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Brain temperature and the cerebral circulation in the chicken
SHORT COMMUNICATIONS
265
Brain temperature and the cerebral circulation in the chicken In mammals, Hayward and Bakerl,a, 6 have shown that the most important factor influencing brain temperature is the temperature of the cerebral arterial blood at the circle of Willis. The rabbit and monkey have a patent internal carotid artery directly linking the cerebral and systemic circulations, and they show a direct association between the temperature fluctuations of the arterial blood in the cranial cavity and in the body core. However, the cat and sheep possess no internal carotid artery and the circle of Willis is supplied by way of a network of small vessels, the rete mirabile, formed from the internal maxillary branch of the external carotid artery. In these species the blood at the circle of Willis has a lower temperature than that in the carotid arteries owing to heat exchange between the cooler venous blood in the cavernous sinus (sheep) or pterygoid plexus (cat) and the warmer arterial blood in the fete. As a result, there is a dissociation between the temperatures of the brain and of the body core. Birds generally do not possess an intact circle of Willis like that of mammals, although the well developed intercarotid anastomosis functions as an alternative and effective collateral channel2, la. In the chicken there is no communication between the vertebral and basilar arteries so that the entire brain is supplied from the intercarotid anastomosis which surrounds the pituitary on its lateral and caudal borders 9 (Fig. 1). The anastomosis, together with the intrasphenoid portions of the internal carotid and internal ophthalmic arteries, lies within the cavernous sinus TM. Although this structure is probably not homologous with that of the same name in mammals 15 it could play a similar role in brain temperature regulation because it receives blood
A DBI
IVv Va
VS
~.C
ACL
JJ
Fig. 1. The cerebral circulation in the chicken. A, Diagram illustrating the arrangement of the vessels with respect to the brain. B, The ventral surface of the brain showing the relationship between the intercarotid anastomosis and cavernous sinus. The arteries are shown in black, the veins and sinuses in white, and the central nervous tissue in stippling. AC, anterior cephalic vein; B, basilar artery; CC, common carotid artery; CS, cavernous sinus; Cv, carotid vein; CW, 'circle of Willis'; DB, dorsal brain sinuses; EC, external carotid artery; IC, internal carotid artery; ICa, intercarotid anastomosis; .1,jugular vein ; O, occipital veins; OC, optic chiasma; Ov, ophthalmic veins; OVa, occipital-vertebral anastomosis; P, pituitary; PC, posterior cephalic vein; RM, fete mirabile; Va, vertebral artery; VS, ventral spinal artery; Vv, vertebral vein. Brain Research, 23 (1970) 265-268
266
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from the ethmoid and superficial ophthalmic veins draining the anterior facial region and nasal cavities. On anatomical grounds it is therefore feasible that countercurrent heat exchange could occur between the extensive areas of arterio-venous contact at the base of the brain, and this might influence brain temperature, particularly that of the hypothalamus which is supplied directly from the intercarotid anastomosis. Since there have been very few measurements of intracerebral temperatures in birds, and in view of the anatomical analogies with the mammalian cerebral circulation, it is of interest to know whether similar physiological effects can be detected. To test this possibility, thermistors and thermocouples were chronically implanted into the anterior hypothalamus and into the central neostriatal region about half way in depth between the intercarotid anastomosis and the surface ot' the cerebrum. After recovery the fowls were exposed to ambient temperatures of 15-22°C and the brain and colonic temperatures recorded during control periods of 2 h. They were then subjected for the same period to 40°C to examine the effect on brain temperatures of heat exposure and thermal panting, and finally allowed to recover in the control environment. The results are presented in Table I. Under resting thermoneutral conditions both brain temperatures were lower than colonic temperature by 0.6-1. I ' C ; that of the hypothalamus was higher than neostriatal temperature by an average of 0.2°C. During exposure to heat there was a decrease in the cerebral-visceral gradient such that after about 2 h at 40°C the two brain temperatures were identical and very close to that of the colon. Moreover, the decrease commenced before the onset of panting. When the birds were returned to 15-22°C there was a precipitous fall in hypothalamic temperature but only a gradual decline in the colon. In some instances, colonic temperature continued to rise by 0.05-0.2°C even while hypothalamic temperature fell by up to 0.6°C. Hypothalamic temperature was generally lower and colonic temperature higher at the cessation than at the onset of panting. In so far as hypothalamic temperature is normally lower than colonic temperature, the fowl resembles the sheep 7, and the basis for this temperature difference could be heat exchange between the intercarotid anastomosis and cavernous sinus.
