2010 Carl Ludwig Distinguished Lectureship of the APS Neural Control and Autonomic Regulation Section: Central neural pathways for thermoregulatory cold defense

Central neural circuits orchestrate the homeostatic repertoire to maintain body temperature during environmental temperature challenges and to alter body temperature during the inflammatory response. This review summarizes the research leading to a model representing our current understanding of the neural pathways through which cutaneous thermal receptors alter thermoregulatory effectors: the cutaneous circulation for control of heat loss, and brown adipose tissue, skeletal muscle, and the heart for thermogenesis. The activation of these effectors is regulated by parallel but distinct, effector-specific core efferent pathways within the central nervous system (CNS) that share a common peripheral thermal sensory input. The thermal afferent circuit from cutaneous thermal receptors includes neurons in the spinal dorsal horn projecting to lateral parabrachial nucleus neurons that project to the medial aspect of the preoptic area. Within the preoptic area, warm-sensitive, inhibitory output neurons control heat production by reducing the discharge of thermogenesis-promoting neurons in the dorsomedial hypothalamus. The rostral ventromedial medulla, including the raphe pallidus, receives projections form the dorsomedial hypothalamus and contains spinally projecting premotor neurons that provide the excitatory drive to spinal circuits controlling the activity of thermogenic effectors. A distinct population of warm-sensitive preoptic neurons controls heat loss through an inhibitory input to raphe pallidus sympathetic premotor neurons controlling cutaneous vasoconstriction. The model proposed for central thermoregulatory control provides a platform for further understanding of the functional organization of central thermoregulation.     

Physiological mechanisms of thermoregulation in reptiles: a review

The thermal dependence of biochemical reaction rates means that many animals regulate their body temperature so that fluctuations in body temperature are small compared to environmental temperature fluctuations. Thermoregulation is a complex process that involves sensing of the environment, and subsequent processing of the environmental information. We suggest that the physiological mechanisms that facilitate thermoregulation transcend phylogenetic boundaries. Reptiles are primarily used as model organisms for ecological and evolutionary research and, unlike in mammals, the physiological basis of many aspects in thermoregulation remains obscure. Here, we review recent research on regulation of body temperature, thermoreception, body temperature set-points, and cardiovascular control of heating and cooling in reptiles. The aim of this review is to place physiological thermoregulation of reptiles in a wider phylogenetic context. Future research on reptilian thermoregulation should focus on the pathways that connect peripheral sensing to central processing which will ultimately lead to the thermoregulatory response.     

Ontogeny of thermoregulation in precocial birds

The aim of this paper is to summarise the results of earlier experiments on thermoregulation and heat balance in birds, to present new results concerning thermoregulation during the perinatal period in precocial embryos and to develop a model of the ontogeny of thermoregulation over the whole lifespan of birds. The ontogeny of thermoregulation in precocial birds is characterised by three phases with different efficiency of the system. In the prenatal phase, all control elements of the thermoregulatory system can function, but the efficiency of the system is low. It is postulated that endothermic reactions during the prenatal period do not have a proximate (immediate), but rather an ultimate influence on the efficiency of thermoregulation. They may support adaptivity to expected environmental conditions and may be involved in epigenetic adaptation processes. During the early postnatal phase, the thermoregulatory system develops and matures. Summit metabolism and resting metabolic rate and their thermoregulatory set points increase. Preferred temperature is significantly different during different behavioural activities. The phase of full-blown homeothermy starts at approximately the 10th day of life. It is characterised by an activation order of thermoregulatory control elements and by secondary chemical thermoregulation. The influence of thermal and non-thermal climatic factors on heat production and heat loss may be described by mathematical models.     

