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1.
Biol Lett ; 20(9): 20240291, 2024 Sep.
Artículo en Inglés | MEDLINE | ID: mdl-39288816

RESUMEN

Hibernators face an energetic dilemma in the autumn at northern latitudes; while temperatures and food availability decrease, hibernating species need to build fat deposits to survive the winter. During this critical fattening phase, insectivorous boreal bats use torpor to build and conserve their reserves. However, we still know little about temporal variability in torpor use employed by bats during the prehibernation fattening period and how decreasing temperatures and food availability in combination with increasing individual body mass impact this. Here, we present two general hypotheses for explaining temporal torpor patterns observed in a boreal bat (Eptesicus nilssonii), in which torpor use (i) facilitates rapid mass gain or (ii) conserves stored body mass. Although temporally separated in our dataset, data on temperature, insect abundance and body mass throughout the prehibernation period indicate that E. nilssonii reaches the majority of its overwintering mass before the onset of increasing daytime and night-time torpor use. In combination with low food availability by this point in time, these observations suggest torpor expression may be intended to conserve gained reserves rather than facilitate mass gain. Our study is intended as a first proof of concept for disentangling temporal drivers of torpor in bats during the prehibernation fattening phase.


Asunto(s)
Quirópteros , Hibernación , Letargo , Animales , Quirópteros/fisiología , Letargo/fisiología , Hibernación/fisiología , Estaciones del Año , Peso Corporal
2.
J Exp Biol ; 227(18)2024 Sep 15.
Artículo en Inglés | MEDLINE | ID: mdl-39206564

RESUMEN

Torpor is an adaptive strategy allowing heterothermic animals to cope with energy limitations. In birds and mammals, intrinsic and extrinsic factors, such as body mass and ambient temperature, are the main variables influencing torpor use. A theoretical model of the relationship between metabolic rate during torpor and ambient temperature has been proposed. Nevertheless, no empirical attempts have been made to assess the model predictions under different climates. Using open-flow respirometry, we evaluated the ambient temperature at which bats entered torpor and when torpid metabolic rate reached its minimum, the reduction in metabolic rate below basal values, and minimum torpid metabolic rate in 11 bat species of the family Vespertilionidae with different body mass from warm and cold climates. We included data on the minimum torpid metabolic rate of five species we retrieved from the literature. We tested the effects using mixed-effect phylogenetic models. All models showed a significant interaction between body mass and climate. Smaller bats went into torpor and reached minimum torpid metabolic rates at warmer temperatures, showed a higher reduction in the metabolic rate below basal values, and presented lower torpid metabolic rates than larger ones. The slopes of the models were different for bats from different climates. These results are likely explained by differences in body mass and the metabolic rate of bats, which may favor larger bats expressing torpor in colder sites and smaller bats in the warmer ones. Further studies to assess torpor use in bats from different climates are proposed.


Asunto(s)
Peso Corporal , Quirópteros , Clima , Metabolismo Energético , Letargo , Animales , Quirópteros/fisiología , Letargo/fisiología , Temperatura , Metabolismo Basal , Modelos Biológicos , Filogenia
3.
J Therm Biol ; 124: 103933, 2024 Aug.
Artículo en Inglés | MEDLINE | ID: mdl-39208468

