Periodic arousal from hibernation is necessary for initiation of immune responses in ground squirrels

Golden-mantled ground squirrels ( Spermophilus lateralis) undergo seasonal hibernation during which core body temperature (Tb) values are maintained 1–2°C above ambient temperature. Hibernation is not continuous. Squirrels arouse at ∼7-day intervals, during which Tbincreases to 37°C for ∼16 h; thereafter, they return to hibernation and sustain low Tbs until the next arousal. Over the course of the hibernation season, arousals consume 60–80% of a squirrel's winter energy budget, but their functional significance is unknown and disputed. Host-defense mechanisms appear to be downregulated during the hibernation season and preclude normal immune responses. These experiments assessed immune function during hibernation and subsequent periodic arousals. The acute-phase response to bacterial lipopolysaccharide (LPS) was arrested during hibernation and fully restored on arousal to normothermia. LPS injection (ip) resulted in a 1–1.5°C fever in normothermic animals that was sustained for >8 h. LPS was without effect in hibernating squirrels, neither inducing fever nor provoking arousal, but a fever did develop several days later, when squirrels next aroused from hibernation; the duration of this arousal was increased sixfold above baseline values. Intracerebroventricular infusions of prostaglandin E2provoked arousal from hibernation and induced fever, suggesting that neural signaling pathways that mediate febrile responses are functional during hibernation. Periodic arousals may activate a dormant immune system, which can then combat pathogens that may have been introduced immediately before or during hibernation.

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The contribution of the vagus nerve in interleukin-1β-induced fever is dependent on dose

AJP Regulatory Integrative and Comparative Physiology ◽

10.1152/ajpregu.2001.280.4.r929 ◽

2001 ◽

Vol 280 (4) ◽

pp. R929-R934 ◽

Cited By ~ 86

Author(s):

Michael K. Hansen ◽

Kevin A. O'Connor ◽

Lisa E. Goehler ◽

Linda R. Watkins ◽

Steven F. Maier

Keyword(s):

Core Body Temperature ◽

Vagal Afferents ◽

Interleukin 1Β ◽

Blood Levels ◽

Low Doses ◽

Neural Pathway ◽

Subdiaphragmatic Vagotomy ◽

Core Body ◽

Neural Signaling ◽

The Brain

It has been suggested that proinflammatory cytokines communicate to the brain via a neural pathway involving activation of vagal afferents by interleukin-1β (IL-1β), in addition to blood-borne routes. In support, subdiaphragmatic vagotomy blocks IL-1β-induced, brain-mediated responses such as fever. However, vagotomy has also been reported to be ineffective. Neural signaling would be expected to be especially important at low doses of cytokine, when local actions could occur, but only very small quantities of cytokine would become systemic. Here, we examined core body temperature after intraperitoneal injections of three doses of recombinat human IL-1β (rh-IL-1β). Subdiaphragmatic vagotomy completely blocked the fever produced by 0.1 μg/kg, only partially blocked the fever produced by 0.5 μg/kg, and had no effect at all on the fever that followed 1.0 μg/kg rh-IL-1β. Blood levels of rh-IL-1β did not become greater than normal basal levels of endogenous rat IL-β until the 0.5-μg/kg dose nor was IL-1β induced in the pituitary until this dose. These results suggest that low doses of intraperitoneal IL-1β induce fever via a vagal route and that dose may account for some of the discrepancies in the literature.

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Sulprostone-Induced Gastric Dysrhythmia in the Ferret: Conventional and Advanced Analytical Approaches

Frontiers in Physiology ◽

10.3389/fphys.2020.583082 ◽

2021 ◽

Vol 11 ◽

Author(s):

Zengbing Lu ◽

Yu Zhou ◽

Longlong Tu ◽

Sze Wa Chan ◽

Man P. Ngan ◽

...

