Cognitive brain responses during circadian wake-promotion: evidence for sleep-pressure-dependent hypothalamic activations

Abstract The two-process model of sleep-wake regulation posits that sleep-wake-dependent homeostatic processes interact with the circadian timing system to affect human behavior. The circadian timing system is fundamental to maintaining stable cognitive performance, as it counteracts growing homeost...

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Main Authors: Carolin F. Reichert, Micheline Maire, Virginie Gabel, Antoine U. Viola, Thomas Götz, Klaus Scheffler, Markus Klarhöfer, Christian Berthomier, Werner Strobel, Christophe Phillips, Eric Salmon, Christian Cajochen, Christina Schmidt
Format: Article
Language:English
Published: Nature Publishing Group 2017-07-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-017-05695-1
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spelling doaj-4e9e94685be94459975422e0b82515622020-12-08T00:29:48ZengNature Publishing GroupScientific Reports2045-23222017-07-01711910.1038/s41598-017-05695-1Cognitive brain responses during circadian wake-promotion: evidence for sleep-pressure-dependent hypothalamic activationsCarolin F. Reichert0Micheline Maire1Virginie Gabel2Antoine U. Viola3Thomas Götz4Klaus Scheffler5Markus Klarhöfer6Christian Berthomier7Werner Strobel8Christophe Phillips9Eric Salmon10Christian Cajochen11Christina Schmidt12Centre for Chronobiology, Psychiatric Hospital of the University of BaselCentre for Chronobiology, Psychiatric Hospital of the University of BaselCentre for Chronobiology, Psychiatric Hospital of the University of BaselCentre for Chronobiology, Psychiatric Hospital of the University of BaselDepartment of Psychiatry, Public Health OfficeMax-Planck Institute for Biological CyberneticsDepartment of Medical Radiology, MR-Physics, University of BaselPHYSIPRespiratory Medicine, Department of Internal Medicine, University Hospital BaselGIGA-CRC, In Vivo Imaging Unit, University of LiègeGIGA-CRC, In Vivo Imaging Unit, University of LiègeCentre for Chronobiology, Psychiatric Hospital of the University of BaselCentre for Chronobiology, Psychiatric Hospital of the University of BaselAbstract The two-process model of sleep-wake regulation posits that sleep-wake-dependent homeostatic processes interact with the circadian timing system to affect human behavior. The circadian timing system is fundamental to maintaining stable cognitive performance, as it counteracts growing homeostatic sleep pressure during daytime. Using magnetic resonance imaging, we explored brain responses underlying working memory performance during the time of maximal circadian wake-promotion under varying sleep pressure conditions. Circadian wake-promoting strength was derived from the ability to sleep during an evening nap. Hypothalamic BOLD activity was positively linked to circadian wake-promoting strength under normal, but not under disproportionally high or low sleep pressure levels. Furthermore, higher hypothalamic activity under normal sleep pressure levels predicted better performance under sleep loss. Our results reappraise the two-process model by revealing a homeostatic-dose-dependent association between circadian wake-promotion and cognition-related hypothalamic activity.https://doi.org/10.1038/s41598-017-05695-1
collection DOAJ
language English
format Article
sources DOAJ
author Carolin F. Reichert
Micheline Maire
Virginie Gabel
Antoine U. Viola
Thomas Götz
Klaus Scheffler
Markus Klarhöfer
Christian Berthomier
Werner Strobel
Christophe Phillips
Eric Salmon
Christian Cajochen
Christina Schmidt
spellingShingle Carolin F. Reichert
Micheline Maire
Virginie Gabel
Antoine U. Viola
Thomas Götz
Klaus Scheffler
Markus Klarhöfer
Christian Berthomier
Werner Strobel
Christophe Phillips
Eric Salmon
Christian Cajochen
Christina Schmidt
Cognitive brain responses during circadian wake-promotion: evidence for sleep-pressure-dependent hypothalamic activations
Scientific Reports
author_facet Carolin F. Reichert
Micheline Maire
Virginie Gabel
Antoine U. Viola
Thomas Götz
Klaus Scheffler
Markus Klarhöfer
Christian Berthomier
Werner Strobel
Christophe Phillips
Eric Salmon
Christian Cajochen
Christina Schmidt
author_sort Carolin F. Reichert
title Cognitive brain responses during circadian wake-promotion: evidence for sleep-pressure-dependent hypothalamic activations
title_short Cognitive brain responses during circadian wake-promotion: evidence for sleep-pressure-dependent hypothalamic activations
title_full Cognitive brain responses during circadian wake-promotion: evidence for sleep-pressure-dependent hypothalamic activations
title_fullStr Cognitive brain responses during circadian wake-promotion: evidence for sleep-pressure-dependent hypothalamic activations
title_full_unstemmed Cognitive brain responses during circadian wake-promotion: evidence for sleep-pressure-dependent hypothalamic activations
title_sort cognitive brain responses during circadian wake-promotion: evidence for sleep-pressure-dependent hypothalamic activations
publisher Nature Publishing Group
series Scientific Reports
issn 2045-2322
publishDate 2017-07-01
description Abstract The two-process model of sleep-wake regulation posits that sleep-wake-dependent homeostatic processes interact with the circadian timing system to affect human behavior. The circadian timing system is fundamental to maintaining stable cognitive performance, as it counteracts growing homeostatic sleep pressure during daytime. Using magnetic resonance imaging, we explored brain responses underlying working memory performance during the time of maximal circadian wake-promotion under varying sleep pressure conditions. Circadian wake-promoting strength was derived from the ability to sleep during an evening nap. Hypothalamic BOLD activity was positively linked to circadian wake-promoting strength under normal, but not under disproportionally high or low sleep pressure levels. Furthermore, higher hypothalamic activity under normal sleep pressure levels predicted better performance under sleep loss. Our results reappraise the two-process model by revealing a homeostatic-dose-dependent association between circadian wake-promotion and cognition-related hypothalamic activity.
url https://doi.org/10.1038/s41598-017-05695-1
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