RESUMEN

To assess the vulnerability of birds and mammals to climate change recent studies have used the upper critical limit of thermoneutrality (TUC) as an indicator of thermal tolerance. But, the association between TUC and thermal tolerance is not straightforward and most studies describe TUC based solely on a deviation in metabolism from basal levels, without also considering the onset of evaporative cooling. It was argued recently that certain torpor-using bat species who survived prolonged exposure to high ambient temperatures (i.e. high thermal tolerance) experienced during extreme heat events did so by entering torpor and using facultative heterothermy to thermoconform and save on body water. Assuming that TUC is indicative of thermal tolerance, we expect TUC in torpor-using species to be higher than that of species which are obligate homeotherms, albeit that this distinction is based on confirmation of torpor use at low temperatures. To test this prediction, we performed a phylogenetically informed comparison of bat species known to use torpor (n = 48) and homeothermic (n = 16) bat species using published thermoregulatory datasets to compare the lower critical limit of thermoneutrality (TLC) and TUC in relation to body temperature. The influence of diet, biogeographical region, body mass and basal metabolic rate (BMR) was also considered. Body mass had a positive relationship with BMR, an inverse relationship with TLC and no relationship with TUC. Normothermic body temperature scaled positively with BMR, TLC and TUC. There was no relationship between diet or region and BMR, but both influenced thermal limits. Torpor-using bats had lower body mass and body temperatures than homeothermic bats, but there was no difference in BMR, TLC and TUC between them. Exceptional examples of physiological flexibility were observed in 34 torpor-using species and eight homeothermic species, which included 15 species of bats maintaining BMR-level metabolism at ambient temperatures as high as 40 °C (and corresponding body temperatures ∼39.2 °C). However, we argue that TUC based on metabolism alone is not an appropriate indicator of thermal tolerance as it disregards differences in the ability of animals to tolerate higher levels of hyperthermia, importance of hydration status and capacity for evaporative cooling. Also, the variability in TUC based on diet challenges the idea of evolutionary conservatism and warrants further consideration.


Asunto(s)
Quirópteros , Termotolerancia , Quirópteros/fisiología , Animales , Letargo/fisiología , Metabolismo Basal , Regulación de la Temperatura Corporal , Temperatura Corporal
4.
Proc Biol Sci ; 291(2026): 20240855, 2024 Jul.
Artículo en Inglés | MEDLINE | ID: mdl-38981523

RESUMEN

Understanding how animals meet their daily energy requirements is critical in our rapidly changing world. Small organisms with high metabolic rates can conserve stored energy when food availability is low or increase energy intake when energetic requirements are high, but how they balance this in the wild remains largely unknown. Using miniaturized heart rate transmitters, we continuously quantified energy expenditure, torpor use and foraging behaviour of free-ranging male bats (Nyctalus noctula) in spring and summer. In spring, bats used torpor extensively, characterized by lowered heart rates and consequently low energy expenditures. In contrast, in summer, bats consistently avoided torpor, even though they could have used this low-energy mode. As a consequence, daytime heart rates in summer were three times as high compared with the heart rates in spring. Daily energy use increased by 42% during summer, despite lower thermogenesis costs at higher ambient temperatures. Likely, as a consequence, bats nearly doubled their foraging duration. Overall, our results indicate that summer torpor avoidance, beneficial for sperm production and self-maintenance, comes with a high energetic cost. The ability to identify and monitor such vulnerable energetic life-history stages is particularly important to predict how species will deal with increasing temperatures and changes in their resource landscapes.


Asunto(s)
Quirópteros , Metabolismo Energético , Frecuencia Cardíaca , Estaciones del Año , Animales , Masculino , Quirópteros/fisiología , Letargo/fisiología
5.
Proc Biol Sci ; 291(2026): 20241137, 2024 Jul.
Artículo en Inglés | MEDLINE | ID: mdl-38981525

RESUMEN

Torpor is widespread among bats presumably because most species are small, and torpor greatly reduces their high mass-specific resting energy expenditure, especially in the cold. Torpor has not been recorded in any bat species larger than 50 g, yet in theory could be beneficial even in the world's largest bats (flying-foxes; Pteropus spp.) that are exposed to adverse environmental conditions causing energy bottlenecks. We used temperature telemetry to measure body temperature in wild-living adult male grey-headed flying-foxes (P. poliocephalus; 799 g) during winter in southern Australia. We found that all individuals used torpor while day-roosting, with minimum body temperature reaching 27°C. Torpor was recorded following a period of cool, wet and windy weather, and on a day with the coldest maximum air temperature, suggesting it is an adaptation to reduce energy expenditure during periods of increased thermoregulatory costs and depleted body energy stores. A capacity for torpor among flying-foxes has implications for understanding their distribution, behavioural ecology and life history. Furthermore, our discovery increases the body mass of bats known to use torpor by more than tenfold and extends the documented use of this energy-saving strategy under wild conditions to all bat superfamilies, with implications for the evolutionary maintenance of torpor among bats and other mammals.


