Guttural pouches, brain temperature and exercise in horses

Selective brain cooling (SBC) is defined as the lowering of brain temperature below arterial blood temperature. Artiodactyls employ a carotid rete, an anatomical heat exchanger, to cool arterial blood shortly before it enters the brain. The survival advantage of this anatomy traditionally is believed to be a protection of brain tissue from heat injury, especially during exercise. Perissodactyls such as horses do not possess a carotid rete, and it has been proposed that their guttural pouches serve the heat-exchange function of the carotid rete by cooling the blood that traverses them, thus protecting the brain from heat injury. We have tested this proposal by measuring brain and carotid artery temperature simultaneously in free-living horses. We found that despite evidence of cranial cooling, brain temperature increased by about 2.5 degrees C during exercise, and consistently exceeded carotid temperature by 0.2-0.5 degrees C. We conclude that cerebral blood flow removes heat from the brain by convection, but since SBC does not occur in horses, the guttural pouches are not surrogate carotid retes.     

The contribution of carotid rete variability to brain temperature variability in sheep in a thermoneutral environment

The degree of variability in the temperature difference between the brain and carotid arterial blood is greater than expected from the presumed tight coupling between brain heat production and brain blood flow. In animals with a carotid rete, some of that variability arises in the rete. Using thermometric data loggers in five sheep, we have measured the temperature of arterial blood before it enters the carotid rete and after it has perfused the carotid rete, as well as hypothalamic temperature, every 2 min for between 6 and 12 days. The sheep were conscious, unrestrained, and maintained at an ambient temperature of 20-22 degrees C. On average, carotid arterial blood and brain temperatures were the same, with a decrease in blood temperature of 0.35 degrees C across the rete and then an increase in temperature of the same magnitude between blood leaving the rete and the brain. Rete cooling of arterial blood took place at temperatures below the threshold for selective brain cooling. All of the variability in the temperature difference between carotid artery and brain was attributable statistically to variability in the temperature difference across the rete. The temperature difference between arterial blood leaving the rete and the brain varied from -0.1 to 0.9 degrees C. Some of this variability was related to a thermal inertia of the brain, but the majority we attribute to instability in the relationship between brain blood flow and brain heat production.     

Dehydration increases the magnitude of selective brain cooling independently of core temperature in sheep

By cooling the hypothalamus during hyperthermia, selective brain cooling reduces the drive on evaporative heat loss effectors, in so doing saving body water. To investigate whether selective brain cooling was increased in dehydrated sheep, we measured brain and carotid arterial blood temperatures at 5-min intervals in nine female Dorper sheep (41 +/- 3 kg, means +/- SD). The animals, housed in a climatic chamber at 23 degrees C, were exposed for nine days to a cyclic protocol with daytime heat (40 degrees C for 6 h). Drinking water was removed on the 3rd day and returned 5 days later. After 4 days of water deprivation, sheep had lost 16 +/- 4% of body mass, and plasma osmolality had increased from 290 +/- 8 to 323 +/- 9 mmol/kg (P < 0.0001). Although carotid blood temperature increased during heat exposure to similar levels during euhydration and dehydration, selective brain cooling was significantly greater in dehydration (0.38 +/- 0.18 degrees C) than in euhydration (-0.05 +/- 0.14 degrees C, P = 0.0008). The threshold temperature for selective brain cooling was not significantly different during euhydration (39.27 degrees C) and dehydration (39.14 degrees C, P = 0.62). However, the mean slope of lines of regression of brain temperature on carotid blood temperature above the threshold was significantly lower in dehydrated animals (0.40 +/- 0.31) than in euhydrated animals (0.87 +/- 0.11, P = 0.003). Return of drinking water at 39 degrees C led to rapid cessation of selective brain cooling, and brain temperature exceeded carotid blood temperature throughout heat exposure on the following day. We conclude that for any given carotid blood temperature, dehydrated sheep exposed to heat exhibit selective brain cooling up to threefold greater than that when euhydrated.     

Heterothermy in large mammals: inevitable or implemented?