An alternative heat-budget model relevant to heat transfer in fishes and its practical use for detecting their physiological thermoregulation

Previous studies have detected activity-independent fish thermoregulation or conservation mechanisms by applying a mathematical model to body temperature data collected with electronic tags. This model is inadequate, due to its inability to separate quantitatively the effects of physiological thermoregulation from those of physical thermal inertia (the low thermal conductance of the body). In this paper, we have developed an alternative mathematical model that separates these effects. We have then applied it to published electronic tagging data from a large, free-swimming blue shark, Prinoca glauca, to demonstrate physiological thermoregulation. Resultant estimated body-temperature curves indicate that the fish could adjust its whole-body heat-transfer coefficient by changes in arterial blood flow over a range of one order of magnitude. To look at the physical effect on thermoregulation, body temperature for a smaller hypothetical fish was calculated. The estimated temperature was significantly lower than the actual value, indicating that an ectothermic fish like the blue shark cannot achieve physiological thermoregulation without assistance from thermal inertia. In addition, the blue shark returns to cooler depths without recovering its body temperature to the normal surface-temperature level, indicating that this behavior contributes to maximization of the rate of body-temperature recovery. Furthermore, the model indicated that the time for body-temperature recovery is irrelevant to the initial body temperature. Thus, the model made it possible to quantify thermophysiological manipulation. In addition, it was also useful in the comparison of thermoregulatory mechanisms between fishes of different sizes or species.     

A hot lunch for herbivores: physiological effects of elevated temperatures on mammalian feeding ecology

Mammals maintain specific body temperatures (T_b) across a broad range of ambient temperatures. The energy required for thermoregulation ultimately comes from the diet, and so what animals eat is inextricably linked to thermoregulation. Endothermic herbivores must balance energy requirements and expenditure with complicated thermoregulatory challenges from changing thermal, nutritional and toxicological environments. In this review we provide evidence that plant‐based diets can influence thermoregulation beyond the control of herbivores, and that this can render them susceptible to heat stress. Notably, herbivorous diets often require specialised digestive systems, are imbalanced, and contain plant secondary metabolites (PSMs). PSMs in particular are able to interfere with the physiological processes responsible for thermoregulation, for example by uncoupling mitochondrial oxidative phosphorylation, binding to thermoreceptors, or because the pathways required to detoxify PSMs are thermogenic. It is likely, therefore, that increased ambient temperatures due to climate change may have greater and more‐specific impacts on herbivores than on other mammals, and that managing internal and external heat loads under these conditions could drive changes in feeding ecology.     

Seasonal effects of sleep deprivation on thermoregulatory responses in a hot environment

Effects of sleep deprivation and season on thermoregulation during 60 min. of leg-bathing (water temperature of 42 degrees C, air temperature of 30 degrees C, and relative humidity of 70%) were studied in eight men who completed all 4 experiments for normal sleep and sleep deprivation in summer and winter. Rectal temperature (T(re)), skin temperature, total body sweating rate (M(sw-t)), local sweating rate on the back (M(sw-back)) and forearm (M(sw-forearm)), and skin blood flow on the back (SBF(back)) and forearm (SBF(forearm)) were measured. The changes in T(re) (DeltaT(re)) were smaller (P<0.05) for sleep deprivation than for normal sleep regardless of the season. This decrease in DeltaT(re) was significant only in summer (P<0.05). Mean skin temperature (T(mean of)(sk)) was higher (P<0.05) for sleep deprivation than for normal sleep regardless of the season. M(sw-t) was smaller (P<0.05) for sleep deprivation than for normal sleep regardless of season, although M(sw-back) and M(sw-forearm) were similar. SBF(back) and SBF(forearm) tended to be higher for sleep deprivation than normal sleep. The sensitivity of SBF to T(re) was higher (P<0.05) for sleep deprivation than for normal sleep. These data indicate that seasonal differences in thermoregulation were small because of morning time. Sleep deprivation increased dry heat loss and restrained T(re) rise, in spite of decreased sweating rate.     