Asunto(s)
Quirópteros , Letargo , Animales , Quirópteros/fisiología , Letargo/fisiología , Masculino , Metabolismo Energético , Telemetría , Temperatura Corporal , Estaciones del Año , Australia del Sur
6.
J Comp Physiol B ; 194(4): 519-535, 2024 Aug.
Artículo en Inglés | MEDLINE | ID: mdl-38972930

RESUMEN

Ultradian rhythms of metabolism, body temperature and activity are attenuated or disappear completely during torpor in Djungarian hamsters, for all three ultradian periodicities (URsmall, URmedium and URlarge). URsmall and URmedium disappear during entrance into torpor, whereas URlarge disappear later or continue with a low amplitude. This suggests a tight functional link between torpor and the expression of ultradian rhythms, i.e. torpor is achieved by suppression of metabolic rate as well as silencing of ultradian rhythms. Spontaneous torpor is often initiated after an ultradian burst of activity and metabolic rate, beginning with a period of motionless rest and accompanied by a decrease of metabolic rate and body temperature. To extend previous findings on the potential role of the adrenergic system on torpor induction we analysed the influence of the ß3-adrenergic agonist Mirabegron on torpor in Djungarian hamsters, as compared to the influence of the ß-adrenergic antagonist Propranolol. Hamsters were implanted with 10 day release pellets of Mirabegron (0.06 mg day-1) or Propranolol (0.3 mg day-1). Mirabegron transiently supressed and accelerated ultradian rhythms but had no effect on torpor behaviour. Propranolol did not affect torpor behaviour nor the expression of ultradian rhythms with the dosage applied during this study.


Asunto(s)
Phodopus , Letargo , Ritmo Ultradiano , Animales , Letargo/fisiología , Phodopus/fisiología , Cricetinae , Masculino , Ritmo Ultradiano/fisiología , Propranolol/farmacología , Antagonistas Adrenérgicos beta/farmacología , Temperatura Corporal , Actividad Motora , Metabolismo Basal
7.
Acta Neuropathol Commun ; 12(1): 86, 2024 06 04.
Artículo en Inglés | MEDLINE | ID: mdl-38835043

RESUMEN

Tau protein hyperphosphorylation and aggregation are key pathological events in neurodegenerative tauopathies such as Alzheimer's disease. Interestingly, seasonal hibernators show extensive tau hyperphosphorylation during torpor, i.e., the hypothermic and hypometabolic state of hibernation, which is completely reversed during arousal. Torpor-associated mechanisms that reverse tau hyperphosphorylation may be of therapeutic relevance, however, it is currently not known to what extent they apply to human tau. Here we addressed this issue using daily torpor in wildtype mice that express mouse tau (mtau) and in mice that lack mtau expression and instead express human tau (htau). AT8, AT100 and Ser396 immunoblotting and immunohistochemistry were used to assess tau (hyper)phosphorylation at clinically relevant phosphorylation sites. We found that torpor robustly and reversibly increases the levels of phosphorylated tau in both mtau and htau mice. Immunohistochemistry revealed four brain areas that show prominent tau phosphorylation: the hippocampus, posterior parietal cortex, piriform cortex and cortical amygdala. Whereas wildtype mice primarily showed increased levels of diffusely organized hyperphosphorylated tau during torpor, htau mice contained clear somato-dendritic accumulations of AT8 reactivity resembling tau pre-tangles as observed in the Alzheimer brain. Interestingly, AT8-positive accumulations disappeared upon arousal, and tau phosphorylation levels at 24 h after arousal were lower than observed at baseline, suggesting a beneficial effect of torpor-arousal cycles on preexisting hyperphosphorylated tau. In conclusion, daily torpor in mice offers a quick and standardized method to study tau phosphorylation, accumulation and clearance in mouse models relevant for neurodegeneration, as well as opportunities to discover new targets for the treatment of human tauopathies.


