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Research Articles, Behavioral/Cognitive

Total Sleep Deprivation Increases Brain Age Prediction Reversibly in Multisite Samples of Young Healthy Adults

Congying Chu, Sebastian C. Holst, Eva-Maria Elmenhorst, Anna L. Foerges, Changhong Li, Denise Lange, Eva Hennecke, Diego M. Baur, Simone Beer, Felix Hoffstaedter, Gitte M. Knudsen, Daniel Aeschbach, Andreas Bauer, Hans-Peter Landolt and David Elmenhorst
Journal of Neuroscience 22 March 2023, 43 (12) 2168-2177; DOI: https://doi.org/10.1523/JNEUROSCI.0790-22.2023
Congying Chu
1Institute of Neuroscience and Medicine (INM-2), Forschungszentrum Jülich, 52428 Jülich, Germany
8State Key Laboratory of Cognitive Neuroscience and Learning, Beijing Normal University, Beijing 100875, China
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Sebastian C. Holst
2Neurobiology Research Unit, Copenhagen University Hospital Rigshospitalet, 2100 Copenhagen, Denmark
3Institute of Pharmacology and Toxicology, University of Zurich, CH-8006 Zurich, Switzerland
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Eva-Maria Elmenhorst
4Department of Sleep and Human Factors Research, Institute of Aerospace Medicine, German Aerospace Center, 51147 Cologne, Germany
15Institute for Occupational, Social and Environmental Medicine, Medical Faculty, RWTH Aachen University, 52074 Aachen, Germany
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Anna L. Foerges
1Institute of Neuroscience and Medicine (INM-2), Forschungszentrum Jülich, 52428 Jülich, Germany
12Department of Neurophysiology, Institute of Zoology (Bio-II), RWTH Aachen University, 52074 Aachen, Germany
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Changhong Li
1Institute of Neuroscience and Medicine (INM-2), Forschungszentrum Jülich, 52428 Jülich, Germany
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Denise Lange
4Department of Sleep and Human Factors Research, Institute of Aerospace Medicine, German Aerospace Center, 51147 Cologne, Germany
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Eva Hennecke
4Department of Sleep and Human Factors Research, Institute of Aerospace Medicine, German Aerospace Center, 51147 Cologne, Germany
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Diego M. Baur
3Institute of Pharmacology and Toxicology, University of Zurich, CH-8006 Zurich, Switzerland
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Simone Beer
1Institute of Neuroscience and Medicine (INM-2), Forschungszentrum Jülich, 52428 Jülich, Germany
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Felix Hoffstaedter
5Institute of Systems Neuroscience, Medical Faculty, Heinrich Heine University Düsseldorf, 40225 Düsseldorf, Germany
6Institute of Neuroscience and Medicine, Brain and Behaviour (INM-7), Forschungszentrum Jülich, 52428 Jülich, Germany
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Gitte M. Knudsen
2Neurobiology Research Unit, Copenhagen University Hospital Rigshospitalet, 2100 Copenhagen, Denmark
16Institute of Clinical Medicine, University of Copenhagen, 2200 Copenhagen, Denmark
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Daniel Aeschbach
4Department of Sleep and Human Factors Research, Institute of Aerospace Medicine, German Aerospace Center, 51147 Cologne, Germany
9Division of Sleep and Circadian Disorders, Brigham and Women's Hospital, Boston, Massachusetts 02115
10Division of Sleep Medicine, Harvard Medical School, Boston, Massachusetts 02115
17Institute of Experimental Epileptology and Cognition Research, Faculty of Medicine, University of Bonn, 53127, Bonn, Germany
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Andreas Bauer
1Institute of Neuroscience and Medicine (INM-2), Forschungszentrum Jülich, 52428 Jülich, Germany
7Neurological Department, Medical Faculty, Heinrich-Heine-University, 40225 Düsseldorf, Germany
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Hans-Peter Landolt
3Institute of Pharmacology and Toxicology, University of Zurich, CH-8006 Zurich, Switzerland
11Sleep & Health Zurich, University Center of Competence, University of Zurich, Zurich, Switzerland
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David Elmenhorst
1Institute of Neuroscience and Medicine (INM-2), Forschungszentrum Jülich, 52428 Jülich, Germany
13Department of Nuclear Medicine, Faculty of Medicine, University Hospital Cologne, University of Cologne, 50937 Cologne, Germany
14Division of Medical Psychology, Rheinische Friedrich-Wilhelms-University Bonn, Bonn, 53127 Germany
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Abstract

