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      The bear circadian clock doesn’t ‘sleep’ during winter dormancy

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          Abstract

          Background

          Most biological functions are synchronized to the environmental light:dark cycle via a circadian timekeeping system. Bears exhibit shallow torpor combined with metabolic suppression during winter dormancy. We sought to confirm that free-running circadian rhythms of body temperature (Tb) and activity were expressed in torpid grizzly (brown) bears and that they were functionally responsive to environmental light. We also measured activity and ambient light exposures in denning wild bears to determine if rhythms were evident and what the photic conditions of their natural dens were. Lastly, we used cultured skin fibroblasts obtained from captive torpid bears to assess molecular clock operation in peripheral tissues. Circadian parameters were estimated using robust wavelet transforms and maximum entropy spectral analyses.

          Results

          Captive grizzly bears housed in constant darkness during winter dormancy expressed circadian rhythms of activity and Tb. The rhythm period of juvenile bears was significantly shorter than that of adult bears. However, the period of activity rhythms in adult captive bears was virtually identical to that of adult wild denning bears as was the strength of the activity rhythms. Similar to what has been found in other mammals, a single light exposure during the bear’s active period delayed subsequent activity onsets whereas these were advanced when light was applied during the bear’s inactive period. Lastly, in vitro studies confirmed the expression of molecular circadian rhythms with a period comparable to the bear’s own behavioral rhythms.

          Conclusions

          Based on these findings we conclude that the circadian system is functional in torpid bears and their peripheral tissues even when housed in constant darkness, is responsive to phase-shifting effects of light, and therefore, is a normal facet of torpid bear physiology.

          Electronic supplementary material

          The online version of this article (doi:10.1186/s12983-016-0173-x) contains supplementary material, which is available to authorized users.

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          Most cited references56

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          The meter of metabolism.

          The circadian system orchestrates the temporal organization of many aspects of physiology, including metabolism, in synchrony with the 24 hr rotation of the Earth. Like the metabolic system, the circadian system is a complex feedback network that involves interactions between the central nervous system and peripheral tissues. Emerging evidence suggests that circadian regulation is intimately linked to metabolic homeostasis and that dysregulation of circadian rhythms can contribute to disease. Conversely, metabolic signals also feed back into the circadian system, modulating circadian gene expression and behavior. Here, we review the relationship between the circadian and metabolic systems and the implications for cardiovascular disease, obesity, and diabetes.
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            Hibernation in black bears: independence of metabolic suppression from body temperature.

            Black bears hibernate for 5 to 7 months a year and, during this time, do not eat, drink, urinate, or defecate. We measured metabolic rate and body temperature in hibernating black bears and found that they suppress metabolism to 25% of basal rates while regulating body temperature from 30° to 36°C, in multiday cycles. Heart rates were reduced from 55 to as few as 9 beats per minute, with profound sinus arrhythmia. After returning to normal body temperature and emerging from dens, bears maintained a reduced metabolic rate for up to 3 weeks. The pronounced reduction and delayed recovery of metabolic rate in hibernating bears suggest that the majority of metabolic suppression during hibernation is independent of lowered body temperature.
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              Circadian rhythms and metabolic syndrome: from experimental genetics to human disease.

              The incidence of the metabolic syndrome represents a spectrum of disorders that continue to increase across the industrialized world. Both genetic and environmental factors contribute to metabolic syndrome and recent evidence has emerged to suggest that alterations in circadian systems and sleep participate in the pathogenesis of the disease. In this review, we highlight studies at the intersection of clinical medicine and experimental genetics that pinpoint how perturbations of the internal clock system, and sleep, constitute risk factors for disorders including obesity, diabetes mellitus, cardiovascular disease, thrombosis and even inflammation. An exciting aspect of the field has been the integration of behavioral and physiological approaches, and the emerging insight into both neural and peripheral tissues in disease pathogenesis. Consideration of the cell and molecular links between disorders of circadian rhythms and sleep with metabolic syndrome has begun to open new opportunities for mechanism-based therapeutics.
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                Author and article information

                Contributors
                heiko@vetmed.wsu.edu
                tleise@amherst.edu
                gstenhouse@foothillsri.ca
                karine.pigeon@gmail.com
                wayne_kasworm@fws.gov
                justin_teisberg@fws.gov
                thomas_radandt@fws.gov
                r.dallmann@warwick.ac.uk
                steven.brown@pharma.uzh.ch
                ctrobbins@wsu.edu
                Journal
                Front Zool
                Front. Zool
                Frontiers in Zoology
                BioMed Central (London )
                1742-9994
                17 September 2016
                17 September 2016
                2016
                : 13
                : 42
                Affiliations
                [1 ]Department of Integrative Physiology and Neuroscience, College of Veterinary Medicine, Washington State University, Mailstop 7620, Veterinary and Biomedical Research Bldg., Room 205, Pullman, WA 99164-7620 USA
                [2 ]Department of Mathematics and Statistics, Amherst College, Amherst, MA 01002 USA
                [3 ]Foothills Research Institute, Hinton, AB T7V 1X6 Canada
                [4 ]U.S. Fish and Wildlife Service, Libby, MT 59923 USA
                [5 ]Institute for Pharmacology and Toxicology, University of Zürich, Zürich, 8057 Switzerland
                [6 ]School of the Environment, Washington State University, Pullman, WA 99164 USA
                [7 ]Present address: Warwick Medical School and Warwick Systems Biology Centre, University of Warwick, Gibbet Hill Road, Coventry, CV4 7AL UK
                Article
                173
                10.1186/s12983-016-0173-x
                5026772
                253701ab-890e-4c7e-b03c-dff81906898d
                © The Author(s). 2016

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided 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 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.

                History
                : 6 April 2016
                : 22 August 2016
                Funding
                Funded by: Interagency Grizzly Bear Committee
                Funded by: Raili Korkka Brown Bear Endowment
                Funded by: Bear Research and Conservation Endowment
                Award ID: None
                Funded by: Funding partners of the Foothills Research Institute Program
                Funded by: Swiss National Science Foundation
                Funded by: US Fish and Wildlife Service
                Award ID: None
                Award ID: None
                Award Recipient :
                Categories
                Research
                Custom metadata
                © The Author(s) 2016

                Animal science & Zoology
                Animal science & Zoology

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