Asunto(s)
Encéfalo , Ratones Transgénicos , Letargo , Proteínas tau , Animales , Humanos , Masculino , Ratones , Encéfalo/metabolismo , Ratones Endogámicos C57BL , Fosforilación , Proteínas tau/metabolismo , Proteínas tau/genética , Letargo/fisiología
8.
Ecol Evol Physiol ; 97(1): 53-63, 2024.
Artículo en Inglés | MEDLINE | ID: mdl-38717368

RESUMEN

AbstractMany animals follow annual cycles wherein physiology and behavior change seasonally. Hibernating mammals undergo one of the most drastic seasonal alterations of physiology and behavior, the timing of which can have significant fitness consequences. The environmental cues regulating these profound phenotypic changes will heavily influence whether hibernators acclimate and ultimately adapt to climate change. Hence, identifying the cues and proximate mechanisms responsible for hibernation termination timing is critical. Northern Idaho ground squirrels (Urocitellus brunneus)-a rare, endemic species threatened with extinction-exhibit substantial variation in hibernation termination phenology, but it is unclear what causes this variation. We attached geolocators to free-ranging squirrels to test the hypothesis that squirrels assess surface conditions in spring before deciding whether to terminate seasonal heterothermy or reenter torpor. Northern Idaho ground squirrels frequently reentered torpor following a brief initial emergence from hibernacula and were more likely to do so earlier in spring or when challenged by residual snowpack. Female squirrels reentered torpor when confronted with relatively shallow snowpack upon emergence, whereas male squirrels reentered torpor in response to deeper spring snowpack. This novel behavior was previously assumed to be physiologically constrained in male ground squirrels by testosterone production required for spermatogenesis and activated by the circannual clock. Assessing surface conditions to decide when to terminate hibernation may help buffer these threatened squirrels against climate change. Documenting the extent to which other hibernators can facultatively alter emergence timing by reentering torpor after emergence will help identify which species are most likely to persist under climate change.


Asunto(s)
Hibernación , Sciuridae , Estaciones del Año , Nieve , Animales , Sciuridae/fisiología , Hibernación/fisiología , Femenino , Masculino , Letargo/fisiología
9.
J Comp Physiol B ; 194(3): 383-401, 2024 Jun.
Artículo en Inglés | MEDLINE | ID: mdl-38733409

RESUMEN

Vocalisations are increasingly being recognised as an important aspect of normal rodent behaviour yet little is known of how they interact with other spontaneous behaviours such as sleep and torpor, particularly in a social setting. We obtained chronic recordings of the vocal behaviour of adult male and female Djungarian hamsters (Phodopus sungorus) housed under short photoperiod (8 h light, 16 h dark, square wave transitions), in different social contexts. The animals were kept in isolation or in same-sex sibling pairs, separated by a grid which allowed non-physical social interaction. On approximately 20% of days hamsters spontaneously entered torpor, a state of metabolic depression that coincides with the rest phase of many small mammal species in response to actual or predicted energy shortages. Animals produced ultrasonic vocalisations (USVs) with a peak frequency of 57 kHz in both social and asocial conditions and there was a high degree of variability in vocalisation rate between subjects. Vocalisation rate was correlated with locomotor activity across the 24-h light cycle, occurring more frequently during the dark period when the hamsters were more active and peaking around light transitions. Solitary-housed animals did not vocalise whilst torpid and animals remained in torpor despite overlapping with vocalisations in social-housing. Besides a minor decrease in peak USV frequency when isolated hamsters were re-paired with their siblings, changing social contexts did not influence vocalisation behaviour or structure. In rare instances, temporally overlapping USVs occurred when animals were socially-housed and were grouped in such a way that could indicate coordination. We did not observe broadband calls (BBCs) contemporaneous with USVs in this paradigm, corroborating their correlation with physical aggression which was absent from our experiment. Overall, we find little evidence to suggest a direct social function of hamster USVs. We conclude that understanding the effects of vocalisations on spontaneous behaviours, such as sleep and torpor, will inform experimental design of future studies, especially where the role of social interactions is investigated.


Asunto(s)
Ritmo Circadiano , Phodopus , Fotoperiodo , Vocalización Animal , Animales , Vocalización Animal/fisiología , Masculino , Phodopus/fisiología , Femenino , Ritmo Circadiano/fisiología , Cricetinae , Actividad Motora/fisiología , Fenotipo , Letargo/fisiología , Ultrasonido , Estaciones del Año , Conducta Social
10.
J Therm Biol ; 121: 103829, 2024 Apr.
Artículo en Inglés | MEDLINE | ID: mdl-38569326

