Many mammals use adaptive heterothermy (e.g., torpor, hibernation) to reduce metabolic demands of maintaining high body temperature ( T b ). Torpor is typically characterized by coordinated declines in T b and metabolic rate (MR) followed by active rewarming. Most hibernators experience periods of euthermy between bouts of torpor during which homeostatic processes are restored. In contrast, the common tenrec, a basoendothermic Afrotherian mammal, hibernates without interbout arousals and displays extreme flexibility in T b and MR. We investigated the molecular basis of this plasticity in tenrecs by profiling the liver proteome of animals that were active or torpid with high and more stable T b (∼32°C) or lower T b (∼14°C). We identified 768 tenrec liver proteins, of which 50.9% were differentially abundant between torpid and active animals. Protein abundance was significantly more variable in active cold and torpid compared with active warm animals, suggesting poor control of proteostasis. Our data suggest that torpor in tenrecs may lead to mismatches in protein pools due to poor coordination of anabolic and catabolic processes. We propose that the evolution of endothermy leading to a more realized homeothermy of boreoeutherians likely led to greater coordination of homeostatic processes and reduced mismatches in thermal sensitivities of metabolic pathways.
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Activation of oxytocinergic neurons enhances torpor in mice
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 tempera- ture 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.
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- Award ID(s):
- 1652060
- NSF-PAR ID:
- 10488010
- Publisher / Repository:
- Springer Nature
- Date Published:
- Journal Name:
- Journal of Comparative Physiology B
- ISSN:
- 0174-1578
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract Torpor, or a regulated drop in body temperature and metabolic rate, allows animals to inhabit energetically costly environments, but among torpor‐using species, we have a poor understanding of how plasticity in torpor use relates to the experienced environment.
To better understand the ecology of daily torpor, we completed the largest study to date on the intraspecific variation of daily torpor use in hummingbirds by exposing 149 individuals of two hummingbird species to ambient or experimentally cooled temperatures in a field setting.
The smaller species, a latitudinal migrant, used daily torpor frequently under ambient conditions. The larger species, an elevational migrant, also used daily torpor regularly, but further increased the frequency of daily torpor use when experiencing colder temperatures and prior to migration—indicating a facultative adaptation.
To place our results within a broader phylogenetic context, we combined our experimental results with a meta‐analysis, including 31 species and all major hummingbird clades, and found a broad taxonomic pattern in which smaller hummingbirds are more likely to use daily torpor than their larger counterparts. Smaller hummingbirds may be physiologically constrained, requiring nearly obligate daily torpor use, while larger hummingbirds are physiologically more flexible and can facultatively respond to changing environmental conditions.
Our results reveal how physiological traits, such as the frequency and depth of daily torpor, can provide a mechanism to understand how hummingbird species have established and persisted across broad environmental gradients.
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Synopsis Variability in body temperature is now recognized to be widespread among whole-body endotherms with homeothermy being the exception rather than the norm. A wide range of body temperature patterns exists in extant endotherms, spanning from strict homeothermy, to occasional use of torpor, to deep seasonal hibernation with many points in between. What is often lost in discussions of heterothermy in endotherms are the benefits of variations in body temperature outside of torpor. Endotherms that do not use torpor can still obtain extensive energy and water savings from varying levels of flexibility in normothermic body temperature regulation. Flexibility at higher temperatures (heat storage or facultative hyperthermia) can provide significant water savings, while decreases at cooler temperatures, even outside of torpor, can lower the energetic costs of thermoregulation during rest. We discuss the varying uses of the terms heterothermy, thermolability, and torpor to describe differences in the amplitude of body temperature cycles and advocate for a broader use of the term “heterothermy” to include non-torpid variations in body temperature.
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The stress response necessitates an immediate boost in vital physiological functions from their homeostatic operation to an elevated emergency response. However, the neural mechanisms underlying this state-dependent change remain largely unknown. Using a combination of in vivo and ex vivo electrophysiology with computational modeling, we report that corticotropin releasing hormone (CRH) neurons in the paraventricular nucleus of the hypothalamus (PVN), the effector neurons of hormonal stress response, rapidly transition between distinct activity states through recurrent inhibition. Specifically, in vivo optrode recording shows that under non-stress conditions, CRH PVN neurons often fire with rhythmic brief bursts (RB), which, somewhat counterintuitively, constrains firing rate due to long (~2 s) interburst intervals. Stressful stimuli rapidly switch RB to continuous single spiking (SS), permitting a large increase in firing rate. A spiking network model shows that recurrent inhibition can control this activity-state switch, and more broadly the gain of spiking responses to excitatory inputs. In biological CRH PVN neurons ex vivo, the injection of whole-cell currents derived from our computational model recreates the in vivo-like switch between RB and SS, providing direct evidence that physiologically relevant network inputs enable state-dependent computation in single neurons. Together, we present a novel mechanism for state-dependent activity dynamics in CRH PVN neurons.more » « less
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Objective We examine the spatiotemporal dynamics of neural activity and its correlates in heart rate and its variability (HR/HRV) during a fatiguing visuospatial working memory task.
Background The neural and physiological drivers of fatigue are complex, coupled, and poorly understood. Investigations that combine the fidelity of neural indices and the field-readiness of physiological measures can facilitate measurements of fatigue states in operational settings.
Method Sixteen healthy adults, balanced by sex, completed a 60-minute fatiguing visuospatial working memory task. Changes in task performance, subjective measures of effort and fatigue, cerebral hemodynamics, and HR/HRV were analyzed. Peak brain activation, functional and effective connections within relevant brain networks were contrasted against spectral and temporal features of HR/HRV.
Results Task performance elicited increased neural activation in regions responsible for maintaining working memory capacity. With the onset of time-on-task effects, resource utilization was seen to increase beyond task-relevant networks. Over time, functional connections in the prefrontal cortex were seen to weaken, with changes in the causal relationships between key regions known to drive working memory. HR/HRV indices were seen to closely follow activity in the prefrontal cortex.
Conclusion This investigation provided a window into the neurophysiological underpinnings of working memory under the time-on-task effect. HR/HRV was largely shown to mirror changes in cortical networks responsible for working memory, therefore supporting the possibility of unobtrusive state recognition under ecologically valid conditions.
Applications Findings here can inform the development of a fieldable index for cognitive fatigue.