Advances in biologging techniques over the past 20 years have allowed for the remote and continuous measurement of body temperatures in free‐living mammals. While there is an abundance of literature on heterothermy in small mammals, fewer studies have investigated the daily variability of body core temperature in larger mammals. Here we review measures of heterothermy and the factors that influence heterothermy in large mammals in their natural habitats, focussing on large mammalian herbivores. The mean 24 h body core temperatures for 17 species of large mammalian herbivores (>10 kg) decreased by ～1.3°C for each 10‐fold increase in body mass, a relationship that remained significant following phylogenetic correction. The degree of heterothermy, as measured by the 24 h amplitude of body core temperature rhythm, was independent of body mass and appeared to be driven primarily by energy and water limitations. When faced with the competing demands of osmoregulation, energy acquisition and water or energy use for thermoregulation, large mammalian herbivores appear to relax the precision of thermoregulation thereby conserving body water and energy. Such relaxation may entail a cost in that an animal moves closer to its thermal limits for performance. Maintaining homeostasis requires trade‐offs between regulated systems, and homeothermy apparently is not accorded the highest priority; large mammals are able to maintain optimal homeothermy only if they are well nourished, hydrated, and not compromised energetically. We propose that the amplitude of the 24 h rhythm of body core temperature provides a useful index of any compromise experienced by a free‐living large mammal and may predict the performance and fitness of an animal.     

Selective Brain Cooling Reduces Water Turnover in Dehydrated Sheep

In artiodactyls, arterial blood destined for the brain can be cooled through counter-current heat exchange within the cavernous sinus via a process called selective brain cooling. We test the hypothesis that selective brain cooling, which results in lowered hypothalamic temperature, contributes to water conservation in sheep. Nine Dorper sheep, instrumented to provide measurements of carotid blood and brain temperature, were dosed with deuterium oxide (D₂O), exposed to heat for 8 days (40◦C for 6-h per day) and deprived of water for the last five days (days 3 to 8). Plasma osmolality increased and the body water fraction decreased over the five days of water deprivation, with the sheep losing 16.7% of their body mass. Following water deprivation, both the mean 24h carotid blood temperature and the mean 24h brain temperature increased, but carotid blood temperature increased more than did brain temperature resulting in increased selective brain cooling. There was considerable inter-individual variation in the degree to which individual sheep used selective brain cooling. In general, sheep spent more time using selective brain cooling, and it was of greater magnitude, when dehydrated compared to when they were euhydrated. We found a significant positive correlation between selective brain cooling magnitude and osmolality (an index of hydration state). Both the magnitude of selective brain cooling and the proportion of time that sheep spent selective brain cooling were negatively correlated with water turnover. Sheep that used selective brain cooling more frequently, and with greater magnitude, lost less water than did conspecifics using selective brain cooling less efficiently. Our results show that a 50kg sheep can save 2.6L of water per day (~60% of daily water intake) when it employs selective brain cooling for 50% of the day during heat exposure. We conclude that selective brain cooling has a water conservation function in artiodactyls.     

Absence of selective brain cooling in unrestrained baboons exposed to heat

To test whether baboons are capable of implementing selective brain cooling, we measured, every 5 min, the temperature in their hypothalamus, carotid arterial bloodstream, and abdominal cavity. The baboons were unrestrained and exposed to 22 degrees C for 7 days and then to a cyclic environment with 15 degrees C at night and 35 degrees C during the day for a further 7 days. During the latter 7 days some of the baboons also were exposed to radiant heat during the day. For three days, during heat exposure, water was withheld. At no time was the hypothalamus cooler than carotid arterial blood, despite brain temperatures above 40 degrees C. With little variation, the hypothalamus was consistently 0.5 degrees C warmer than arterial blood. At high body temperatures, the hypothalamus was sometimes cooler than the abdomen. Abdominal temperature was more variable than arterial blood and tended to exceed arterial blood temperature at higher body temperatures. Hypothalamic temperature cooler than a warm abdomen is not evidence for selective brain cooling. In species that can implement selective brain cooling, the brain is most likely to be cooler than carotid arterial blood when an animal is hyperthermic, during heat exposure, and also dehydrated and undisturbed by human presence. When we exposed baboons to high ambient temperatures while they were water deprived and undisturbed, they never implemented selective brain cooling. We conclude that baboons cannot implement selective brain cooling and can find no convincing evidence that any primate species can do so.     