RESUMEN

The physiological mechanisms of responses to stressors are at the core of ecophysiological studies that examine the limits of an organism's flexibility. Interindividual variability in these physiological responses can be particularly important and lead to differences in the stress response among population groups, which can affect population dynamics. Some observations of intersexual differences in heterothermy raise the question of whether there is a difference in energy management between the sexes. In this study, we assessed male and female differences in mouse lemurs (Microcebus murinus), a highly seasonal malagasy primate, by measuring their physiological flexibility in response to caloric restriction and examining the subsequent impact on reproductive success. Using complementary methods aiming to describe large-scale and daily variations in body temperature throughout a 6-month winter-like short-day (SD) period, we monitored 12 males and 12 females, applying chronic 40% caloric restriction (CR) to 6 individuals in each group. We found variations in Tb modulation throughout the SD period and in response to caloric treatment that depended on sex, as females, regardless of food restriction, and CR males, only, entered deep torpor. The use of deeper torpor, however, did not translate into a lower loss of body mass in females and did not affect reproductive success. Captive conditions may have buffered the depth of torpor and minimised the positive effects of torpor on energy savings. However, the significant sex differences in heterothermy we observed may point to physiological benefits other than preservation of energy reserves.


Asunto(s)
Restricción Calórica , Cheirogaleidae , Metabolismo Energético , Estaciones del Año , Animales , Femenino , Masculino , Cheirogaleidae/fisiología , Letargo/fisiología , Caracteres Sexuales , Temperatura Corporal , Reproducción , Regulación de la Temperatura Corporal
11.
J Comp Physiol B ; 194(3): 369-381, 2024 Jun.
Artículo en Inglés | MEDLINE | ID: mdl-38653849

RESUMEN

Monitoring body temperature and energy expenditure in freely-moving laboratory mice remains a powerful methodology used widely across a variety of disciplines-including circadian biology, sleep research, metabolic phenotyping, and the study of body temperature regulation. Some of the most pronounced changes in body temperature are observed when small heterothermic species reduce their body temperature during daily torpor. Daily torpor is an energy saving strategy characterized by dramatic reductions in body temperature employed by mice and other species when challenged to meet energetic demands. Typical measurements used to describe daily torpor are the measurement of core body temperature and energy expenditure. These approaches can have drawbacks and developing alternatives for these techniques provides options that can be beneficial both from an animal-welfare and study-complexity perspective. First, this paper presents and assesses a method to estimate core body temperature based on measurements of subcutaneous body temperature, and second, a separate approach to better estimate energy expenditure during daily torpor based on core body temperature. Third, the effects of light exposure during the habitual dark phase and sleep deprivation during the light period on body temperature dynamics were tested preliminary in fed and fasted mice. Together, the here-published approaches and datasets can be used in the future to assess body temperature and metabolism in freely-moving laboratory mice.


Asunto(s)
Temperatura Corporal , Metabolismo Energético , Ayuno , Privación de Sueño , Animales , Privación de Sueño/fisiopatología , Privación de Sueño/metabolismo , Ratones , Masculino , Luz , Ratones Endogámicos C57BL , Letargo/fisiología , Regulación de la Temperatura Corporal/fisiología , Ritmo Circadiano/fisiología
12.
J Physiol Sci ; 74(1): 27, 2024 Apr 27.
Artículo en Inglés | MEDLINE | ID: mdl-38678189

RESUMEN

Growth and differentiation are reduced or stopped during hibernation, an energy conserving strategy in harsh seasons by lowered metabolism and body temperature. However, few studies evaluated this in a same individual using a non-invasive method. In this study, we applied a non-invasive tracking method of the nail growth throughout the hibernation period in the same hibernating animals, the Syrian hamster (Mesocricetus auratus). We found that nail growth was markedly suppressed during the hibernation period but rapidly recovered by the exit from the hibernation period. Our data suggest that nail growth was arrested during deep torpor, a hypometabolic and hypothermic state, but recovered during periodic arousal, a euthermic phase. Consistent with this, nail stem cells located in the nail matrix did not exit the cell cycle in the deep torpor. Thus, hibernation stops nail growth in a body temperature-dependent manner.