TABLE I BRAIN AND COLONIC TEMPERATURES OF CHICKENS AT TWO LEVELS OF AMBIENT TEMPERATURE AND IN RELATION TO THERMAL P A N T I N G
Mean values (± S.E.) of 13 experiments on 7 birds. Time o f measurement
After 2 h at 15-22°C At onset of panting in 40°C After 2 h at 40°C At cessation of panting in 15-22°C After 2 h at 15-22°C Brain Research, 23 (1970) 265-268
Temperature ('~C) Hypothalamus
Neostriatum
Colon
40.6 :~-0.13 41.8 ~ 0.11 43.1 3 0.11 41.4 0.22 40.4 ! 0.16
40.4 ± 0.13 41.7 :~ 0.12 43.1 ~ 0.12 41.3 ~::0.25 40.3 :! 0.15
41.4 E: 0;08 42.2 ~: 0.14 43.2 :k 0.10 42.5 +: 0.37 41.3 j: 0.10
SHORT COMMUNICATIONS
267
However, the arterial walls are thick and muscular at the anastomosis and there is no network at this site comparable to the rete of the sheep I through which heat exchange would be more efficient. A fete mirabile does occur in the fowl, although it is developed chiefly from the external ophthalmic branch of the internal carotid artery rather than from the internal maxillary 9 (Fig. 1): nevertheless, it is capable of providing an adequate supply of blood to the brain after total occlusion of the direct route through the internal carotid la. The arterial fete is closely associated with a similar venous network which connects the cavernous sinus and ophthalmic veins to the branches of the anterior cephalic vein. Exchange of heat could therefore occur equally well at this site, although the presence of such a large internal carotid artery in the fowl makes it difficult to envisage anything comparable to the situation which occurs in the dog 5 where the dual vascular anatomy, consisting of a rudimentary fete as well as a small internal carotid, is reflected in the presence of both types of brain temperature regulation. Panting elicited by exposing the chickens to heat generally caused the opposite effect to that described in the cat s aond sheep 1, namely, a decrease in the temperature gradient between brain and colon. The greater part of this decrease occurred before the onset of panting, suggesting that the cooling effect normally exerted at moderate air temperatures was absent at 40°C. The fact that after 2 h the brain temperature sometimes reached, but seldom surpassed, the colonic temperature may indicate that under these conditions the former is regulated primarily by the temperature of the carotid arterial blood, heat loss by convection and radiation from the nasal passageways and skin of the head having been eliminated. If, as is generally assumed, most of the evaporative cooling in birds occurs from the thoracic and abdominal air sacs rather than from the upper respiratory tract as in mammals 1~, no special localized protection for the brain against rising body temperature could be expected. Also, the increase in the fowl's hypothalamic temperature which is seen during behavioural arousal 11 could be explained in terms of vasoconstriction in the nasal mucosa and a reduced supply of cool venous blood to the cavernous sinus, as has been demonstrated for the sheep l. Similarly, the dissociation between brain and colonic temperatures which often occurred after withdrawal of the birds from heat may reflect the sudden increase in efficiency of evaporative and non-evaporative heat loss to the cool ambient air as distinct from the air in the air sacs which is always at or near deep body temperature. Nevertheless, the thermal delay in the colon is likely to be in part the result of its relatively poor blood supply compared to that of the brain. The observation that neostriatal temperature is normally lower than hypothalamic temperature agrees with previous findings in both mammals a,4 and birds ~4 that deep brain sites are warmer than superficial cortical regions. It remains to be seen in the fowl, however, whether the position of a deep site in relation to the circle of Willis also influences its temperature, as Hayward and Baker's hypothesis would require. Only further studies, including direct measurements of intravascular temperatures, can ~esolve this issue, and show whether arterio-venous heat exchange ill
Brain Research, 23 (1970) 265-268
268
SHORT COMMUNICATIONS
the cerebral c ir c u l a t io n is a m o r e i m p o r t a n t f a c t o r in c o n t r i b u t i n g to the low temp er at u res in the avian brain t h a n is loss o f heat f r o m the l o n g cervical arteries. T h e work was s u p p o r t e d by a g r a n t f r o m the A g r i c u l t u r a l Research Council.