Tropical bats counter heat by combining torpor with adaptive hyperthermia

Many tropical mammals are vulnerable to heat because their water budget limits the use of evaporative cooling for heat compensation. Further increasing temperatures and aridity might consequently exceed their thermoregulatory capacities. Here, we describe two novel modes of torpor, a response usually associated with cold or resource bottlenecks, as efficient mechanisms to counter heat. We conducted a field study on the Malagasy bat Macronycteris commersoni resting in foliage during the hot season, unprotected from environmental extremes. On warm days, the bats alternated between remarkably short micro-torpor bouts and normal resting metabolism within a few minutes. On hot days, the bats extended their torpor bouts over the hottest time of the day while tolerating body temperatures up to 42.9°C. Adaptive hyperthermia combined with lowered metabolic heat production from torpor allows higher heat storage from the environment, negates the need for evaporative cooling and thus increases heat tolerance. However, it is a high-risk response as the torpid bats cannot defend body temperature if ambient temperature increases above a critical/lethal threshold. Torpor coupled with hyperthermia and micro-torpor bouts broaden our understanding of the basic principles of thermal physiology and demonstrate how mammals can perform near their upper thermal limits in an increasingly warmer world.     

REM sleep related increase in brain temperature: a physiologic problem

The roles of metabolic heat production, arterial blood flow and temperature in the genesis of the brain temperature increase related to REM sleep occurrence in several mammalian species are discussed on the basis of available experimental evidence. The experimental data show that only changes in arterial blood flow and temperature consistently underlie the rise in brain temperature in presence (cat) or absence (rabbit) of the carotid rete. The alteration of cardiovascular regulation in REM sleep is the remote cause of such rise. The proximate causes are decrease in carotid blood supply and increase in vertebral blood supply to the brain and related depression of systemic and selective brain cooling.     

Temperature difference between the body core and arterial blood supplied to the brain during hyperthermia or hypothermia in humans

 A vascular heat transfer model is developed to simulate temperature decay along the carotid arteries in humans, and thus, to evaluate temperature differences between the body core and arterial blood supplied to the brain. Included are several factors, including the local blood perfusion rate, blood vessel bifurcation in the neck, and blood vessel pairs on both sides of the neck. The potential for cooling blood in the carotid artery by countercurrent heat exchange with the jugular veins and by radial heat conduction to the neck surface was estimated. Cooling along the common and internal carotid arteries was calculated to be up to 0.87 °C during hyperthermia by high environmental temperatures or muscular exercise. This model was also used to evaluate the feasibility of lowering the brain temperature effectively by placing ice pads on the neck and head surface or by wearing cooling garments during hypothermia treatment for brain injury or other medical conditions. It was found that a 1.1 °C temperature drop along the carotid arteries is possible when the neck surface is cooled to 0 °C. Thus, the body core temperature may not be a good indication of the brain temperature during hyperthermia or hypothermia. Received: 10 January 2002 / Accepted: 7 May 2002 This research was supported by a UMBC Summer Faculty Fellowship.     

Selective brain cooling is impaired in REM sleep.

There are systemic and selective mechanisms for brain cooling in mammals. The difference between the temperatures of the vertebral and the carotid blood perfusing the brain is determined by selective heat loss and is, therefore, a quantitative indicator of the intensity of selective brain cooling. Across the wake-sleep cycle systemic and selective brain cooling are affected by state-dependent autonomic changes. In REM sleep selective brain cooling is impaired.     

Non-thermal signals govern selective brain cooling in pigs

We used implanted miniature data loggers and fine thermistors to measure arterial blood and brain temperatures in four female pigs, to a resolution of 0.04 °C, every 5 min, for 4 weeks. Within that period, pigs were exposed on different days, and in random order, to a cold (5 °C) or hot (38 °C) environment. In the thermoneutral environment of the pigs' home pens, brain temperature was usually lower than blood temperature. Such selective brain cooling was absent for 2 days after surgery, during handling and transport stress, and on waking. The magnitude of selective brain cooling was greatest when pigs were sleeping and body temperatures were low, and was smallest, or even absent, during hyperthermia and natural fever. Our results showed that selective brain cooling was present in pigs, but there was no clear relationship between blood temperature and the magnitude of selective brain cooling. Instead, the degree of selective brain cooling in pigs was governed by non-thermal factors, especially those associated with high sympathetic nervous system activity. Our results further support the concept that selective brain cooling does not serve to protect the brain from thermal damage during heat stress. Accepted: 14 September 1999     