Asunto(s)
Hibernación , Animales , Hibernación/fisiología , Mesocricetus , Uñas/fisiología , Temperatura Corporal/fisiología , Masculino , Cricetinae , Letargo/fisiología , Frío
13.
J Comp Physiol B ; 194(2): 203-212, 2024 Apr.
Artículo en Inglés | MEDLINE | ID: mdl-38587619

RESUMEN

Winter energy stores are finite and factors influencing patterns of activity are important for overwintering energetics and survival. Hibernation patterns (e.g., torpor bout duration and arousal frequency) often depend on microclimate, with more stable hibernacula associated with greater energy savings than less stable hibernacula. We monitored hibernation patterns of individual big brown bats (Eptesicus fuscus; Palisot de Beauvois, 1796) overwintering in rock-crevices that are smaller, drier, and less thermally stable than most known cave hibernacula. While such conditions would be predicted to increase arousal frequency in many hibernators, we did not find support for this. We found that bats were insensitive to changes in hibernacula microclimate (temperature and humidity) while torpid. We also found that the probability of arousal from torpor remained under circadian influence, likely because throughout the winter during arousals, bats commonly exit their hibernacula. We calculated that individuals spend most of their energy on maintaining a torpid body temperature a few degrees above the range of ambient temperatures during steady-state torpor, rather than during arousals as is typical of other small mammalian hibernators. Flight appears to be an important winter activity that may expedite the benefits of euthermic periods and allow for short, physiologically effective arousals. Overall, we found that big brown bats in rock crevices exhibit different hibernation patterns than conspecifics hibernating in buildings and caves.


Asunto(s)
Quirópteros , Hibernación , Animales , Quirópteros/fisiología , Hibernación/fisiología , Estaciones del Año , Conducta Animal/fisiología , Adaptación Fisiológica , Ritmo Circadiano/fisiología , Metabolismo Energético , Masculino , Temperatura Corporal , Femenino , Temperatura , Microclima , Humedad , Nivel de Alerta/fisiología , Letargo/fisiología
14.
Cell Rep ; 43(4): 113960, 2024 Apr 23.
Artículo en Inglés | MEDLINE | ID: mdl-38507407

RESUMEN

GFRAL-expressing neurons actuate aversion and nausea, are targets for obesity treatment, and may mediate metformin effects by long-term GDF15-GFRAL agonism. Whether GFRAL+ neurons acutely regulate glucose and energy homeostasis is, however, underexplored. Here, we report that cell-specific activation of GFRAL+ neurons using a variety of techniques causes a torpor-like state, including hypothermia, the release of stress hormones, a shift from glucose to lipid oxidation, and impaired insulin sensitivity, glucose tolerance, and skeletal muscle glucose uptake but augmented glucose uptake in visceral fat. Metabolomic analysis of blood and transcriptomics of muscle and fat indicate alterations in ketogenesis, insulin signaling, adipose tissue differentiation and mitogenesis, and energy fluxes. Our findings indicate that acute GFRAL+ neuron activation induces endocrine and gluco- and thermoregulatory responses associated with nausea and torpor. While chronic activation of GFRAL signaling promotes weight loss in obesity, these results show that acute activation of GFRAL+ neurons causes hypothermia and hyperglycemia.


Asunto(s)
Glucosa , Hipotermia , Náusea , Neuronas , Letargo , Animales , Neuronas/metabolismo , Náusea/metabolismo , Hipotermia/metabolismo , Letargo/fisiología , Glucosa/metabolismo , Ratones , Masculino , Músculo Esquelético/metabolismo , Ratones Endogámicos C57BL , Insulina/metabolismo , Resistencia a la Insulina , Transducción de Señal
15.
Curr Biol ; 34(4): 923-930.e5, 2024 02 26.
Artículo en Inglés | MEDLINE | ID: mdl-38325375