Wye College, University of London, Ashford, Kent (Great Britain)
S. A. RICHARDS
1 BAKER, M. A., AND HAYWARD, J. N., The influence of the nasal mucosa and the carotid fete upon hypothalamic temperature in sheep, J. Physiol. (Lond.), 198 (1968) 561-579. 2 BAUMEL,J. J., ANDGERCHMAN,L., The avian intercarotid anastomosis and its homologue in other vertebrates, Amer. J. Anat., 122 (1968) 1-18. 3 DELGADO,J. M. R., AND HANAL T., Intracerebral temperature in free-moving cats, Amer. J. Physiol., 211 (1966) 755-769. 4 Fusco, M. M., Temperature pattern throughout the hypothalamus in the resting dog. In J. D. HARDY (Ed.), Temperature, its Measurement and Control in Science and Industry, Reinhold, New York, 1963, pp. 585-587. 5 HAYWARD,J. N., Brain temperature regulation during sleep and arousal in the dog, Exp. Neurol., 21 (1968) 201-212. 6 HAYWARD,J. N., AND BAKER, M. A., A comparative study of the role of the cerebral arterial blood in the regulation of brain temperature in five mammals, Brain Research, 16 (1969) 417-440. 7 HEMINGWAY,A.,ROBINSON,R.,HEMINGWAY,C.,ANDWALL,J., Cutaneous and brain temperatures related to respiratory metabolism of the sheep, J. appl. PhysioL, 21 (1966) 1223-1227. 8 HUNTER,W. S., ANDADAMS,T., Respiratory heat exchange influences on diencephalic temperature in the cat, J. appl. PhysioL, 21 (1966) 873-876. 9 RICnARDS,S. A., Anatomy of the arteries of the head in the domestic fowl, J. ZooL (Lond.), 152 (1967) 221-234. 10 RICHARDS,S. A., Anatomy of the veins of the head in the domestic fowl, J. ZooL (Lond.), 154 (1968) 223-234. 11 RICHARDS, S. A., The biology and comparative physiology of thermal panting, Biol. Rev., 45 (1970) 223-264. 12 RICr~ARDS,S. A., The role of hypothalamic temperature in the control of panting in the chicken exposed to heat, J. PhysioL (Lond.), 212 (1970)in press. 13 RICHARDS,S. A., AND SYKES,A. H., Responses of the domestic fowl to occlusion of the cervical arteries and veins, Comp. Biochem. Physiol., 21 (1967) 39-50. 14 SAINTPAUL, U., UND ASCHOFF,J., Gehirntemperaturen bei Hiihnern, Pfliigers Arch. ffes. Physiol., 301 (1968) 109-123. 15 WtNGSTRAND,K. G., The Structure and Development of the Avian Pituitary, Gleerup, Lund, 1951.
p. 264. (Accepted August 6th, 1970)
Brain Research, 23 (1970) 265-268
265
Brain temperature and the cerebral circulation in the chicken In mammals, Hayward and Bakerl,a, 6 have shown that the most important factor influencing brain temperature is the temperature of the cerebral arterial blood at the circle of Willis. The rabbit and monkey have a patent internal carotid artery directly linking the cerebral and systemic circulations, and they show a direct association between the temperature fluctuations of the arterial blood in the cranial cavity and in the body core. However, the cat and sheep possess no internal carotid artery and the circle of Willis is supplied by way of a network of small vessels, the rete mirabile, formed from the internal maxillary branch of the external carotid artery. In these species the blood at the circle of Willis has a lower temperature than that in the carotid arteries owing to heat exchange between the cooler venous blood in the cavernous sinus (sheep) or pterygoid plexus (cat) and the warmer arterial blood in the fete. As a result, there is a dissociation between the temperatures of the brain and of the body core. Birds generally do not possess an intact circle of Willis like that of mammals, although the well developed intercarotid anastomosis functions as an alternative and effective collateral channel2, la. In the chicken there is no communication between the vertebral and basilar arteries so that the entire brain is supplied from the intercarotid anastomosis which surrounds the pituitary on its lateral and caudal borders 9 (Fig. 1). The anastomosis, together with the intrasphenoid portions of the internal carotid and internal ophthalmic arteries, lies within the cavernous sinus TM. Although this structure is probably not homologous with that of the same name in mammals 15 it could play a similar role in brain temperature regulation because it receives blood
A DBI
IVv Va
VS
~.C
ACL
JJ
Fig. 1. The cerebral circulation in the chicken. A, Diagram illustrating the arrangement of the vessels with respect to the brain. B, The ventral surface of the brain showing the relationship between the intercarotid anastomosis and cavernous sinus. The arteries are shown in black, the veins and sinuses in white, and the central nervous tissue in stippling. AC, anterior cephalic vein; B, basilar artery; CC, common carotid artery; CS, cavernous sinus; Cv, carotid vein; CW, 'circle of Willis'; DB, dorsal brain sinuses; EC, external carotid artery; IC, internal carotid artery; ICa, intercarotid anastomosis; .1,jugular vein ; O, occipital veins; OC, optic chiasma; Ov, ophthalmic veins; OVa, occipital-vertebral anastomosis; P, pituitary; PC, posterior cephalic vein; RM, fete mirabile; Va, vertebral artery; VS, ventral spinal artery; Vv, vertebral vein. Brain Research, 23 (1970) 265-268
