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.     

Angularis oculi vein blood flow modulates the magnitude but not the control of selective brain cooling in sheep

To investigate the role of the angularis oculi vein (AOV) in selective brain cooling (SBC), we measured brain and carotid blood temperatures in six adult female Dorper sheep. Halfway through the study, a section of the AOV, just caudal to its junction with the dorsal nasal vein, was extirpated on both sides. Before and after AOV surgery, the sheep were housed outdoors at 21-22°C and were exposed in a climatic chamber to daytime heat (40°C) and water deprivation for 5 days. In sheep outdoors, SBC was significantly lower after the AOV had been cut, with its 24-h mean reduced from 0.25 to 0.01°C (t(5) = 3.06, P = 0.03). Carotid blood temperature also was lower (by 0.28°C) at all times of day (t(5) = 3.68, P = 0.01), but the pattern of brain temperature was unchanged. The mean threshold temperature for SBC was not different before (38.85 ± 0.28°C) and after (38.85 ± 0.39°C) AOV surgery (t(5) =0.00, P = 1.00), but above the threshold, SBC magnitude was about twofold less after surgery. SBC after AOV surgery also was less during heat exposure and water deprivation. However, SBC increased progressively by the same magnitude (0.4°C) over the period of water deprivation, and return of drinking water led to rapid cessation of SBC in sheep before and after AOV surgery. We conclude that the AOV is not the only conduit for venous drainage contributing to SBC in sheep and that, contrary to widely held opinion, control of SBC does not involve changes in the vasomotor state of the AOV.     

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.     

Adaptive heterothermy and selective brain cooling in arid-zone mammals

Adaptive heterothermy and selective brain cooling are regarded as important thermal adaptations of large arid-zone mammals. Adaptive heterothermy, a process which reduces evaporation by storing body heat, ought to be enhanced by ambient heat load and by water deficit, but most mammals studied fail to show at least one of those attributes. Selective brain cooling, the reduction of brain temperature below arterial blood temperature, is most evident in artiodactyls, which possess a carotid rete, and traditionally has been considered to protect the brain during hyperthermia. The development of miniature ambulatory data loggers for recording body temperature allows the temperatures of free-living wild mammals to be measured in their natural habitats. All the African ungulates studied so far, in their natural habitats, do not exhibit adaptive heterothermy. They have low-amplitude nychthemeral rhythms of temperature, with mean body temperature over the night exceeding that over the day. Those with carotid retes (black wildebeest, springbok, eland) employ selective brain cooling but zebra, without a rete, do not. None of the rete ungulates, however, seems to employ selective brain cooling to prevent the brain overheating during exertional hyperthermia. Rather, they use it at rest, under moderate heat load, we believe in order to switch body heat loss from evaporative to non-evaporative routes.     

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.     

Activity, blood temperature and brain temperature of free-ranging springbok

We used miniature data loggers to record temperature and activity in free-ranging springbok (Antidorcas marsupialis) naturally exposed to severe nocturnal cold and moderate diurnal heat. The animals were active throughout the day and night, with short rests; the intensity of activity increased during daylight. Arterial blood temperature, averaged over many days, exhibited a circadian rhythm with amplitude <1 °C, but with a wide range which resulted from sporadic rapid deviations of body temperature. Peak blood temperature occurred after sunset. Environmental thermal loads had no detectable effect on blood temperature, even though globe temperature varied by >10 °C from day to day and >20 °C within a day. Brain temperature increased approximately linearly with blood temperature but with a slope <1, so that selective brain cooling tended to be activated at high body temperature, but without a precise threshold for the onset of brain cooling. Low activity attenuated selective brain cooling and high activity abolished it, even at high brain temperature. Our results support the concept that selective brain cooling serves to modulate thermoregulation rather than to protect the brain against heat injury. Accepted: 7 January 1997     

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     

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.     

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.     

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.     

The carotid rete and artiodactyl success

Since the Eocene, the diversity of artiodactyls has increased while that of perissodactyls has decreased. Reasons given for this contrasting pattern are that the evolution of a ruminant digestive tract and improved locomotion in artiodactyls were adaptively advantageous in the highly seasonal post-Eocene climate. We suggest that evolution of a carotid rete, a structure highly developed in artiodactyls but absent in perissodactyls, was at least as important. The rete confers an ability to regulate brain temperature independently of body temperature. The net effect is that in hot ambient conditions artiodactyls are able to conserve energy and water, and in cold ambient conditions they are able to conserve body temperature. In perissodactyls, brain and body temperature change in parallel and thermoregulation requires abundant food and water to warm/cool the body. Consequently, perissodactyls occupy habitats of low seasonality and rich in food and water, such as tropical forests. Conversely, the increased thermoregulatory flexibility of artiodactyls has facilitated invasion of new adaptive zones ranging from the Arctic Circle to deserts and tropical savannahs.     