Competition for cool nasal blood between trunk and brain in hyperthermic goats

An influence of brain and trunk temperatures controlled independently of each other by means of artificial heat exchangers, on the intensity of natural selective brain cooling (SBC) was studied in 6 conscious goats. Intensity of SBC was markedly enhanced by increasing brain temperature. On the other hand, a rise of trunk temperature with the cerebral temperature clamped at 39 degrees C or 40 degrees C, reduced SBC intensity in spite of a simultaneous increase in the respiratory evaporative heat loss. When brain temperature was clamped at 41 degrees C, the magnitude of SBC was essentially independent of trunk temperature. These results suggest that during hyperthermia a competition exists between trunk and brain for cool nasal blood.     

Thermoregulatory anatomy of pronghorn (Antilocapra americana)

We have found that pronghorn (Antilocapra americana) use external heat exchange with the environment and internal heat exchange between the carotid artery rete and cavernous venous sinus blood to regulate body temperature. Now we have investigated the relationship between the histological structure of the skin, cephalic veins, and carotid rete–cavernous sinus system and the physiological mechanisms pronghorn use, and whether their thermoregulatory anatomy has adaptive advantages. We harvested tissue samples of skin, three veins (i.e., angularis oculi vein, dorsal nasal vein, and facial vein), and the carotid rete–cavernous sinus system from four pronghorn, two culled in summer and two in winter, and examined each histologically. The three veins had the typical structure of veins with large lumina and thin walls. The carotid rete consisted of small (0.1–0.5 mm) arterioles with a density of ~10/mm², intertwined with veins (~2/mm²), enclosed within the cavernous sinus; a structure ideal for heat exchange. We concluded that the main function of the dorsal nasal and facial veins is to return cold blood to the body to effect whole body cooling. The cavernous sinus is supplied with warm blood by the palatine veins in winter and cold blood by the deep facial veins in summer, an arrangement different to that in other ungulates, such as sheep, in which the angularis oculi vein supplies the cavernous sinus. Pronghorn skin is richly supplied with blood vessels that facilitate convective heat loss in summer. In winter, the number of coarse and fine hairs per square millimeter increases more than in European deer to form a thick pelage that minimizes heat loss. In summer, the pelage is shed because hair follicles involute. Unlike in other ungulates, pronghorn skin has little adipose tissue. The number of apocrine glands increases in winter rather than in summer. We concluded that the glands have a reproductive/social function rather than a thermoregulatory one. In summary, our study shows that the thermoregulatory anatomy is consistent with our physiological data and has adaptive advantages that help explain the survival of pronghorn in an arid habitat characterized by extreme temperature variation and sparse vegetation.     

Brain thermal inertia,but no evidence for selective brain cooling,in free-ranging western grey kangaroos (<Emphasis Type="Italic">Macropus fuliginosus</Emphasis>)

Marsupials reportedly can implement selective brain cooling despite lacking a carotid rete. We measured brain (hypothalamic) and carotid arterial blood temperatures every 5 min for 5, 17, and 63 days in spring in three free-living western grey kangaroos. Body temperature was highest during the night, and decreased rapidly early in the morning, reaching a nadir at 10:00. The highest body temperatures recorded occurred sporadically in the afternoon, presumably associated with exercise. Hypothalamic temperature consistently exceeded arterial blood temperature, by an average 0.3°C, except during these afternoon events when hypothalamic temperature lagged behind, and was occasionally lower than, the simultaneous arterial blood temperature. The reversal in temperatures resulted from the thermal inertia of the brain; changes in the brain to arterial blood temperature difference were related to the rate of change of arterial blood temperature on both heating and cooling (P < 0.001 for all three kangaroos). We conclude that these data are not evidence for active selective brain cooling in kangaroos. The effect of thermal inertia on brain temperature is larger than might be expected in the grey kangaroo, a discrepancy that we speculate derives from the unique vascular anatomy of the marsupial brain.     