Keyword(s):

Blood Pressure ◽

Body Temperature ◽

Core Body Temperature ◽

Analytical Techniques ◽

Dominant Frequency ◽

Fluctuation Analysis ◽

Prostaglandin E ◽

Myoelectric Activity ◽

Core Body ◽

Analytical Approaches

Nausea and emesis resulting from disease or drug treatment may be associated with disrupted gastric myoelectric activity (GMA). Conventional analytical techniques can determine the relative degrees of brady-, normo-, and tachygastric power, but lose information relative to the basic slow wave shape. The aim of the present study was to investigate the application of advanced analytical techniques in the analysis of disrupted GMA recorded after administration of sulprostone, a prostaglandin E3/1 agonist, in ferrets. Ferrets were implanted with radiotelemetry devices to record GMA, blood pressure, heart rate (HR) and core body temperature 1 week before the administration of sulprostone (30 μg/kg) or vehicle (saline, 0.5 mL/kg). GMA was initially analyzed using fast Fourier transformations (FFTs) and a conventional power partitioning. Detrended fluctuation analysis (DFA) was also applied to the GMA recordings to reveal information relative to the fluctuation of signals around local trends. Sample entropy (SampEn) analysis was used for examining the regularity of signals. Conventional signal processing techniques revealed that sulprostone increased the dominant frequency (DF) of slow waves, with an increase in the percentage power of the tachygastric range and a decrease in the percentage power of the normogastric range. DFA revealed that sulprostone decreased the fluctuation function, indicative of a loss of the variability of GMA fluctuations around local trends. Sulprostone increased SampEn values, indicating a loss of regularity in the GMA data. Behaviorally, sulprostone induced emesis and caused defecation. It also increased blood pressure and elevated HR, with an associated decrease in HR variability (HRV). Further analysis of HRV revealed a decrease in both low-frequency (LF) and high-frequency (HF) components, with an overall increase in the LF/HF ratio. Sulprostone did not affect core body temperature. In conclusion, DFA and SampEn permit a detailed analysis of GMA, which is necessary to understand the action of sulprostone to modulate gastric function. The action to decrease HRV and increase the LF/HF ratio may be consistent with a shift toward sympathetic nervous system dominance, commonly seen during nausea.

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Are ground squirrels sleep deprived during hibernation?

AJP Regulatory Integrative and Comparative Physiology ◽

10.1152/ajpregu.1991.260.6.r1123 ◽

1991 ◽

Vol 260 (6) ◽

pp. R1123-R1129 ◽

Cited By ~ 19

Author(s):

L. Trachsel ◽

D. M. Edgar ◽

H. C. Heller

Keyword(s):

Slow Wave ◽

Slow Wave Sleep ◽

Ground Squirrels ◽

Wave Intensity ◽

Spermophilus Lateralis ◽

Sleep Debt ◽

Function Of Sleep ◽

Deep Hibernation ◽

To Receive ◽

Periodic Arousals

Hibernation is an adaptation for energy conservation, which probably evolved as an extension of non-rapid-eye-movement sleep mechanisms. Yet, during periodic arousals from bouts of deep hibernation, ground squirrels (Spermophilus lateralis) spend most of their time asleep. Spectral analysis of the electroencephalogram revealed that cortical slow-wave intensity during sleep is high at the beginning of a euthermic period and declines thereafter. Sleep slow-wave intensity is greater after longer bouts of hibernation than after shorter bouts. We hypothesize that low body temperatures during hibernation are incompatible with the restorative function of sleep as reflected in cortical slow-wave activity. Animals must incur the energetic costs of periodic arousals from hibernation to receive the restorative benefits of euthermic slow-wave sleep. The timing of arousals from hibernation may be a function of accumulated sleep debt.

