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      Oxygen consumption rate of flatworms under the influence of wake‐ and sleep‐promoting neurotransmitters

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          Abstract

          Flatworms are among the best studied animal models for regeneration; however, they also represent an emerging opportunity to investigate other biological processes as well. For instance, flatworms are nocturnal and sleep during the day, a state that is regulated by sleep/wake history and the action of the sleep‐promoting neurotransmitter gamma‐aminobutyric acid (or GABA). Sleep is widespread across the animal kingdom, where it serves many nonexclusive functions. Notably, sleep saves energy by reducing metabolic rate and by not doing something more energetically taxing. Whether the conservation of energy is apparent in sleeping flatworms is unclear. We measured the oxygen consumption rate (OCR) of flatworms dosed with either ( 1) GABA ( n = 29) which makes flatworms inactive or ( 2) dopamine ( n = 20) which stimulates flatworms to move, or ( 3) day and night neurotransmitter‐free controls ( n = 28 and 27, respectively). While OCR did not differ between the day and night, flatworms treated with GABA used less oxygen than those treated with dopamine, and less than the day‐time control. Thus, GABA affected flatworm physiology, ostensibly by enforcing energy‐conserving sleep. Evidence that dopamine increased metabolism was less strong. This work broadens our understanding of flatworm physiology and expands the phylogenetic applicability of energy conservation as a function of sleep.

          Abstract

          In the free‐living platyhelminth flatworm, Girardia tigrina, the sleep‐promoting neurotransmitter, gamma‐aminobutyric acid (or GABA), decreases oxygen consumption rate relative to the wake‐promoting neurotransmitter, dopamine, and also a neurotransmitter‐free control. This metabolic rate study builds on the behavioral and biochemical characterization of sleep in flatworms.

          Research Highlights

          While flatworms are known to sleep, it has been unclear whether restful flatworms reap the metabolic benefits of this quiescent state. Using neurotransmitters that regulate sleep and wakefulness, we show that sleep‐promoting gamma‐aminobutyric acid reduces oxygen consumption in flatworms.

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          Most cited references41

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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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            Sleep viewed as a state of adaptive inactivity.

            Sleep is often viewed as a vulnerable state that is incompatible with behaviours that nourish and propagate species. This has led to the hypothesis that sleep has survived because it fulfills some universal, but as yet unknown, vital function. I propose that sleep is best understood as a variant of dormant states seen throughout the plant and animal kingdoms and that it is itself highly adaptive because it optimizes the timing and duration of behaviour. Current evidence indicates that ecological variables are the main determinants of sleep duration and intensity across species.
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              Sleeping under the risk of predation

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                Author and article information

                Contributors
                shauni.omond@gmail.com
                j.lesku@latrobe.edu.au
                Journal
                J Exp Zool A Ecol Integr Physiol
                J Exp Zool A Ecol Integr Physiol
                10.1002/(ISSN)2471-5646
                JEZ
                Journal of Experimental Zoology. Part A, Ecological and Integrative Physiology
                John Wiley and Sons Inc. (Hoboken )
                2471-5638
                2471-5646
                27 May 2024
                December 2024
                : 341
                : 10 , Special Issue on Comparative Biology of Sleep & Circadian Rhythms ( doiID: 10.1002/jez.v341.10 )
                : 1130-1136
                Affiliations
                [ 1 ] School of Agriculture, Biomedicine and Environment La Trobe University Melbourne Australia
                [ 2 ]Present address: The Brigham and Women's Hospital, Harvard Medical School Boston USA
                Author notes
                [*] [* ] Correspondence Shauni E. T. Omond and John A. Lesku, School of Agriculture, Biomedicine and Environment, La Trobe University, Melbourne, Australia.

                Email: shauni.omond@ 123456gmail.com and j.lesku@ 123456latrobe.edu.au

                Author information
                http://orcid.org/0000-0002-7390-1403
                http://orcid.org/0000-0003-3664-8776
                http://orcid.org/0000-0003-1884-6306
                http://orcid.org/0000-0002-7604-3985
                http://orcid.org/0000-0001-5073-6954
                Article
                JEZ2828
                10.1002/jez.2828
                11579807
                38801005
                79564a43-e8f1-4c90-8db9-c5df7b993ac1
                © 2024 The Author(s). Journal of Experimental Zoology Part A: Ecological and Integrative Physiology published by Wiley Periodicals LLC.

                This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 09 May 2024
                : 21 April 2024
                : 09 May 2024
                Page count
                Figures: 4, Tables: 1, Pages: 7, Words: 4439
                Funding
                Funded by: Australian Research Council , doi 10.13039/501100000923;
                Categories
                Research Article
                Research Article
                Custom metadata
                2.0
                December 2024
                Converter:WILEY_ML3GV2_TO_JATSPMC version:6.5.1 mode:remove_FC converted:21.11.2024

                circadian,dopamine,dugesia,gaba,girardia,planarian,platyhelminthes
                circadian, dopamine, dugesia, gaba, girardia, planarian, platyhelminthes

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