RESUMEN

Thirteen-lined ground squirrels (Ictidomys tridecemlineatus) hibernate for several months each winter without access to water,1 but the mechanisms that maintain fluid homeostasis during hibernation are poorly understood. In torpor, when body temperature (TB) reaches 4°C, squirrels decrease metabolism, slow heart rate, and reduce plasma levels of the antidiuretic hormones arginine vasopressin (AVP) and oxytocin (OXT).1 Squirrels spontaneously undergo interbout arousal (IBA) every 2 weeks, temporarily recovering an active-like metabolism and a TB of 37°C for up to 48 h.1,2 Despite the low levels of AVP and OXT during torpor, profound increases in blood pressure and heart rate during the torpor-IBA transition are not associated with massive fluid loss, suggesting the existence of a mechanism that protects against diuresis at a low TB. Here, we demonstrate that the antidiuretic hormone release pathway is activated by hypothalamic supraoptic nucleus (SON) neurons early in the torpor-arousal transition. SON neuron activity, dense-core vesicle release from the posterior pituitary, and plasma hormone levels all begin to increase before TB reaches 10°C. In vivo fiber photometry of SON neurons from hibernating squirrels, together with RNA sequencing and c-FOS immunohistochemistry, confirms that SON is electrically, transcriptionally, and translationally active to monitor blood osmolality throughout the dynamic torpor-arousal transition. Our work emphasizes the importance of the antidiuretic pathway during the torpor-arousal transition and reveals that the neurophysiological mechanism that coordinates the hormonal response to retain fluid is active at an extremely low TB, which is prohibitive for these processes in non-hibernators.


Asunto(s)
Hibernación , Letargo , Animales , Hibernación/fisiología , Letargo/fisiología , Sciuridae/fisiología , Secuencia de Bases
16.
J Therm Biol ; 120: 103792, 2024 Feb.
Artículo en Inglés | MEDLINE | ID: mdl-38403496

RESUMEN

Small birds and mammals face similar energetic challenges, yet use of torpor to conserve energy while resting is considered less common among birds, especially within the most specious order Passeriformes. We conducted the first study to record the natural thermoregulatory physiology of any species from the family Hirundinidae, which we predicted would use torpor because of their specialised foraging by aerial pursuit of flying insects, that are less active during cold or windy weather. We used temperature telemetry on wild-living welcome swallows (Hirundo neoxena, 13 to 17 g) and found that skin temperature declined during nightly resting by an average by 5 °C, from daytime minima of 41.0 ± 0.8 °C to nightly minima of 36.3 ± 0.8 °C, and by a maximum of 8 °C to a minimum recorded skin temperature of 32.0 °C. The extent of reduction in skin temperature was greater on cold nights and following windy daytime (foraging) periods. Further, we found that transmitters glued directly to the skin between feather tracts (i.e., an apterium) provided a less variable and probably also more accurate reflection of body temperature than transmitters applied over closely trimmed feathers. A moderate decrease in skin temperature, equivalent to shallow torpor, would provide energy savings during rest. Yet, deeper torpor was not observed, despite a period of extreme rainfall that presumedly decreased foraging success. Further studies are needed to understand the resting thermoregulatory energetics of swallows under different environmental conditions. We advocate the importance of measuring thermal biology in wild-living birds to increase our knowledge of the physiology and ecological importance of torpor among passerine birds.


Asunto(s)
Passeriformes , Golondrinas , Letargo , Animales , Temperatura Corporal , Regulación de la Temperatura Corporal/fisiología , Letargo/fisiología , Temperatura , Passeriformes/fisiología , Metabolismo Energético/fisiología , Mamíferos
17.
J Comp Physiol B ; 194(1): 95-104, 2024 Feb.
Artículo en Inglés | MEDLINE | ID: mdl-38170253

RESUMEN

Mus musculus enters a torpid state in response to caloric restriction in sub-thermoneutral ambient temperatures. This torpid state is characterized by an adaptive and controlled decrease in metabolic rate, heart rate, body temperature, and activity. Previous research has identified the paraventricular nucleus (PVN) within the hypothalamus, a region containing oxytocin neurons, as a location that is active during torpor onset. We hypothesized that oxytocin neurons within the PVN are part of this neural circuit and that activation of oxytocin neurons would deepen and lengthen torpor bouts. We report that activation of oxytocin neurons alone is not sufficient to induce a torpor-like state in the fed mouse, with no significant difference in body temperature or heart rate upon activation of oxytocin neurons. However, we found that activation of oxytocin neurons prior to the onset of daily torpor both deepens and lengthens the subsequent bout, with a 1.7 ± 0.4 °C lower body temperature and a 135 ± 32 min increase in length. We therefore conclude that oxytocin neurons are involved in the neural circuitry controlling daily torpor in the mouse.