Thermoregulation and diurnal rhythms in 1-week-old rat pups

This paper reviews the ontogeny of thermoregulation and diurnal rhythmicity in rats. Additionally, original data are presented that indicate the emergence of an endogenous circadian core temperature rhythm during the first postnatal week. Despite neurological immaturity, newborn rats display autonomic and behavioral thermoregulatory responses within 24 h of birth. Their "biological clock" is already running before birth. The thermal environment of pups changes cyclically owing to diurnal variations in maternal behavior, but the core temperatures of 1-week-old pups huddling in the absence of the dam also show marked diurnal fluctuations. Five- to 8-day-old lean Zucker rat pups artificially reared in the absence of 24-h cycles of ambient temperature and food intake show diurnal changes in core temperature similar to those in huddling mother-reared pups. Diurnal core temperature changes, evident only when regulatory effectors are not overwhelmed, are one of the first self-maintained diurnal rhythms to appear. Because thermoregulation and circadian rhythmicity both appear before maturation of the neural networks believed to be critical for their control in adult animals, studying the immature rat might increase our understanding of the control of these processes in the more complex mature central nervous system.     

Extending the cost-benefit model of thermoregulation: high-temperature environments

The classic cost-benefit model of ectothermic thermoregulation compares energetic costs and benefits, providing a critical framework for understanding this process (Huey and Slatkin 1976 ). It considers the case where environmental temperature (T(e)) is less than the selected temperature of the organism (T(sel)), and it predicts that, to minimize increasing energetic costs of thermoregulation as habitat thermal quality declines, thermoregulatory effort should decrease until the lizard thermoconforms. We extended this model to include the case where T(e) exceeds T(sel), and we redefine costs and benefits in terms of fitness to include effects of body temperature (T(b)) on performance and survival. Our extended model predicts that lizards will increase thermoregulatory effort as habitat thermal quality declines, gaining the fitness benefits of optimal T(b) and maximizing the net benefit of activity. Further, to offset the disproportionately high fitness costs of high T(e) compared with low T(e), we predicted that lizards would thermoregulate more effectively at high values of T(e) than at low ones. We tested our predictions on three sympatric skink species (Carlia rostralis, Carlia rubrigularis, and Carlia storri) in hot savanna woodlands and found that thermoregulatory effort increased as thermal quality declined and that lizards thermoregulated most effectively at high values of T(e).     

Reactivite thermique de la peau scrotale chez l’homme

Although the existence of heat exchange between the testicular artery and the adjacent veins is well known, it may be insufficient to maintain the lower temperature of the testis. In order to investigate the role of the scrotum in testicular thermoregulation, the dynamics of scrotal and other skin temperatures was studied in relation to thermal stress. The results of this study revealed that the scrotal skin exhibited a greater thermal inertia than did other skin areas. This finding may be due to modifications in scrotal blood flow patterns as temperature increased, as well as changes in the scrotal surface area. Other possible thermoregulatory factors may include the evaporation of sweat from the scrotum. In conclusion, there seems to be a complex collection of mechanisms, rather than a single specific mechanism, regulating testicular temperature.     

Are black-box models of thermoregulatory control obsolete? The importance of borrowed knowledge.

Black-box models of thermoregulatory control have gained increasing importance in describing the properties of the biological thermostat and in devising working hypotheses for further experimental analysis. Incorporation of knowledge acquired independently from the systems analysis approach into black-box models of thermoregulation has proven useful in improving their predictive ability. The pieces of "borrowed knowledge" from independent analysis which are currently utilized in devising models of homeothermic thermoregulation comprise: the proportional control property of the biological thermostat, the Sherringtonian principles of synaptic interaction, the multiple input control of thermoregulatory effectors with differential input-effector coupling, the lack of significant thermosensory contribution from the hypothalamus in birds, the existence of warm and cold receptors and the thermal characteristics of their responses, and the Q10-type temperature dependence of temperature signal transmission within the central nervous system. Consideration of these pieces of borrowed knowledge has resulted in black-box models of temperature regulation in which explicit set-point terms are avoided.     