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Circulation and metabolic rates in a natural hibernator: an integrative physiological model

AJP Regulatory Integrative and Comparative Physiology ◽

10.1152/ajpregu.00273.2010 ◽

2010 ◽

Vol 299 (6) ◽

pp. R1478-R1488 ◽

Cited By ~ 28

Author(s):

Marshall Hampton ◽

Bethany T. Nelson ◽

Matthew T. Andrews

Keyword(s):

Body Temperature ◽

Metabolic Rate ◽

Core Body Temperature ◽

Circulatory System ◽

Physiological Model ◽

Ground Squirrels ◽

Metabolic Rates ◽

Spermophilus Tridecemlineatus ◽

Brown Adipose ◽

Core Body

Small hibernating mammals show regular oscillations in their heart rate and body temperature throughout the winter. Long periods of torpor are abruptly interrupted by arousals with heart rates that rapidly increase from 5 beats/min to over 400 beats/min and body temperatures that increase by ∼30°C only to drop back into the hypothermic torpid state within hours. Surgically implanted transmitters were used to obtain high-resolution electrocardiogram and body temperature data from hibernating thirteen-lined ground squirrels ( Spermophilus tridecemlineatus ). These data were used to construct a model of the circulatory system to gain greater understanding of these rapid and extreme changes in physiology. Our model provides estimates of metabolic rates during the torpor-arousal cycles in different model compartments that would be difficult to measure directly. In the compartment that models the more metabolically active tissues and organs (heart, brain, liver, and brown adipose tissue) the peak metabolic rate occurs at a core body temperature of 19°C approximately midway through an arousal. The peak metabolic rate of the active tissues is nine times the normothermic rate after the arousal is complete. For the overall metabolic rate in all tissues, the peak-to-resting ratio is five. This value is high for a rodent, which provides evidence for the hypothesis that the arousal from torpor is limited by the capabilities of the cardiovascular system.

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Hibernation strategies and patterns in sympatric arctic species, the Alaska marmot and the arctic ground squirrel

Journal of Mammalogy ◽

10.1093/jmammal/gyv163 ◽

2015 ◽

Vol 97 (1) ◽

pp. 135-144 ◽

Cited By ~ 7

Author(s):

Trixie N. Lee ◽

Franziska Kohl ◽

C. Loren Buck ◽

Brian M. Barnes

Keyword(s):

Ground Squirrel ◽

Core Body Temperature ◽

Ground Squirrels ◽

The Arctic ◽

Arctic Ground Squirrel ◽

Slow Cooling ◽

Ambient Temperatures ◽

The Difference ◽

Arctic Ground Squirrels ◽

Core Body

Abstract We compared patterns of core body temperature ( Tb ) change, including inter-individual synchrony, in 2 free-living arctic hibernators that differ in size and sociality, the Alaska marmot ( Marmota broweri ) and the arctic ground squirrel ( Urocitellus parryii ). We report overwinter Tb changes from 3 to 4 marmots from the same hibernaculum in each of 3 years and from 7 ground squirrels that hibernated at 2 nearby burrow sites in 1 year. Very close synchrony in the timing of torpor and arousal cycles in Alaska marmots indicates social hibernation and thermoregulation, while lack of synchrony in arctic ground squirrels further confirms solitary hibernation. The mean duration between the first and last marmot measured within the group to initiate an arousal was 3.7±2.5h and to recool to 30°C during torpor entrance was 5.7±3.7h. The minimum Tb recorded in marmots was 0.6°C and in ground squirrels was −2.0°C. Marmots entering torpor displayed an interrupted pattern of Tb change defined by 2 distinct rates of cooling, early and late during entry, that differed by 21-fold. Ground squirrels cooled in a continuous pattern, initially 3-fold slower than marmots during rapid cooling but 4-fold faster during slow cooling. Both species must minimize energy expenditure to survive long arctic winters; our results suggest that Alaska marmots do this through social thermoregulation, while arctic ground squirrels decrease Tb below freezing to minimize the difference between body and ambient temperatures.