Asunto(s)
Hibernación , Letargo , Ratones , Animales , Ayuno , Oxitocina , Letargo/fisiología , Temperatura Corporal/fisiología , Neuronas/fisiología , Hibernación/fisiología
18.
PLoS One ; 18(11): e0293971, 2023.
Artículo en Inglés | MEDLINE | ID: mdl-37930992

RESUMEN

Djungarian hamsters are small rodents that show pronounced physiological acclimations in response to changes in photoperiod, and unfavorable environmental conditions such as reduced food availability and low external temperature. These include substantial adjustments, such as severe body weight loss and the use of daily torpor. Torpor is a state of decreased physiological activity in eutherms, usually marked by low metabolic rate and a reduced body temperature. In this study, we investigated the effects of photoperiodic acclimation and food deprivation on systemic iron metabolism in Djungarian hamsters. Our study illustrates the association between liver iron levels and the incidence of torpor expression during the course of the experiment. Moreover, we show that both, acclimation to short photoperiods and long-term food restriction, associated with iron sequestration in the liver. This effect was accompanied with hypoferremia and mild reduction in the expression of principal iron-hormone, hepcidin. In addition to iron, the levels of manganese, selenium, and zinc were increased in the liver of hamsters under food restriction. These findings may be important factors for regulating physiological processes in hamsters, since iron and other trace elements are essential for many metabolic and physiological processes.


Asunto(s)
Hipotermia , Letargo , Cricetinae , Animales , Phodopus/fisiología , Estaciones del Año , Letargo/fisiología , Fotoperiodo , Ayuno
19.
Curr Biol ; 33(24): 5381-5389.e4, 2023 12 18.
Artículo en Inglés | MEDLINE | ID: mdl-37992720

RESUMEN

Endotherms can survive low temperatures and food shortage by actively entering a hypometabolic state known as torpor. Although the decrease in metabolic rate and body temperature (Tb) during torpor is controlled by the brain, the specific neural circuits underlying these processes have not been comprehensively elucidated. In this study, we identify the neural circuits involved in torpor regulation by combining whole-brain mapping of torpor-activated neurons, cell-type-specific manipulation of neural activity, and viral tracing-based circuit mapping. We find that Trpm2-positive neurons in the preoptic area and Vgat-positive neurons in the dorsal medial hypothalamus are activated during torpor. Genetic silencing shows that the activity of either cell type is necessary to enter the torpor state. Finally, we show that these cells receive projections from the arcuate and suprachiasmatic nucleus and send projections to brain regions involved in thermoregulation. Our results demonstrate an essential role of hypothalamic neurons in the regulation of Tb and metabolic rate during torpor and identify critical nodes of the torpor regulatory network.


Asunto(s)
Hipotálamo , Letargo , Hipotálamo/fisiología , Letargo/fisiología , Área Preóptica , Núcleo Supraquiasmático , Encéfalo
20.
Pflugers Arch ; 475(10): 1149-1160, 2023 10.
Artículo en Inglés | MEDLINE | ID: mdl-37542567

RESUMEN

Hibernation enables many species of the mammalian kingdom to overcome periods of harsh environmental conditions. During this physically inactive state metabolic rate and body temperature are drastically downregulated, thereby reducing energy requirements (torpor) also over shorter time periods. Since blood cells reflect the organism´s current condition, it was suggested that transcriptomic alterations in blood cells mirror the torpor-associated physiological state. Transcriptomics on blood cells of torpid and non-torpid Djungarian hamsters and QIAGEN Ingenuity Pathway Analysis (IPA) revealed key target molecules (TMIPA), which were subjected to a comparative literature analysis on transcriptomic alterations during torpor/hibernation in other mammals. Gene expression similarities were identified in 148 TMIPA during torpor nadir among various organs and phylogenetically different mammalian species. Based on TMIPA, IPA network analyses corresponded with described inhibitions of basic cellular mechanisms and immune system-associated processes in torpid mammals. Moreover, protection against damage to the heart, kidney, and liver was deduced from this gene expression pattern in blood cells. This study shows that blood cell transcriptomics can reflect the general physiological state during torpor nadir. Furthermore, the understanding of molecular processes for torpor initiation and organ preservation may have beneficial implications for humans in extremely challenging environments, such as in medical intensive care units and in space.


Asunto(s)
Hibernación , Letargo , Cricetinae , Humanos , Animales , Phodopus/fisiología , Hibernación/genética , Transcriptoma , Letargo/fisiología , Mamíferos/fisiología
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