Scaling of the brain and the eye cooling system in birds: A morphometric analysis of the <i>Rete ophthalmicum</i>

Midtgård, Uffe

doi:10.1002/jez.1402250204

Cited by 57 publications

(51 citation statements)

References 22 publications

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“…The periorbital region was chosen as this provided the only region of the body that was uninsulated and is associated with a rich intermingled network of small blood vessels, the rete ophthalmicum that can affect the heat loss from the eye 31 . The fast frame rate of the thermal videoing technique was able to show a drop in eye-region temperature of approximately 2 °C in 10 sec followed by a subsequent rise in temperature to within 0.5 °C of baseline within 3 min.…”

Section: Discussionmentioning

confidence: 99%

Thermal Imaging to Study Stress Non-invasively in Unrestrained Birds

Jerem

Herborn

McCafferty

et al. 2015

JoVE

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Stress, a central concept in biology, describes a suite of emergency responses to challenges. Among other responses, stress leads to a change in blood flow that results in a net influx of blood to key organs and an increase in core temperature. This stress-induced hyperthermia is used to assess stress. However, measuring core temperature is invasive. As blood flow is redirected to the core, the periphery of the body can cool. This paper describes a protocol where peripheral body temperature is measured non-invasively in wild blue tits (Cyanistes caeruleus) using infrared thermography. In the field we created a set-up bringing the birds to an ideal position in front of the camera by using a baited box. The camera takes a short thermal video recording of the undisturbed bird before applying a mild stressor (closing the box and therefore capturing the bird), and the bird's response to being trapped is recorded. The bare skin of the eye-region is the warmest area in the image. This allows an automated extraction of the maximum eye-region temperature from each image frame, followed by further steps of manual data filtering removing the most common sources of errors (motion blur, blinking). This protocol provides a time series of eye-region temperature with a fine temporal resolution that allows us to study the dynamics of the stress response non-invasively. Further work needs to demonstrate the usefulness of the method to assess stress, for instance to investigate whether eye-region temperature response is proportional to the strength of the stressor. If this can be confirmed, it will provide a valuable alternative method of stress assessment in animals and will be useful to a wide range of researchers from ecologists, conservation biologists, physiologists to animal welfare researchers.

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Section: Discussionmentioning

confidence: 99%

Thermal Imaging to Study Stress Non-invasively in Unrestrained Birds

Jerem

Herborn

McCafferty

et al. 2015

JoVE

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“…Functionally, the ophthalmic rete appears to be an analogue of the carotid rete in mammals, allowing heat to be transferred from warm arterial blood to cool venous blood returning from evaporative surfaces of the head. Blood from the two pathways is thought to mix, so that the resultant brain temperature reflects the relative contribution of blood from the each pathway (Midtgard, 1983). If arterial blood is cooled in the rete, and most of the blood supply to the brain is via this indirect pathway, selective brain cooling will be invoked.…”

Section: Discussionmentioning

confidence: 99%

“…Moreover, birds that have a poorly developed rete (zebra finch; Bech and Midtgard, 1981) or no rete (calliope hummingbird; Burgoon et al, 1987), exhibit a reduced capacity for selective brain cooling. Although the cranial blood supply in ostriches has not been systematically investigated, it has been reported that they have a welldeveloped ophthalmic rete (Midtgard, 1983), and one would predict that selective brain cooling occurs by a similar mechanism.…”

Section: Discussionmentioning

confidence: 99%

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

Fuller

Kamerman

Maloney

et al. 2003

Journal of Experimental Biology

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The main determinant of deep brain temperature, measured in or near the hypothalamus, is the temperature of the arterial blood supplying the brain (Hayward and Baker, 1968). 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). Moderate exercise on a treadmill or exposure to heat in a laboratory uncouples brain and carotid blood temperatures, so that the gradient between brain and blood temperatures narrows until, at a threshold temperature of approximately 39°C, brain temperature equals carotid blood temperature (Baker, 1982;Kuhnen and Jessen, 1991;Kuhnen and Mercer, 1993). Beyond that threshold, brain temperature rises at a slower rate than does blood temperature, establishing selective brain cooling with a magnitude, at most, of about 1°C.In mammals that are free-living in their natural habitat and exposed to a variety of complex stressors, however, a similar tight thermal relationship between brain and arterial blood temperatures is apparently absent. In free-ranging antelope, selective brain cooling occurs within the normothermic range of body temperature, and only sporadically in response to high heat loads (Jessen et al., 1994;Mitchell et al., 1997;Fuller et al., 1999b;Maloney et al., 2002). During high-intensity exercise, when brain temperatures reach their highest levels, selective brain cooling is abolished. Indeed, for any given blood temperature, brain temperature is highly variable and unpredictable. Large-amplitude, transient deviations in brain temperature, independent of any changes in the temperature of arterial blood supplying the brain, have also been observed in several laboratory animals in response to non-thermal stimuli (Fuller et al., 1999a;Maloney et al., 2001). This variability arises because the efferent arm of the control mechanism We used implanted miniature data loggers to measure brain (in or near the hypothalamus) and carotid arterial blood temperatures at 5 min intervals in six free-ranging ostriches Struthio camelus in their natural habitat, for a period of up to 14 days. Carotid blood temperature exhibited a large amplitude (3.0-4.6°C) circadian rhythm, and was positively correlated with air temperature. During the day, brain temperature exceeded carotid blood temperature by approx. 0.4°C, but there were episodes when brain temperature was lowered below blood temperature. Selecti...

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“…The first is the external ophthalmic artery. On its way through the temporal fossa, the artery releases several small branches, fewer than 10 in a 10 g finch and more than 200 in a 200 g kestrel [38], that are intertwined with veins carrying cool blood returning from the moist surfaces of the nasal and buccal cavities and the eye [39,40]. Downstream from the rete, the retal arteries rejoin the external ophthalmic artery, the final destinations of which are the anterior regions of the brain and the eye.…”

Section: Birdsmentioning

confidence: 99%

Selective Brain Cooling in Mammals and Birds.

Jessen

2001

JJP

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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...

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Scaling of the brain and the eye cooling system in birds: A morphometric analysis of the Rete ophthalmicum

Cited by 57 publications

References 22 publications

Thermal Imaging to Study Stress Non-invasively in Unrestrained Birds

Thermal Imaging to Study Stress Non-invasively in Unrestrained Birds

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

Selective Brain Cooling in Mammals and Birds.

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