Posthatching development of the rete ophthalmicum in relation to brain temperature of mallard ducks (anas platyrhynchos)

In posthatching mallard ducks (Anas platyrhynchos), brain cooling improves with growth. To determine whether this may be correlated with growth-related changes in morphology of the rete ophthalmicum, we studied the development of this rete in immature mallards from hatching to 29 days of age. We found that the number of arteries and veins was fixed at hatching. The rete continued to grow, however, in length and vessel diameter during body and brain growth. The vascular surface area for heat exchange in the rete therefore also increased with body and brain mass. The increase in retial heat-exchange area was faster than the simultaneous increase in brain mass. The increase in body-to-brain temperature difference (delta T) described previously occurred nearly in direct proportion to heat-exchange area, such that the ratio of delta T to exchange area was nearly constant at about 0.1 degrees C per mm2 during growth. It is concluded that the increase in heat-exchange area of the rete ophthalmicum plays a major role in the development of brain cooling capacity of posthatching ducks.     

Does size matter? Comparison of body temperature and activity of free-living Arabian oryx (<Emphasis Type="Italic">Oryx leucoryx</Emphasis>) and the smaller Arabian sand gazelle (<Emphasis Type="Italic">Gazella subgutturosa marica</Emphasis>) in the Saudi desert

Heterothermy, a variability in body temperature beyond the normal limits of homeothermy, is widely viewed as a key adaptation of arid-adapted ungulates. However, desert ungulates with a small body mass, i.e. a relatively large surface area-to-volume ratio and a small thermal inertia, are theoretically less likely to employ adaptive heterothermy than are larger ungulates. We measured body temperature and activity patterns, using implanted data loggers, in free-ranging Arabian oryx (Oryx leucoryx, ±70 kg) and the smaller Arabian sand gazelle (Gazella subgutturosa marica, ±15 kg) inhabiting the same Arabian desert environment, at the same time. Compared to oryx, sand gazelle had higher mean daily body temperatures (F _1,6 = 47.3, P = 0.0005), higher minimum daily body temperatures (F _1,6 = 42.6, P = 0.0006) and higher maximum daily body temperatures (F _1,6 = 11.0, P = 0.02). Despite these differences, both species responded similarly to changes in environmental conditions. As predicted for adaptive heterothermy, maximum daily body temperature increased (F _1,6 = 84.0, P < 0.0001), minimum daily body temperature decreased (F _1,6 = 92.2, P < 0.0001), and daily body temperature amplitude increased (F _1,6 = 97.6, P < 0.0001) as conditions got progressively hotter and drier. There were no species differences in activity levels, however, both gazelle and oryx showed a biphasic or crepuscular rhythm during the warm wet season but shifted to a more nocturnal rhythm during the hot dry season. Activity was attenuated during the heat of the day at times when both species selected cool microclimates. These two species of Arabian ungulates employ heterothermy, cathemerality and shade seeking very similarly to survive the extreme, arid conditions of Arabian deserts, despite their size difference.     

Hibernation and non-shivering thermogenesis in the Hottentot golden mole (<Emphasis Type="Italic">Amblysomus hottentottus longiceps</Emphasis>)

Although heterothermy (hibernation and torpor) is a common feature among mammals, there is debate over whether it is a derived or ancestral trait relative to endothermic homeothermy. Determination of the physiological characteristics of primitive mammals is central to understanding the evolution of endothermy. Moreover, evaluation of physiological mechanisms responsible for endothermic heat production [e.g. non-shivering thermogenesis (NST)] is key to understanding how early mammals responded to historical climate changes and colonised different geographical regions. Here we investigated the capacity for NST and heterothermy in the Hottentot golden mole, a basal eutherian mammal. NST was measured as the metabolic response to injections of noradrenalin and heterothermy by recording body temperature in free-ranging animals. We found that hibernation and torpor occurred and that the seasonal phenotypic adjustment of NST capacity was similar to that found in other placental mammals. Using phylogenetically independent contrasts, we compared measured values of NST with those obtained from the literature. This showed that all variation in NST was accounted for by differences in phylogeny and not zoogeography. These findings lend support to the observation that NST and heterothermy occur in the Afrotheria, the basal placental mammalian clade. Furthermore, this work suggests that heterothermy, rather than homeothermy is a plesiomorphic trait in mammals and supports the notion that NST mechanisms are phylogenetically ancient.     