Shade as a thermoregulatory resource for captive chimpanzees

In nature, the thermoregulatory strategies of species have evolved in response to the environmental conditions in which they live. Primates display extensive behavioural flexibility but few have examined the role of this behavioural flexibility with regard to thermoregulation. Chimpanzees, under free-living conditions, utilise natural vertical light/thermal gradients in rainforest canopies as a means of thermoregulation, moving along the gradient to maintain homoeostasis. In contrast, captive chimpanzees are often housed at latitudes outside their natural range under conditions that do not allow for this natural behavioural thermoregulation. We investigated the use of shade by captive chimpanzees as a behavioural thermoregulatory strategy at the Johannesburg Zoo, South Africa. We performed behavioural observations over the austral winter/spring period on a group of captive chimpanzees recording their behaviour in relation to shade use. Despite experiencing temperatures in Johannesburg below or just within their thermoneutral zone, chimpanzees consistently spent more time in shade than in direct sun. This pattern of shade use was most pronounced for the hotter midday period than for other times, was not dependent on the overall availability of shade within the enclosure and was not predicted by mean daily or hourly temperatures nor thermal maxima or minima. Instead, ultraviolet radiation and humidity levels appear to predict the observed patterns of shade utilisation and these findings suggest that chimpanzees in captivity adopt a sun-avoidance strategy, possibly as a result of the rapid heat gain associated with their dark skin and pelage. The findings suggest that chimpanzees are flexible when responding to the thermal challenges associated with housing outside of their natural environment.     

An application of randomization for detecting evidence of thermoregulation in timber rattlesnakes (Crotalus horridus) from northwest Arkansas

Most reptiles maintain their body temperatures within normal functional ranges through behavioral thermoregulation. Under some circumstances, thermoregulation may be a time-consuming activity, and thermoregulatory needs may impose significant constraints on the activities of ectotherms. A necessary (but not sufficient) condition for demonstrating thermoregulation is a difference between observed body temperature distributions and available operative temperature distributions. We examined operative and body temperature distributions of the timber rattlesnake (Crotalus horridus) for evidence of thermoregulation. Specifically, we compared the distribution of available operative temperatures in the environment to snake body temperatures during August and September. Operative temperatures were measured using 48 physical models that were randomly deployed in the environment and connected to a Campbell CR-21X data logger. Body temperatures (n=1,803) were recorded from 12 radiotagged snakes using temperature-sensitive telemetry. Separate randomization tests were conducted for each hour of day within each month. Actual body temperature distributions differed significantly from operative temperature distributions at most time points considered. Thus, C. horridus exhibits a necessary (but not sufficient) condition for demonstrating thermoregulation. However, unlike some desert ectotherms, we found no compelling evidence for thermal constraints on surface activity. Randomization may prove to be a powerful technique for drawing inferences about thermoregulation without reliance on studies of laboratory thermal preference.     

The effect of carbon dioxide enrichment on apparent stem respiration from <Emphasis Type="Italic">Pinus taeda</Emphasis> L. is confounded by high levels of soil carbon dioxide

Huey and Slatkin’s (Q Rev Biol 51:363–384, 1976) cost–benefit model of lizard thermoregulation predicts variation in thermoregulatory strategies (from active thermoregulation to thermoconformity) with respect to the costs and benefits of the thermoregulatory behaviour and the thermal quality of the environment. Although this framework has been widely employed in correlative field studies, experimental tests aiming to evaluate the model are scarce. We conducted laboratory experiments to see whether the common lizard Zootoca vivipara, an active and effective thermoregulator in the field, can alter its thermoregulatory behaviour in response to differences in perceived predation risk and food supply in a constant thermal environment. Predation risk and food supply were represented by chemical cues of a sympatric snake predator and the lizards’ food in the laboratory, respectively. We also compared males and postpartum females, which have different preferred or “target” body temperatures. Both sexes thermoregulated actively in all treatments. We detected sex-specific differences in the way lizards adjusted their accuracy of thermoregulation to the treatments: males were less accurate in the predation treatment, while no such effects were detected in females. Neither sex reacted to the food treatment. With regard to the two main types of thermoregulatory behaviour (activity and microhabitat selection), the treatments had no significant effects. However, postpartum females were more active than males in all treatments. Our results further stress that increasing physiological performance by active thermoregulation has high priority in lizard behaviour, but also shows that lizards can indeed shift their accuracy of thermoregulation in response to costs with possible immediate negative fitness effects (i.e. predation-caused mortality).     