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Disturbance of thermal homeostasis following dynamic exercise

Applied Physiology Nutrition and Metabolism ◽

10.1139/h07-044 ◽

2007 ◽

Vol 32 (4) ◽

pp. 818-831 ◽

Cited By ~ 20

Author(s):

Glen P. Kenny ◽

Ollie Jay ◽

W. Shane Journeay

Keyword(s):

Body Temperature ◽

Heat Loss ◽

Core Body Temperature ◽

Dynamic Exercise ◽

Hemodynamic Changes ◽

Post Exercise ◽

Cutaneous Vasodilation ◽

Baseline Values ◽

Sudomotor Activity ◽

Core Body

Recovery from dynamic exercise results in significant perturbations of thermoregulatory control. These perturbations evoke a prolonged elevation in core body temperature and a concomitant decrease in sweating, skin blood flow, and skin temperature to pre-exercise baseline values within the early stages of recovery. Cutaneous vasodilation and sweating are critical responses necessary for effective thermoregulation during heat stress in humans. The ability to modulate the rate of heat loss through adjustments in vasomotor and sudomotor activity is a fundamental mechanism of thermoregulatory homeostasis. There is a growing body of evidence in support of a possible relationship between hemodynamic changes postexercise and heat loss responses. Specifically, nonthermoregulatory factors, such as baroreceptors, associated with hemodynamic changes, influence the regulation of core body temperature during exercise recovery. The following review will examine the etiology of the post-exercise disturbance in thermal homeostasis and evaluate possible thermal and nonthermal factors associated with a prolonged hyperthermic state following exercise.

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Effect of environmental temperature on sleep, locomotor activity, core body temperature and immune responses of C57BL/6J mice

Brain Behavior and Immunity ◽

10.1016/j.bbi.2007.03.007 ◽

2007 ◽

Vol 21 (7) ◽

pp. 975-987 ◽

Cited By ~ 35

Author(s):

K.A. Jhaveri ◽

R.A. Trammell ◽

L.A. Toth

Keyword(s):

Locomotor Activity ◽

Body Temperature ◽

Immune Responses ◽

Environmental Temperature ◽

Core Body Temperature ◽

Core Body

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Body Temperature Frequency Distributions: A Tool for Assessing Thermal Performance in Endotherms?

Frontiers in Physiology ◽

10.3389/fphys.2021.760797 ◽

2021 ◽

Vol 12 ◽

Author(s):

D.L. Levesque ◽

J. Nowack ◽

J.G. Boyles

Keyword(s):

Body Temperature ◽

Thermal Performance ◽

Core Body Temperature ◽

Ground Squirrels ◽

Body Temperatures ◽

Frequency Distributions ◽

Biologically Relevant ◽

Performance Curves ◽

Continuous Body ◽

Core Body

There is increasing recognition that rather than being fully homeothermic, most endotherms display some degree of flexibility in body temperature. However, the degree to which this occurs varies widely from the relatively strict homeothermy in species, such as humans to the dramatic seasonal hibernation seen in Holarctic ground squirrels, to many points in between. To date, attempts to analyse this variability within the framework generated by the study of thermal performance curves have been lacking. We tested if frequency distribution histograms of continuous body temperature measurements could provide a useful analogue to a thermal performance curve in endotherms. We provide examples from mammals displaying a range of thermoregulatory phenotypes, break down continuous core body temperature traces into various components (active and rest phase modes, spreads and skew) and compare these components to hypothetical performance curves. We did not find analogous patterns to ectotherm thermal performance curves, in either full datasets or by breaking body temperature values into more biologically relevant components. Most species had either bimodal or right-skewed (or both) distributions for both active and rest phase body temperatures, indicating a greater capacity for mammals to tolerate body temperatures elevated above the optimal temperatures than commonly assumed. We suggest that while core body temperature distributions may prove useful in generating optimal body temperatures for thermal performance studies and in various ecological applications, they may not be a good means of assessing the shape and breath of thermal performance in endotherms. We also urge researchers to move beyond only using mean body temperatures and to embrace the full variability in both active and resting temperatures in endotherms.

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