Taking the heat: thermoregulation in Asian elephants under different climatic conditions

Some mammals indigenous to desert environments, such as camels, cope with high heat load by tolerating an increase in body temperature (T _b) during the hot day, and by dissipating excess heat during the cooler night hours, i.e., heterothermy. Because diurnal heat storage mechanisms should be favoured by large body size, we investigated whether this response also exists in Asian elephants when exposed to warm environmental conditions of their natural habitat. We compared daily cycles of intestinal T _b of 11 adult Asian elephants living under natural ambient temperatures (T _a) in Thailand (mean T _a ~ 30°C) and in 6 Asian elephants exposed to cooler conditions (mean T _a ~ 21°C) in Germany. Elephants in Thailand had mean daily ranges of T _b oscillations (1.15°C) that were significantly larger than in animals kept in Germany (0.51°C). This was due to both increased maximum T _b during the day and decreased minimum T _b at late night. Elephant’s minimum T _b lowered daily as T _a increased and hence entered the day with a thermal reserve for additional heat storage, very similar to arid-zone ungulates. We conclude that these responses show all characteristics of heterothermy, and that this thermoregulatory strategy is not restricted to desert mammals, but is also employed by Asian elephants.     

Effect of warm rearing on temperature regulation in resting and exercising rats

1. 1.|Hypothalamic and rectal temperatures were recorded in 8 warm-reared (wr) and in 12 warm-acclimated control rats during resting in the heat and during 30 min running under thermoneutral conditions.

2. 2.|Brain and body temperatures of wr rats were significantly higher (P < 0.001) than control rats, both in normothermia as well as in hyperthermia; at rest, and also during exercise.

3. 3.|Warm-reared rats were more tolerant to heat.

4. 4.|During normothermia a weak selective brain cooling was present in control but absent in wr rats. During hyperthermia, however, the cooling intensified in control and occurred in wr rats.

5. 5.|The main strategy of adaptation to heat in wr rats is an upward resetting of the temperature set-point and increased passivity.

ORIGINAL ARTICLE: Eyes wide shut: can hypometabolism really explain the primate colonization of Madagascar?

Aim We investigate the hypothesis that it was the capacity for torpor or hibernation that enabled the lemuriforms (and possibly other mammal groups, e.g. tenrecs and rodents) to invade Madagascar by means of over‐water dispersal. Location Madagascar, East Africa and the Mozambique Channel. Methods We consider the body weights and life‐style features of living primate taxa that employ heterothermy. Using this information as a standard for comparison, we summarize the available information on the Palaeogene strepsirrhine radiation (i.e. members of the infraorder Adapiformes, the extinct sister‐taxon to the lemuriforms, as well as putative stem lemuriforms), particularly with respect to possible trends in body weight among early, middle and late Eocene adapiforms. We discuss Eocene climatic conditions in the northern hemisphere and Africa, and assess the likelihood of adaptations for heterothermy in adapiforms. Finally, we estimate the body weights of the common ancestors to the living Lemuriformes and Lemuroidea using the method of phylogenetically independent contrasts. Results The mean body weights estimated for the early, middle and late Eocene strepsirrhine faunas remain at approximately 2 kg, outside of the range of living primates using heterothermy. The adapiforms’ appearance coincided with the ‘initial Eocene thermal maximum’, an unusually hot period of global warming, and their demise corresponded with a major cooling event coincident with the appearance of ice sheets on Antarctica. They show no evidence of having evolved adaptations that allowed them to withstand climatic deterioration. The body weights of the ancestral lemuriform and ancestral lemuroid are of a similar order to the mean body weight estimated for the adapiforms, i.e. approximately 1.8 and 2.1 kg, respectively. Main conclusions The available evidence argues against the widespread use of heterothermy by adapiforms. The adapiform–lemuriform divergence may have been the result of the lemuriforms adapting to the drier and more seasonal environments that characterized the African Eocene, and this suite of adaptations may have included the use of heterothermy, but there is as yet no substantial evidence to confirm the presence of either group on the continent prior to c. 40 Ma. The estimated body weights of the common lemuriform and lemuroid ancestors are well outside the size range of living mammals that employ heterothermy. We conclude that the hypothesis that it was the ability to use heterothermy that enabled the strepsirrhines, and not the haplorhines, to invade Madagascar, is unlikely. Alternative explanations for this anomaly should be sought.