266
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from the ethmoid and superficial ophthalmic veins draining the anterior facial region and nasal cavities. On anatomical grounds it is therefore feasible that countercurrent heat exchange could occur between the extensive areas of arterio-venous contact at the base of the brain, and this might influence brain temperature, particularly that of the hypothalamus which is supplied directly from the intercarotid anastomosis. Since there have been very few measurements of intracerebral temperatures in birds, and in view of the anatomical analogies with the mammalian cerebral circulation, it is of interest to know whether similar physiological effects can be detected. To test this possibility, thermistors and thermocouples were chronically implanted into the anterior hypothalamus and into the central neostriatal region about half way in depth between the intercarotid anastomosis and the surface ot' the cerebrum. After recovery the fowls were exposed to ambient temperatures of 15-22°C and the brain and colonic temperatures recorded during control periods of 2 h. They were then subjected for the same period to 40°C to examine the effect on brain temperatures of heat exposure and thermal panting, and finally allowed to recover in the control environment. The results are presented in Table I. Under resting thermoneutral conditions both brain temperatures were lower than colonic temperature by 0.6-1. I ' C ; that of the hypothalamus was higher than neostriatal temperature by an average of 0.2°C. During exposure to heat there was a decrease in the cerebral-visceral gradient such that after about 2 h at 40°C the two brain temperatures were identical and very close to that of the colon. Moreover, the decrease commenced before the onset of panting. When the birds were returned to 15-22°C there was a precipitous fall in hypothalamic temperature but only a gradual decline in the colon. In some instances, colonic temperature continued to rise by 0.05-0.2°C even while hypothalamic temperature fell by up to 0.6°C. Hypothalamic temperature was generally lower and colonic temperature higher at the cessation than at the onset of panting. In so far as hypothalamic temperature is normally lower than colonic temperature, the fowl resembles the sheep 7, and the basis for this temperature difference could be heat exchange between the intercarotid anastomosis and cavernous sinus.
TABLE I BRAIN AND COLONIC TEMPERATURES OF CHICKENS AT TWO LEVELS OF AMBIENT TEMPERATURE AND IN RELATION TO THERMAL P A N T I N G
Mean values (± S.E.) of 13 experiments on 7 birds. Time o f measurement
After 2 h at 15-22°C At onset of panting in 40°C After 2 h at 40°C At cessation of panting in 15-22°C After 2 h at 15-22°C Brain Research, 23 (1970) 265-268
Temperature ('~C) Hypothalamus
Neostriatum
Colon
40.6 :~-0.13 41.8 ~ 0.11 43.1 3 0.11 41.4 0.22 40.4 ! 0.16
40.4 ± 0.13 41.7 :~ 0.12 43.1 ~ 0.12 41.3 ~::0.25 40.3 :! 0.15
41.4 E: 0;08 42.2 ~: 0.14 43.2 :k 0.10 42.5 +: 0.37 41.3 j: 0.10
SHORT COMMUNICATIONS
267
However, the arterial walls are thick and muscular at the anastomosis and there is no network at this site comparable to the rete of the sheep I through which heat exchange would be more efficient. A fete mirabile does occur in the fowl, although it is developed chiefly from the external ophthalmic branch of the internal carotid artery rather than from the internal maxillary 9 (Fig. 1): nevertheless, it is capable of providing an adequate supply of blood to the brain after total occlusion of the direct route through the internal carotid la. The arterial fete is closely associated with a similar venous network which connects the cavernous sinus and ophthalmic veins to the branches of the anterior cephalic vein. Exchange of heat could therefore occur equally well at this site, although the presence of such a large internal carotid artery in the fowl makes it difficult to envisage anything comparable to the situation which occurs in the dog 5 where the dual vascular anatomy, consisting of a rudimentary fete as well as a small internal carotid, is reflected in the presence of both types of brain temperature regulation. Panting elicited by exposing the chickens to heat generally caused the opposite effect to that described in the cat s aond sheep 1, namely, a decrease in the temperature gradient between brain and colon. The greater part of this decrease