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      Waking experience modulates sleep need in mice

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          Abstract

          Background

          Homeostatic regulation of sleep is reflected in the maintenance of a daily balance between sleep and wakefulness. Although numerous internal and external factors can influence sleep, it is unclear whether and to what extent the process that keeps track of time spent awake is determined by the content of the waking experience. We hypothesised that alterations in environmental conditions may elicit different types of wakefulness, which will in turn influence both the capacity to sustain continuous wakefulness as well as the rates of accumulating sleep pressure. To address this, we compared the effects of repetitive behaviours such as voluntary wheel running or performing a simple touchscreen task, with wakefulness dominated by novel object exploration, on sleep timing and EEG slow-wave activity (SWA) during subsequent NREM sleep.

          Results

          We find that voluntary wheel running is associated with higher wake EEG theta-frequency activity and results in longer wake episodes, as compared with exploratory behaviour; yet, it does not lead to higher levels of EEG SWA during subsequent NREM sleep in either the frontal or occipital derivation. Furthermore, engagement in a touchscreen task, motivated by food reward, results in lower SWA during subsequent NREM sleep in both derivations, as compared to exploratory wakefulness, even though the total duration of wakefulness is similar.

          Conclusion

          Overall, our study suggests that sleep-wake behaviour is highly flexible within an individual and that the homeostatic processes that keep track of time spent awake are sensitive to the nature of the waking experience. We therefore conclude that sleep dynamics are determined, to a large degree, by the interaction between the organism and the environment.

          Supplementary Information

          The online version contains supplementary material available at 10.1186/s12915-021-00982-w.

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          Most cited references59

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          A two process model of sleep regulation.

          A Borbély (1982)
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            The sleep-deprived human brain

            How does sleep deprivation affect the human brain? Walker and colleagues review neuroimaging studies on the consequences of sleep deprivation on cognition and emotion — with specific focuses on attention and working memory, positive and negative emotion, and hippocampal learning — and the mechanisms underlying these effects.
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              Clues to the functions of mammalian sleep.

              The functions of mammalian sleep remain unclear. Most theories suggest a role for non-rapid eye movement (NREM) sleep in energy conservation and in nervous system recuperation. Theories of REM sleep have suggested a role for this state in periodic brain activation during sleep, in localized recuperative processes and in emotional regulation. Across mammals, the amount and nature of sleep are correlated with age, body size and ecological variables, such as whether the animals live in a terrestrial or an aquatic environment, their diet and the safety of their sleeping site. Sleep may be an efficient time for the completion of a number of functions, but variations in sleep expression indicate that these functions may differ across species.
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                Author and article information

                Contributors
                vladyslav.vyazovskiy@dpag.ox.ac.uk
                Journal
                BMC Biol
                BMC Biol
                BMC Biology
                BioMed Central (London )
                1741-7007
                6 April 2021
                6 April 2021
                2021
                : 19
                : 65
                Affiliations
                [1 ]GRID grid.4991.5, ISNI 0000 0004 1936 8948, Department of Physiology, Anatomy and Genetics, , University of Oxford/Sleep and Circadian Neuroscience Institute, ; Oxford, UK
                [2 ]GRID grid.4991.5, ISNI 0000 0004 1936 8948, Department of Experimental Psychology, , University of Oxford, ; Oxford, UK
                [3 ]GRID grid.4991.5, ISNI 0000 0004 1936 8948, Nuffield Department of Clinical Neurosciences, , University of Oxford, ; Oxford, UK
                Author information
                http://orcid.org/0000-0002-4336-6681
                Article
                982
                10.1186/s12915-021-00982-w
                8025572
                33823872
                17c6829b-d920-4c84-893d-a3f0aeb37127
                © The Author(s) 2021

                Open AccessThis 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 licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence 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 licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

                History
                : 30 July 2020
                : 14 February 2021
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100000265, Medical Research Council;
                Award ID: MR/L003635/1
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100000703, Action on Hearing Loss;
                Award ID: S52_Bajo
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100000268, Biotechnology and Biological Sciences Research Council;
                Award ID: BB/K011847/1
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100000780, European Commission;
                Award ID: PCIG11-GA-2012-322050
                Award Recipient :
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2021

                Life sciences
                mice,eeg,sleep homeostasis,behaviour,wakefulness,slow-wave activity,operant behaviour,running-wheel activity,exploratory behaviour

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