Neural control of fasting-induced torpor in mice

Hitrec, Timna; Luppi, Marco; Bastianini, Stefano; Squarcio, Fabio; Berteotti, Chiara; Martire, Viviana Lo; Martelli, Davide; Occhinegro, Alessandra; Tupone, Domenico; Zoccoli, Giovanna; Amici, Roberto; Cerri, Matteo

doi:10.1038/s41598-019-51841-2

Cited by 36 publications

(35 citation statements)

References 42 publications

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“…Pioneering studies have identified hypothalamic nuclei and circuits that are critically involved in regulation of body temperature and metabolism 9 , 12 , 98 . Our tracing studies reveal projections from ERα + neurons to several of these hypothalamic nuclei, including the DMH, VMH, and ARC.…”

Section: Discussionmentioning

confidence: 99%

Estrogen-sensitive medial preoptic area neurons coordinate torpor in mice

Zhi

Reis

et al. 2020

Nat Commun

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Homeotherms maintain a stable internal body temperature despite changing environments. During energy deficiency, some species can cease to defend their body temperature and enter a hypothermic and hypometabolic state known as torpor. Recent advances have revealed the medial preoptic area (MPA) as a key site for the regulation of torpor in mice. The MPA is estrogen-sensitive and estrogens also have potent effects on both temperature and metabolism. Here, we demonstrate that estrogen-sensitive neurons in the MPA can coordinate hypothermia and hypometabolism in mice. Selectively activating estrogen-sensitive MPA neurons was sufficient to drive a coordinated depression of metabolic rate and body temperature similar to torpor, as measured by body temperature, physical activity, indirect calorimetry, heart rate, and brain activity. Inducing torpor with a prolonged fast revealed larger and more variable calcium transients from estrogen-sensitive MPA neurons during bouts of hypothermia. Finally, whereas selective ablation of estrogen-sensitive MPA neurons demonstrated that these neurons are required for the full expression of fasting-induced torpor in both female and male mice, their effects on thermoregulation and torpor bout initiation exhibit differences across sex. Together, these findings suggest a role for estrogen-sensitive MPA neurons in directing the thermoregulatory and metabolic responses to energy deficiency.

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Section: Discussionmentioning

confidence: 99%

Estrogen-sensitive medial preoptic area neurons coordinate torpor in mice

Zhi

Reis

et al. 2020

Nat Commun

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“…To examine neural mechanisms underlying stress-induced sleep-like inactivity, we examined c-Fos expression, a histological marker for neuronal activity, in brain regions related to sleep and wake regulations 13 , 31 after either social defeat stress or cage transfer. The stress did not affect c-Fos expression in sleep-promoting brain regions, VLPO and MnPO (Fig.…”

Section: Resultsmentioning

confidence: 99%

“…Although whether DMH neurons can regulate total sleep is not reported, the activation of VLPAG neurons reduced wake periods along with increased non-REM sleep in a previous study 15 . Interestingly, these brain regions are activated by torpor-inducing stimuli 31 , such as fasting and cold exposure, and the DMH is crucial for optogenetically induced hibernation-like state 33 . Consistent with the activation of these brain regions, we found that social defeat stress decreases body temperature in a manner correlated to the proportion of active periods.…”

Section: Discussionmentioning

confidence: 99%

Stress-induced sleep-like inactivity modulates stress susceptibility in mice

Nagai

Numa

et al. 2020

Sci Rep

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Severe environmental and social stress induces dysregulation of sleep along with mood and cognitive disturbances. However, the role and mechanism of this sleep dysregulation remain elusive. Here we evaluated sleep-like inactivity measured by voluntary movements and its relationship to social behaviors in mice without or with social defeat stress as well as the stressed mice with subsequent sleep deprivation. Social defeat stress immediately induced sleep-like inactivity with decreased body temperature. In the social interaction test, the control mice showed high social interest and its correlation with social sniffing intensity, the latter of which indicates positive valence of social sniffing. After the stress, these social characteristics were maintained in stress-resilient mice, but disrupted in stress-susceptible mice, leading to social avoidance. Sleep deprivation after the stress decreased social sniffing intensity along with reduced social interest, but enhanced the exploratory activity with the positive valence of social sniffing. We also found by c-Fos immunohistochemistry that the stress activated sleep-related brain regions, the dorsomedial hypothalamus and ventrolateral periaqueductal gray. Collectively, these findings show that stress activates sleep-related brain regions and induces sleep-like inactivity, contributing to multiple roles of stress-induced sleep for social behaviors.

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“…The use of infrared thermography has the potential to provide a non-invasive method to measure T core but its own methodological limitations have to be taken into account 5,6 . Previous applications of non-contact T skin measurements in biomedical research have been limited by the requirement that animals needed to be handled by the experimenter [7][8][9][10][11][12][13][14][15] , measurements were taken at a limited number of timepoints 7,8,[10][11][12][13][14][15][16][17] , and/or measurements resulted in large datafiles requiring complex data analysis 10,12,13,[16][17][18] . The present study developed, optimised and validated an algorithm that enables estimation of relative changes in T core based on the continuous and non-invasive automated measurement of T skin of mice housed at room temperature.…”

Section: Discussionmentioning

confidence: 99%

“…www.nature.com/scientificreports/ methods typically require animal handling, are not continuous, and do not measure T core [7][8][9][10][11][12][13][14][15][16][17][18] . The non-invasive nature of thermography measurements does however provide the potential to assess body temperature in undisturbed freely-moving laboratory mice, removing the confounding factor of handling stress and representing an obvious refinement in terms of animal welfare.…”

Section: Scientific Reportsmentioning

confidence: 99%

Continuous and non-invasive thermography of mouse skin accurately describes core body temperature patterns, but not absolute core temperature

Vinne

Pothecary

Wilcox

et al. 2020

Sci Rep

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Body temperature is an important physiological parameter in many studies of laboratory mice. Continuous assessment of body temperature has traditionally required surgical implantation of a telemeter, but this invasive procedure adversely impacts animal welfare. Near-infrared thermography provides a non-invasive alternative by continuously measuring the highest temperature on the outside of the body (Tskin), but the reliability of these recordings as a proxy for continuous core body temperature (Tcore) measurements has not been assessed. Here, Tcore (30 s resolution) and Tskin (1 s resolution) were continuously measured for three days in mice exposed to ad libitum and restricted feeding conditions. We subsequently developed an algorithm that optimised the reliability of a Tskin-derived estimate of Tcore. This identified the average of the maximum Tskin per minute over a 30-min interval as the optimal way to estimate Tcore. Subsequent validation analyses did however demonstrate that this Tskin-derived proxy did not provide a reliable estimate of the absolute Tcore due to the high between-animal variability in the relationship between Tskin and Tcore. Conversely, validation showed that Tskin-derived estimates of Tcore reliably describe temporal patterns in physiologically-relevant Tcore changes and provide an excellent measure to perform within-animal comparisons of relative changes in Tcore.

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Neural control of fasting-induced torpor in mice

Cited by 36 publications

References 42 publications

Estrogen-sensitive medial preoptic area neurons coordinate torpor in mice

Estrogen-sensitive medial preoptic area neurons coordinate torpor in mice

Stress-induced sleep-like inactivity modulates stress susceptibility in mice

Continuous and non-invasive thermography of mouse skin accurately describes core body temperature patterns, but not absolute core temperature

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