Sleep loss pervasively affects the human brain at multiple levels. Age-related changes in several sleep characteristics indicate that reduced sleep quality is a frequent characteristic of aging. Conversely, sleep disruption may accelerate the aging process, yet it is not known what will happen to the age status of the brain if we can manipulate sleep conditions. To tackle this question, we used an approach of brain age to investigate whether sleep loss would cause age-related changes in the brain. We included MRI data of 134 healthy volunteers (mean chronological age of 25.3 between the age of 19 and 39 years, 42 females/92 males) from five datasets with different sleep conditions. Across three datasets with the condition of total sleep deprivation (>24 h of prolonged wakefulness), we consistently observed that total sleep deprivation increased brain age by 1–2 years regarding the group mean difference with the baseline. Interestingly, after one night of recovery sleep, brain age was not different from baseline. We also demonstrated the associations between the change in brain age after total sleep deprivation and the sleep variables measured during the recovery night. By contrast, brain age was not significantly changed by either acute (3 h time-in-bed for one night) or chronic partial sleep restriction (5 h time-in-bed for five continuous nights). Together, the convergent findings indicate that acute total sleep loss changes brain morphology in an aging-like direction in young participants and that these changes are reversible by recovery sleep.

SIGNIFICANCE STATEMENT Sleep is fundamental for humans to maintain normal physical and psychological functions. Experimental sleep deprivation is a variable-controlling approach to engaging the brain among different sleep conditions for investigating the responses of the brain to sleep loss. Here, we quantified the response of the brain to sleep deprivation by using the change of brain age predictable with brain morphologic features. In three independent datasets, we consistently found increased brain age after total sleep deprivation, which was associated with the change in sleep variables. Moreover, no significant change in brain age was found after partial sleep deprivation in another two datasets. Our study provides new evidence to explain the brainwide effect of sleep loss in an aging-like direction.

  • brain age
  • sleep deprivation
  • T1 MRI

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The Journal of Neuroscience: 43 (12)
Journal of Neuroscience
Vol. 43, Issue 12
22 Mar 2023
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Total Sleep Deprivation Increases Brain Age Prediction Reversibly in Multisite Samples of Young Healthy Adults
Congying Chu, Sebastian C. Holst, Eva-Maria Elmenhorst, Anna L. Foerges, Changhong Li, Denise Lange, Eva Hennecke, Diego M. Baur, Simone Beer, Felix Hoffstaedter, Gitte M. Knudsen, Daniel Aeschbach, Andreas Bauer, Hans-Peter Landolt, David Elmenhorst
Journal of Neuroscience 22 March 2023, 43 (12) 2168-2177; DOI: 10.1523/JNEUROSCI.0790-22.2023

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Total Sleep Deprivation Increases Brain Age Prediction Reversibly in Multisite Samples of Young Healthy Adults
Congying Chu, Sebastian C. Holst, Eva-Maria Elmenhorst, Anna L. Foerges, Changhong Li, Denise Lange, Eva Hennecke, Diego M. Baur, Simone Beer, Felix Hoffstaedter, Gitte M. Knudsen, Daniel Aeschbach, Andreas Bauer, Hans-Peter Landolt, David Elmenhorst
Journal of Neuroscience 22 March 2023, 43 (12) 2168-2177; DOI: 10.1523/JNEUROSCI.0790-22.2023
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Keywords

  • brain age
  • sleep deprivation
  • T1 MRI

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