occurred before the onset of panting, suggesting that the cooling effect normally exerted at moderate air temperatures was absent at 40°C. The fact that after 2 h the brain temperature sometimes reached, but seldom surpassed, the colonic temperature may indicate that under these conditions the former is regulated primarily by the temperature of the carotid arterial blood, heat loss by convection and radiation from the nasal passageways and skin of the head having been eliminated. If, as is generally assumed, most of the evaporative cooling in birds occurs from the thoracic and abdominal air sacs rather than from the upper respiratory tract as in mammals 1~, no special localized protection for the brain against rising body temperature could be expected. Also, the increase in the fowl's hypothalamic temperature which is seen during behavioural arousal 11 could be explained in terms of vasoconstriction in the nasal mucosa and a reduced supply of cool venous blood to the cavernous sinus, as has been demonstrated for the sheep l. Similarly, the dissociation between brain and colonic temperatures which often occurred after withdrawal of the birds from heat may reflect the sudden increase in efficiency of evaporative and non-evaporative heat loss to the cool ambient air as distinct from the air in the air sacs which is always at or near deep body temperature. Nevertheless, the thermal delay in the colon is likely to be in part the result of its relatively poor blood supply compared to that of the brain. The observation that neostriatal temperature is normally lower than hypothalamic temperature agrees with previous findings in both mammals a,4 and birds ~4 that deep brain sites are warmer than superficial cortical regions. It remains to be seen in the fowl, however, whether the position of a deep site in relation to the circle of Willis also influences its temperature, as Hayward and Baker's hypothesis would require. Only further studies, including direct measurements of intravascular temperatures, can ~esolve this issue, and show whether arterio-venous heat exchange ill
Brain Research, 23 (1970) 265-268
268
SHORT COMMUNICATIONS
the cerebral c ir c u l a t io n is a m o r e i m p o r t a n t f a c t o r in c o n t r i b u t i n g to the low temp er at u res in the avian brain t h a n is loss o f heat f r o m the l o n g cervical arteries. T h e work was s u p p o r t e d by a g r a n t f r o m the A g r i c u l t u r a l Research Council.
Wye College, University of London, Ashford, Kent (Great Britain)
S. A. RICHARDS
1 BAKER, M. A., AND HAYWARD, J. N., The influence of the nasal mucosa and the carotid fete upon hypothalamic temperature in sheep, J. Physiol. (Lond.), 198 (1968) 561-579. 2 BAUMEL,J. J., ANDGERCHMAN,L., The avian intercarotid anastomosis and its homologue in other vertebrates, Amer. J. Anat., 122 (1968) 1-18. 3 DELGADO,J. M. R., AND HANAL T., Intracerebral temperature in free-moving cats, Amer. J. Physiol., 211 (1966) 755-769. 4 Fusco, M. M., Temperature pattern throughout the hypothalamus in the resting dog. In J. D. HARDY (Ed.), Temperature, its Measurement and Control in Science and Industry, Reinhold, New York, 1963, pp. 585-587. 5 HAYWARD,J. N., Brain temperature regulation during sleep and arousal in the dog, Exp. Neurol., 21 (1968) 201-212. 6 HAYWARD,J. N., AND BAKER, M. A., A comparative study of the role of the cerebral arterial blood in the regulation of brain temperature in five mammals, Brain Research, 16 (1969) 417-440. 7 HEMINGWAY,A.,ROBINSON,R.,HEMINGWAY,C.,ANDWALL,J., Cutaneous and brain temperatures related to respiratory metabolism of the sheep, J. appl. PhysioL, 21 (1966) 1223-1227. 8 HUNTER,W. S., ANDADAMS,T., Respiratory heat exchange influences on diencephalic temperature in the cat, J. appl. PhysioL, 21 (1966) 873-876. 9 RICnARDS,S. A., Anatomy of the arteries of the head in the domestic fowl, J. ZooL (Lond.), 152 (1967) 221-234. 10 RICHARDS,S. A., Anatomy of the veins of the head in the domestic fowl, J. ZooL (Lond.), 154 (1968) 223-234. 11 RICHARDS, S. A., The biology and comparative physiology of thermal panting, Biol. Rev., 45 (1970) 223-264. 12 RICr~ARDS,S. A., The role of hypothalamic temperature in the control of panting in the chicken exposed to heat, J. PhysioL (Lond.), 212 (1970)in press. 13 RICHARDS,S. A., AND SYKES,A. H., Responses of the domestic fowl to occlusion of the cervical arteries and veins, Comp. Biochem. Physiol., 21 (1967) 39-50. 14 SAINTPAUL, U., UND ASCHOFF,J., Gehirntemperaturen bei Hiihnern, Pfliigers Arch. ffes. Physiol., 301 (1968) 109-123. 15 WtNGSTRAND,K. G., The Structure and Development of the Avian Pituitary, Gleerup, Lund, 1951.
p. 264. (Accepted August 6th, 1970)
Brain Research, 23 (1970) 265-268