Increased osmolality of conscious water-deprived rats supports arterial pressure and sympathetic activity via a brain action

To test the hypothesis that high osmolality acts in the brain to chronically support mean arterial pressure (MAP) and lumbar sympathetic nerve activity (LSNA), the osmolality of blood perfusing the brain was reduced in conscious water-deprived and water-replete rats by infusion of hypotonic fluid via bilateral nonoccluding intracarotid catheters. In water-deprived rats, the intracarotid hypotonic infusion, estimated to lower osmolality by approximately 2%, decreased MAP by 9+/-1 mmHg and LSNA to 86+/-7% of control; heart increased by 25+/-8 beats per minute (bpm) (all P<0.05). MAP, LSNA, and heart rate did not change when the hypotonic fluid was infused intravenously. The intracarotid hypotonic fluid infusion was also ineffective in water-replete rats. Prior treatment with a V1 vasopressin antagonist did not alter the subsequent hypotensive and tachycardic effects of intracarotid hypotonic fluid infusion in water-deprived rats. In summary, acute decreases in osmolality of the carotid blood of water-deprived, but not water-replete, rats decreases MAP and LSNA and increases heart rate. These data support the hypothesis that the elevated osmolality induced by water deprivation acts via a region perfused by the carotid arteries, presumably the brain, to tonically increase MAP and LSNA and suppress heart rate.     

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.     

Mechanisms of water economy in lactating Ethiopian Somali goats during repeated cycles of intermittent watering

We investigated the physiological and behavioural strategies by which lactating Ethiopian Somali goats endure repeated periods of water deprivation. The experiment lasted for 32 days and was divided into four periods of 8 days each. Measurements were taken during the first 4 days in each period. Seven does (W1) were watered once daily and seven does (W4) were watered once every 4th day. Rectal temperature was taken at 0800 and 1715 h. Blood samples were taken in the evening and milk samples in the morning. The goats were on pasture between 0900 to 1215 h and 1315 to 1630 h with behaviour recorded every 5 min. The does were supplemented with 300 g of concentrates per head per day. Plasma and milk osmolality were determined by freezing point depression. Plasma total protein was measured on a TS refractometer. Plasma vasopressin concentrations were analysed by radio-immunoassay. The mean daily water intake of W1 was 1897 ml compared with the calculated mean of 1075 ml in W4 (P < 0.001). The mean diurnal variation of the rectal temperature was 3.5°C in both groups. Afternoon rectal temperature in W4 during period 1 was higher than that in the W1 on the days of water deprivation (P < 0.05). With repeated periods, plasma osmolality in W4 increased less over the days of water deprivation. It was 336, 321, 311 and 306 mosm/l on the 4th day at periods 1, 2, 3 and 4, respectively. The corresponding vasopressin concentrations were 10.0, 9.2, 4.2 and 4.4 pmol/l. Total plasma protein concentration during period 1 on days 3 and 4 were higher in W4 than in W1 (P < 0.01). During the subsequent periods, it did not increase more in W4 compared with W1, but it was lower in W4 on the days after watering. W4 milk production decreased by 22% compared with W1 in all periods. With increasing days of water deprivation, the W4 goats spent less time in the sun, grazed shorter time and frequently ate cactus (Opuntia ficus-indica) as compared with W1. Results suggested that dehydrated lactating Ethiopian Somali goats economised on water by diurnal variations of rectal temperature, storing water in the extracellular fluid, by changing behaviour at grazing and by decreasing milk production.     

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.     

