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

Abstract

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 ϭ 3.06, P ϭ 0.03). Carotid blood temperature also was lower (by 0.28°C) at all times of day (t 5 ϭ 3.68, P ϭ 0.01), but the pattern of brain temperature was unchanged. The mean threshold temperature for SBC was not different before (38.85 Ϯ 0.28°C) and after (38.85 Ϯ 0.39°C) AOV surgery (t 5 ϭ0.00, P ϭ 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. brain temperature; evaporative heat loss; thermoregulation ARTIODACTYLS AND FELIDS HAVE the capacity to lower brain temperature below arterial blood temperature through a process termed selective brain cooling (SBC) (for reviews see Refs. 11 and 26). In artiodactyls, blood destined for the brain enters the carotid rete, a bilateral network of small arteries at the base of the brain embedded in the cavernous sinus, a venous lake containing relatively cool blood from the nasal mucosa and other areas of the head. Heat exchange between the warm arterial blood in the rete and the cool venous blood in the sinus cools cerebral arterial blood, so that brain temperature (measured near the hypothalamus) is lower than carotid arterial blood temperature (23). Historically, SBC has been investigated mainly in the laboratory, where it is conspicuous in hyperthermic animals (25). However, recent studies, particularly in free-living animals, have revealed that SBC is not exclusively under thermal control. Nonthermal inputs, particularly sympathetic nervous system activity, also influence its magnitude. While a resting, moderately hyperthermic antelope may exhibit SBC, intense exercise, for example, to escape predation, rapidly leads to a cessation of SBC and an increase in brain temperature (11,26).Largely as a result of an elegant series of experiments in reindeer (14 -16), it is widely held that the mechanism that allows SBC to be facilitated or inhibited involves relative blood flow in two routes of venous return from the nose (11,26). Cool blood drains from the nasal mucosa on each side of the head into the dorsal nasal vein, which in turn bifurcates into the angularis oculi vein (AOV) and facial vein. Blood that passes into the AOV...

Functional and diffusion tensor magnetic resonance imaging of the sheep brain

“…We also noted the artifacts in T1 images from the sheep (Fig. 1a , arrows), which were likely attributable to the vascular feature (angularis oculi veins [ 31 , 32 ]) that prominently exists in the ovine facial area but not in humans. The artifacts call for necessary countermeasures, such as introduction of additional flow-suppression [ 47 ] or cardiac gating [ 48 ], when using human-compatible imaging protocol on ovine species.…”

“…1a . In the T1 images, small vascular flow artifacts were visible along the phase-encoding direction (marked with arrows) due to the vascular anatomy on ovine facial area (angularis oculi vein [ 31 , 32 ]). The activated functional areas, from the sensorimotor stimulation (Fig.…”

Body water conservation through selective brain cooling by the carotid rete: a physiological feature for surviving climate change?

“…In addition to the angularis oculi veins, less superficial veins, such as the sphenopalatine, external ophthalmic and ethmoidal veins, also supply venous blood to the cavernous sinus ( Sisson and Grossman, 1967 ; Carlton and McKean, 1977 ). As a result, severing the angularis oculi veins does not completely eliminate selective brain cooling ( Fuller et al ., 2011 ). High sympathetic tone attenuates selective brain cooling not only by constricting the angularis oculi veins, but also by constricting nasal mucosal blood vessels and closing arteriovenous anastomoses.…”

Adaptation to Heat and Water Shortage in Large, Arid-Zone Mammals

“…In the first studies on SBC in free-living mammals, made possible through advances in biologging technology, black wildebeest (43) and springbok (56) exhibited SBC at rest when they were moderately hyperthermic but abandoned SBC during high-intensity exercise when brain temperature reached 42°C without apparent ill effects. High sympathetic discharge, like that required to escape predation, appears to inhibit SBC by reducing arterial flow to the nasal mucosa and by reducing cool venous outflow from the nasal mucosa to the cavernous sinus, which envelopes the carotid rete, the anatomical structure that is considered a prerequisite for SBC (21,53). SBC also is attenuated, or absent, in other events likely to be associated with elevated sympathetic activity, such as the proximity of humans (51), vigilance in dominant male animals (35), and return of drinking water to waterdeprived animals (24).…”