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      Hypothesis and Theory: A Two-Process Model of Torpor-Arousal Regulation in Hibernators

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          Abstract

          Hibernating mammals drastically lower their metabolic rate (MR) and body temperature (T b) for up to several weeks, but regularly rewarm and stay euthermic for brief periods. It has been hypothesized that the necessity for rewarming is due to the accumulation or depletion of metabolites, or the accrual of cellular damage that can be eliminated only in the euthermic state. Recent evidence for significant inverse relationships between the duration of torpor bouts (TBD) and MR in torpor strongly supports this hypothesis. We developed a new mathematical model that simulates hibernation patterns. The model involves an hourglass process H (Hibernation) representing the depletion/accumulation of a crucial enzyme/metabolite, and a threshold process H thr. Arousal, modelled as a logistic process, is initiated once the exponentially declining process H reaches H thr. We show that this model can predict several phenomena observed in hibernating mammals, namely the linear relationship between TMR and TBD, effects of ambient temperature on TBD, the modulation of torpor depth and duration within the hibernation season, (if process H thr undergoes seasonal changes). The model does not need but allows for circadian cycles in the threshold T, which lead to arousals occurring predominantly at certain circadian phases, another phenomenon that has been observed in certain hibernators. It does not however, require circadian rhythms in T b or MR during torpor. We argue that a two-process regulation of torpor-arousal cycles has several adaptive advantages, such as an easy adjustment of TBD to environmental conditions as well as to energy reserves and, for species that continue to forage, entrainment to the light-dark cycle.

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          APE: Analyses of Phylogenetics and Evolution in R language.

          Analysis of Phylogenetics and Evolution (APE) is a package written in the R language for use in molecular evolution and phylogenetics. APE provides both utility functions for reading and writing data and manipulating phylogenetic trees, as well as several advanced methods for phylogenetic and evolutionary analysis (e.g. comparative and population genetic methods). APE takes advantage of the many R functions for statistics and graphics, and also provides a flexible framework for developing and implementing further statistical methods for the analysis of evolutionary processes. The program is free and available from the official R package archive at http://cran.r-project.org/src/contrib/PACKAGES.html#ape. APE is licensed under the GNU General Public License.
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            A two process model of sleep regulation.

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              Timing of human sleep: recovery process gated by a circadian pacemaker.

              A model for the timing of human sleep is presented. It is based on a sleep-regulating variable (S)--possibly, but not necessarily, associated with a neurochemical substance--which increases during wakefulness and decreases during sleep. Sleep onset is triggered when S approaches an upper threshold (H); awakening occurs when S reaches a lower threshold (L). The thresholds show a circadian rhythm controlled by a single circadian pacemaker. Time constants of the S process were derived from rates of change of electroencephalographic (EEG) power density during regular sleep and during recovery from sleep deprivation. The waveform of the circadian threshold fluctuations was derived from spontaneous wake-up times after partial sleep deprivation. The model allows computer simulations of the main phenomena of human sleep timing, such as 1) internal desynchronization in the absence of time cues, 2) sleep fragmentation during continuous bed rest, and 3) circadian phase dependence of sleep duration during isolation from time cues, recovery from sleep deprivation, and shift work. The model shows that the experimental data are consistent with the concept of a single circadian pacemaker in humans. It has implications for the understanding of sleep as a restorative process and its timing with respect to day and night.
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                Author and article information

                Contributors
                Journal
                Front Physiol
                Front Physiol
                Front. Physiol.
                Frontiers in Physiology
                Frontiers Media S.A.
                1664-042X
                20 June 2022
                2022
                : 13
                : 901270
                Affiliations
                [1] 1 Research Institute of Wildlife Ecology , Department of Interdisciplinary Life Sciences , University of Veterinary Medicine , Vienna, Austria
                [2] 2 Centre for Behavioural and Physiological Ecology, Zoology , University of New England , Armidale, NSW, Australia
                Author notes

                Edited by: Nicholas Simon Foulkes, Karlsruhe Institute of Technology (KIT), Germany

                Reviewed by: Matteo Cerri, University of Bologna, Italy

                J. F. Staples, Western University, Canada

                Lennart Hilbert, Karlsruhe Institute of Technology (KIT), Germany

                *Correspondence: Thomas Ruf, thomas.ruf@ 123456vetmeduni.ac.at

                This article was submitted to Chronobiology, a section of the journal Frontiers in Physiology

                Article
                901270
                10.3389/fphys.2022.901270
                9266152
                35812322
                a44530e7-0711-4dac-936f-29689cf0d0c1
                Copyright © 2022 Ruf, Giroud and Geiser.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 21 March 2022
                : 27 May 2022
                Funding
                Funded by: Austrian Science Fund , doi 10.13039/501100002428;
                Award ID: P 31577 P 25023 P 27267
                Categories
                Physiology
                Hypothesis and Theory

                Anatomy & Physiology
                cycles,interbout euthermia,metabolic rate,hourglass mechanism,periodic arousal,circadian rhythms

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