Regional blood flow changes in response to thermal stimulation of the brain and spinal cord in the Pekin duck

Summary In conscious Pekin ducks, carotid and sciatic blood flows, respiratory rate, core and skin temperatures were measured during selective thermal stimulations of the spinal cord and rostral brain stem in thermoneutral (20 °C) and warm (32 °C) ambient conditions.At thermoneutral ambient temperature selective heating of the spinal cord by 2–3 °C (to 43–44 °C) increased the carotid blood flow by 138% and the sciatic blood flow by 46%. Increase in blood flows was correlated with increased breathing rate and beak and web skin temperatures.Selective cooling of the spinal cord at warm ambient temperatures and panting reduced the blood flow in both arteries and decreased the breathing rate.Heating or cooling of the brain stem showed generally very weak but otherwise similar responses as thermal stimulation of the spinal cord. In one duck out of six there was a marked effect on regional blood flow during brain stimulation.The results show that thermal stimulation of the spinal cord exerts a marked influence on regional blood flow important in thermoregulation, whereas the lower brain stem shows only a weak thermosensitivity, and stimulation caused only small cardiovascular changes of no major consequence in thermoregulation.     

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.     

A test of biochemical symmorphosis in a heterothermic tissue: bluefin tuna white muscle

Selective brain cooling (SBC) is defined as a brain temperature cooler than the temperature of arterial blood from the trunk. Surrogate measures of arterial blood temperature have been used in many published studies on SBC. The use of a surrogate for arterial blood temperature has the potential to confound proper identification of SBC. We have measured brain, carotid blood, and rectal temperatures in conscious sheep exposed to 40, 22, and 5 degrees C. Rectal temperature was consistently higher than arterial blood temperature. Brain temperature was consistently cooler than rectal temperature during all exposures. Brain temperature only fell below carotid blood temperature during the final few hours of 40 degrees C exposure and not at all during the 5 degrees C exposure. Consequently, using rectal temperature as a surrogate for arterial blood temperature does not provide a reliable indication of the status of the SBC effector. We also show that rapid suppression of SBC can result if the animals are disturbed.     

Water intake induced by water deprivation in the quail,Coturnix coturnix japonica

Mechanisms inducing drinking after water deprivation, and mechanisms terminating drinking after rehydration, were investigated in the quail, Coturnix coturnix japonica. 1. Water intake was induced after 4 h of water deprivation, and the amount of water drunk increased in proportion to the period of water deprivation. Drinking occurred immediately after deprivation. Drinking occurred immediately after deprived birds were given access to water, and continued for periods proportional to the period of water deprivation. 2. Plasma angiotensin II concentration increased, as did plasma osmolality and Na+ concentration, and blood volume decreased after water deprivation. The increase in plasma angiotensin II concentration and decrease in blood volume occurred soon after the start of water deprivation, whereas plasma osmolality and Na+ concentration did not increase until at least 4 h after the start of water deprivation. 3. These results indicate that extracellular dehydration and angiotensin II are responsible for the significant drinking that follows 4 h of water deprivation, and that cellular dehydration is also involved in the stimulation of drinking that occurs after longer periods of water deprivation. 4. Plasma osmolality and Na+ concentration in birds deprived of water for 48 h quickly returned to normal levels after the birds were allowed access to water. Plasma angiotensin II levels and blood volume also approached the values measured prior to water deprivation. However, the rate and degree of restoration of normal values were reduced, and normal values were not restored even after 1.5 h or rehydration when drinking terminated.(ABSTRACT TRUNCATED AT 250 WORDS)     

Water deprivation in lactating rats: Changes in nucleolar dry mass of paraventricular and supraoptic neurones

Summary The separation of function between and within the paraventricular (PV) and supraoptic (SO) nuclei was investigated in the rat. Nucleolar dry mass of PV and SO neurones was measured to detect increased synthetic activity after water deprivation for 3 days, lactation for 8 days or water deprivation during days 5 to 8 of lactation. Lactation or water deprivation increased nucleolar dry mass in both PV and SO neurones. These stimuli caused similar nucleolar changes in PV neurones, but water deprivation caused greater changes in SO neurones than lactation. The effects of lactation and water deprivation were additive for both SO and PV neurones. Furosemide was used to intensify the dehydration stimulus to determine whether such intensification could have caused the greater nucleolar changes when lactation and water deprivation were combined. For PV neurones this was not the case, but remained a possibility for SO neurones. Measurements of serum osmolality in the experimental groups were ranked as follows: water deprivation + furosemide > lactation + water deprivation > water deprivation > lactation = virgin control. Loss of body weight was similar in the first two groups but less during water deprivation alone. Although milk yield fell, milk was obtained by the litters of lactating animals throughout the period of water deprivation.