in male mice and the predicted effects on perivascular cerebrospinal fluid flow and solute transport
title Sleep cycle-dependent vascular dynamics in male mice and the predicted effects on perivascular cerebrospinal fluid flow and solute transport
title_full Sleep cycle-dependent vascular dynamics in male mice and the predicted effects on perivascular cerebrospinal fluid flow and solute transport
title_fullStr Sleep cycle-dependent vascular dynamics in male mice and the predicted effects on perivascular cerebrospinal fluid flow and solute transport
title_full_unstemmed Sleep cycle-dependent vascular dynamics in male mice and the predicted effects on perivascular cerebrospinal fluid flow and solute transport
title_short Sleep cycle-dependent vascular dynamics in male mice and the predicted effects on perivascular cerebrospinal fluid flow and solute transport
title_sort sleep cycle-dependent vascular dynamics in male mice and the predicted effects on perivascular cerebrospinal fluid flow and solute transport
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9941497/
https://www.ncbi.nlm.nih.gov/pubmed/36806170
http://dx.doi.org/10.1038/s41467-023-36643-5
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