Selective Brain Cooling in Mammals and Birds.

Abstract

The term selective brain cooling (SBC) refers to the lowering of brain temperature, either locally or as a whole, below arterial blood temperature. SBC has been reported to occur in laboratory experiments on many mammalian and avian species and was often seen as a mechanism serving to protect the brain, which was more or less intuitively supposed to be more susceptible to thermal damage than other organs of the body were. So far, however, no evidence has been found showing that brain tissues are less tolerant of elevated temperatures than other tissues are [1,2], and recent studies have cast great doubt on the validity of the protection concept of SBC (see below). This article reviews the present knowledge of the thermal and nonthermal factors conducive to the development of SBC. It is organized in four major sections. The first deals with species in which the presence of a carotid rete provides a well-defined anatomical structure capable of cooling all arterial blood destined for the brain, and thus cooling the brain as a whole. The second section concerns nonhuman mammals in which the carotid rete is either rudimentarily developed or missing; in these species SBC is very likely to be restricted to certain regions of the brain. The situation in humans deserves a separate section. On the one hand, no specialized heat exchanger like the carotid rete is available to cool the arterial blood before it enters the large brain, but on the other a sweating scalp and face may provide heat sinks of sizable capacity for cooling regions of the brain near its outer Key words: selective brain cooling, brain temperature, carotid rete, mammals, birds.Abstract: Artiodactyls and felids have a carotid rete that can cool the blood destined for the brain and consequently the brain itself if the cavernous sinus receives cool blood returning from the nose. This condition is usually fulfilled in resting and moderately hyperthermic animals. During severe exercise hyperthermia, however, the venous return from the nose bypasses the cavernous sinus so that brain cooling is suppressed. This is irreconcilable with the assumption that the purpose of selective brain cooling (SBC) is to protect the brain from thermal damage. Alternatively, SBC is seen as a mechanism engaging the thermoregulatory system in a water-saving economy mode in which evaporative heat loss is inhibited by the effects of SBC on brain temperature sensors. In nonhuman mammals that do not have a carotid rete, no evidence exists of wholebrain cooling. However, the surface of the cavernous sinus is in close contact with the base of the brain and is the likely source of unregulated regional cooling of the rostral brain stem in some species. In humans, the cortical regions next to the inner surface of the cranium are very likely to receive some regional cooling via the scalp-sinus pathway, and the rostral base of the brain can be cooled by conduction to the nearby respiratory tract; mechanisms capable of cooling the brain as a whole have not been found. Studies using conventiona...

Variability in brain and arterial blood temperatures in free-ranging ostriches in their natural habitat

“…For many years it was thought that selective brain cooling, in mammals or birds, functions to protect the apparently vulnerable brain from thermal damage during heat stress (for a review, see Mitchell et al, 1987). However, recent studies of free-ranging mammals in their natural habitat have yielded data that are incompatible with that concept (for reviews, see Jessen, 2001;Mitchell et al, 2002). Rather than being a process that favours protection of the brain, our current view is that selective brain cooling plays a role in whole body thermoregulation (Jessen, 2001;Mitchell et al, 2002).…”

“…It is widely held that birds employ selective brain cooling, analogous to that in mammals. Most studies have shown that brain temperature in birds consistently is lower than core body temperature over a wide range of ambient and body temperatures (for a review, see Arad, 1990;Jessen, 2001). The anatomical structure thought to be responsible for this brain cooling is the ophthalmic rete, a network of extracranial arteries developed from the external ophthalmic branch of the internal carotid artery and closely associated with veins carrying cool blood away from the buccopharyngeal surfaces, beak and eyes (Richards, 1967;Kilgore et al, 1973).…”

“…In most mammals, therefore, brain temperature changes in parallel with carotid blood temperature but, because of its high metabolic rate, exceeds the temperature of arterial blood by 0.2-0.5°C (Hayward and Baker, 1969). However, some mammals, particularly artiodactyls and felids, are able to lower brain temperature below carotid blood temperature, a process termed selective brain cooling (for reviews, see Jessen, 2001;Mitchell et al, 2002). In these mammals, selective brain cooling is facilitated by the carotid rete, a bilateral network of intertwining arteries in the main arterial supply to the brain, situated on either side of the pituitary body within cool venous lakes derived from veins draining the nasal mucosa (Gillilan, 1974;Simoens et al, 1987).…”

Orexinergic bouton density is lower in the cerebral cortex of cetaceans compared to artiodactyls

“…Cetaceans are under constant, significant thermal pressures due to their aquatic environment (Manger, 2006), whereas the artiodactyls have mechanisms in place to prevent overheating (Kuhnen, 1997;Jessen, 1998Jessen, , 2001Mitchell et al, 2002).…”

Thermoregulatory consequences of salt loading in the lizard, Pogona vitticeps

“…A mechanism called 'selective brain cooling' (SBC) has been described to be activated in mammals (Caputa et al, 1976;McConaghy et al, 1995;Jessen, 2001;Mitchell et al, 2002) when they face water stress. SBC is defined as brain temperature lower than arterial blood temperature (IUPS Thermal Commission, 2001), which is achieved by carotid blood cooling on its ascent to the brain (Willmer et al, 2005).…”