Thermoregulatory behavior and orientation preference in bearded dragons

The regulation of body temperature is a critical function for animals. Although reliant on ambient temperature as a heat source, reptiles, and especially lizards, make use of multiple voluntary and involuntary behaviors to thermoregulate, including postural changes in body orientation, either toward or away from solar sources of heat. This thermal orientation may also result from a thermoregulatory drive to maintain precise control over cranial temperatures or a rostrally-driven sensory bias. The purpose of this work was to examine thermal orientation behavior in adult and neonatal bearded dragons (Pogona vitticeps), to ascertain its prevalence across different life stages within a laboratory situation and its interaction with behavioral thermoregulation. Both adult and neonatal bearded dragons were placed in a thermal gradient and allowed to voluntarily select temperatures for up to 8 h to observe the presence and development of a thermoregulatory orientation preference. Both adult and neonatal dragons displayed a non-random orientation, preferring to face toward a heat source while achieving mean thermal preferences of ~ 33–34 °C. Specifically, adult dragons were more likely to face a heat source when at cooler ambient temperatures and less likely at warmer temperatures, suggesting that orientation behavior counter-balances local selected temperatures but contributes to their thermoregulatory response. Neonates were also more likely to select cooler temperatures when facing a heat source, but required more experience before this orientation behavior emerged. Combined, these results demonstrate the importance of orientation to behavioral thermoregulation in multiple life stages of bearded dragons.     

Elderly bioheat modeling: changes in physiology,thermoregulation, and blood flow circulation

A bioheat model for the elderly was developed focusing on blood flow circulatory changes that influence their thermal response in warm and cold environments to predict skin and core temperatures for different segments of the body especially the fingers. The young adult model of Karaki et al. (Int J Therm Sci 67:41–51, 2013) was modified by incorporation of the physiological thermoregulatory and vasomotor changes based on literature observations of physiological changes in the elderly compared to young adults such as lower metabolism and vasoconstriction diminished ability, skin blood flow and its minimum and maximum values, the sweating values, skin fat thickness, as well as the change in threshold parameter related to core or skin temperatures which triggers thermoregulatory action for sweating, maximum dilatation, and maximum constriction. The developed model was validated with published experimental data for elderly exposure to transient and steady hot and cold environments. Predicted finger skin temperature, mean skin temperature, and core temperature were in agreement with published experimental data at a maximum error less than 0.5 °C in the mean skin temperature. The elderly bioheat model showed an increase in finger skin temperature and a decrease in core temperature in cold exposure while it showed a decrease in finger skin temperature and an increase in core temperature in hot exposure.     

Seasonal acclimation of preferred body temperatures improves the opportunity for thermoregulation in newts

Seasonal acclimation and thermoregulation represent major components of complex thermal strategies by which ectotherms cope with the heterogeneity of their thermal environment. Some ectotherms possess the acclimatory capacity to shift seasonally their thermoregulatory behavior, but the frequent use of constant acclimation temperatures during experiments and the lack of information about thermal heterogeneity in the field obscures the ecological relevance of this plastic response. We examined the experimentally induced seasonal acclimation of preferred body temperatures (T(p)) in alpine newts Ichthyosaura (formerly Triturus) alpestris subjected to a gradual increase in acclimation temperature from 5°C during the winter to a constant 15°C or diel fluctuations between 10° and 20°C during the spring/summer. Both the mean and range of T(p) followed the increase in mean acclimation temperature without the influence of diel temperature fluctuations. The direction and magnitude of this acclimatory capacity has the potential to increase the time window available for thermoregulation. Although thermoregulation and thermal acclimation are often considered as separate but coadapted adjustments to thermal heterogeneity, their combined response is employed by newts to tackle seasonal variation in a thermoregulatory-challenging aquatic environment.     

Thermoregulatory effects of central injection of noradrenaline in the new-born columbian ground squirrel (Spermophilus columbianus)

1. 1.Effects of centrally injected noradrenaline (NA) into new-born (12–300 h. post-partum) Columbian ground squirrels (Spermophilus columbianus) were studied to provide comparative data on ontogeny of the thermoregulatory pathways in a hibernating species.

