Abstract
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.
Highlights
Several mammal species, artiodactyls, use the carotid rete to lower hypothalamic temperature below arterial blood temperature, a processPLOS ONE | DOI:10.1371/journal.pone.0115514 February 12, 2015Selective Brain Cooling Conserves Body Water
During the first two days, when water was freely available, carotid blood and brain temperatures followed similar profiles and brain temperature frequently exceeded carotid blood temperature. These patterns changed following the removal of water, with brain temperature clearly decoupling from carotid blood temperature
Peak carotid blood and peak brain temperature increased with continued water deprivation (Fig. 1A), the increase in carotid blood temperature was larger than that of brain temperature, leading to increasing separation of the two temperatures and enhanced selective brain cooling
Summary
Artiodactyls (such as sheep, goats and antelope), use the carotid rete to lower hypothalamic temperature below arterial blood temperature, a process. When dehydrated, Bedouin goats [15] and Dorper sheep [8] showed enhanced selective brain cooling, both in terms of magnitude and the frequency of use. Arabian oryx had a higher magnitude, higher frequency of use, and lower threshold of selective brain cooling in dry environments than when they had free access to water, despite ambient temperatures being similar [9]. These studies provide circumstantial evidence in support of the notion that selective brain cooling serves a water conservation function. We hypothesized that if selective brain cooling does play a role in water conservation it would lead to reduced water turnover in those sheep showing greater selective brain cooling
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