2. 2.At warm ambient temperatures (32–34°C, similar to nest temperature), NA increased heat production (47–92%). rectal temperature (0.27–1.73°C), and axillary temperature (0.59–1.92°C). Peak magnitudes of heat production increased with increasing age on a per unit weight basis.

3. 3.At lower temperatures (28–31°C), NA had no effect on heat production.

4. 4.The data indicate that metabolic and thermal responses to NA in neonates of hibernating species are comparable (e.g. rabbit. guinea pig) or different (e.g. lamb) from those observed in neonates of non-hibernating species.

Behavioral thermoregulation by hypoxic rats.

To address whether a shift in hypothalamic thermal setpoint might be a significant factor in induction of hypoxic hypothermia, behavioral thermoregulation was examined in 7 female Sprague-Dawley rats implanted with radiotelethermometers for deep body temperature (Tb) measurement in a thermocline during normoxia (PO2 = 125 torr) and hypoxia (PO2 = 60 torr). Normoxic rats (TNox) selected a mean ambient temperature of 19.7 +/- 1.4 (SE) degrees C and maintained Tb at 37.0 +/- 0.2 degrees C. Hypoxic rats selected a significantly higher ambient temperature (THox = 28.6 +/- 2.2 degrees C) but maintained Tb significantly lower at 35.5 +/- 0.3 degrees C. Without a thermal gradient (ambient temperature = 25 degrees C), Tb during hypoxia was 35.4 +/- 0.4 degrees C. The maintenance of a lower body temperature during hypoxia through behavioral thermoregulation despite having warmer temperatures available supports the hypothesis that the thermoregulatory setpoint of hypoxic rats is shifted to promote thermoregulation at a lower Tb, effectively reducing oxygen demand when oxygen supply is limited.     

Rhythmic 24 h Variation of Core Body Temperature and Locomotor Activity in a Subterranean Rodent (Ctenomys aff. knighti), the Tuco-Tuco

The tuco-tuco Ctenomys aff. knighti is a subterranean rodent which inhabits a semi-arid area in Northwestern Argentina. Although they live in underground burrows where environmental cycles are attenuated, they display robust, 24 h locomotor activity rhythms that are synchronized by light/dark cycles, both in laboratory and field conditions. The underground environment also poses energetic challenges (e.g. high-energy demands of digging, hypoxia, high humidity, low food availability) that have motivated thermoregulation studies in several subterranean rodent species. By using chronobiological protocols, the present work aims to contribute towards these studies by exploring day-night variations of thermoregulatory functions in tuco-tucos, starting with body temperature and its temporal relationship to locomotor activity. Animals showed daily, 24 h body temperature rhythms that persisted even in constant darkness and temperature, synchronizing to a daily light/dark cycle, with highest values occurring during darkness hours. The range of oscillation of body temperature was slightly lower than those reported for similar-sized and dark-active rodents. Most rhythmic parameters, such as period and phase, did not change upon removal of the running wheel. Body temperature and locomotor activity rhythms were robustly associated in time. The former persisted even after removal of the acute effects of intense activity on body temperature by a statistical method. Finally, regression gradients between body temperature and activity were higher in the beginning of the night, suggesting day-night variation in thermal conductance and heat production. Consideration of these day-night variations in thermoregulatory processes is beneficial for further studies on thermoregulation and energetics of subterranean rodents.     

Single neuron studies and their usefulness in understanding thermoregulation

Electrophysiological studies of hypothalamic thermosensitive neurons have been conducted for the past 25 years. These studies have greatly improved our understanding of the neural control of thermoregulation. They have added a sense of reality to black-box models, and they have fostered the development of neuronal models having a major effect on the predictions and conclusions made in thermoregulatory studies. Neuron studies not only provide an understanding of the synaptic and cellular basis of thermosensitivity, but they also permit morphological identifications of neurons and their pathways. Neuron studies have identified sites at which central temperature information is integrated with peripheral temperature information. In addition, these experiments provide functional explanations for the types of integration observed. Neuron studies also provide explanations for the central actions of a variety of neurochemicals important in thermoregulation. Finally, neuronal specificity studies have aided in restoring the view that thermoregulation is part of a complex homeostatic system in which various regulatory systems interact with each other.