rl.ll;-= r-ougers Amhiv
Pflugers Arch, 370, 107 109 (1977)
EuropeanJournal of Physiology 9 by Springer-Verlag 1977
Thermosensitivity of Preoptic Neurones in a Hibernator at High and Low Ambient Temperatures* E. S P E U L D A and W. W U N N E N B E R G Zoologisches Institut der Universil~it Kie], Lehrstuhl f/ir Zoophysiologie, Hegewischstrasse 3, D-2300 Kiel, Federal Repubtic of Germany Summary: The effect of ambient t e m p e r a t u re on the t h e r m o s e n s i t i v i t y of preoptic n e u r o n e s was studied in euthermic golden hamsters. At skin temperatures (Tsk) of 2o~ preoptic units were still responsive to h y p o t h a l a m i c temperatures ( T _ ) b e l o w lo~ while, at T.s~, ~ 36~ thes8 y neurones became inactmve at Thy = 15 C on the average. These studies s u g g e s t that t h e r m o r e c e p t i v e preoptic neurones, i n f l u e n c e d by a high activity of cutaneous c o l d - r e c e p t o r s , are capable of sensing core t e m p e r a t u r e s even in deep h i b e ~ nation. Key words: T e m p e r a t u r e r e g u l a t i o n - Hib e r n a t i o n - Preoptic region - T h e r m o s e n sitive neurones - Skin temperature. Introduction T h e r m o r e s p o n s i v e preoptic neurones in euthermic golden hamsters m a i n t a i n their function even at h y p o t ~ a l a m i c temperatures r a n g i n g from 15-2o-C, while corresponding structures in a n o n - h i b e r n a t o r (guinea pig) are i n a c t i v a t e @ by h y p o t h a lamic t e m p e r a t u r e s b e l o w 30 C ( lo ). A l t h o u g h these studies show that in a hibernator preoptic neurones i n v o l v e d in temperature r e g u l a t i o n r e s p o n d to local temperatures far below those of the euthermic state, s e n s i t i v i t y to t e m p e r a t u res as m e a s u r e d during deep h i b e r n a t i o n could not be d e m o n s t r a t e d in these experiments. On the basis of the hypothesis that in h i b e r n a t o r s preoptic t h e r m o r e s p o n s i v e units are capable of sensing temperatures in deep hibernation, the present experiments were u n d e r t a k e n to investigate the factors which could modify the temperature response curves of preoptic neurones in such a way that they are sensitive to core t e m p e r a t u r e s r a n g i n g from o-lo~ Such m o d i f i c a t i o n of p r e o p t i c unit therm o s e n s i t i v i t y might be e f f e c t e d by alterations of the a c t i v i t y of e x t r a h y p o t h a l a mic t h e r m o r e c e p t i v e structures, which were shown to have an influence on the +) S u p p o r t e d by the Deutsche g e m e i n s c h a f t , Wu 63/2
Forschungs-
temperature-impulse of t h e r m o r e s p o n s i v e
rate c h a r a c t e r i s t i c preoptic units (1,4,
9). Methods The e x p e r i m e n t s were carried out in 25 euthermic golden hamsters (weighing lo7-148 g). The animals were a n a e s t h e t i zed with urethane (1 g/kg i.p.), tracheotomized and placed in a s t e r e o t a x i c instrument. For thermal s t i m u l a t i o n of the preoptic region (POA) a fine thermode device was used as d e s c r i b e d p r e v i o u s l y ( l o ) . Temperatures of the POA, as well as skin temperatures, were m e a s u r e d by thermocouples and r e c o r d e d continuously. In order to control Tsk the animals were wrapped in a thin plastic coat and immersed (up to the head) in a temperature-regulated, w e l l - s t i r r e d w a t e r bath. Single unit activity was p i c k e d up by stainless steel m i c r o e l e c t r o d e s , amplifled and recorded on m a g n e t i c tape. Analysis of discharge frequency was made with ~he help of a pulse height analyser (Single Channel Analyser, Hewlett and Packard 5583 A) and a Hewlett and P a c k a r d Universal Counter (5325 B). The positions of t h e r m o r e s p o n s i v e units were marked and localized h i s t o l o gically. Results A total of 73 units of the POA were held under o b s e r v a t i o n long enough to complete several h e a t i n g and c o o l i n g cycles.2o of these p r o v e d to be sensitive to local thermal stimulation. As an example Fig. 1. shows a s e c t i o n of the course of an experiment in w h i c h the response of a preoptic single unit to local thermal s t i m ~ lation was tested at Tsk = 21oc (1st part, Fig. 1) and Tsk = 36oc (2nd part, Fig. 1). At both skin t e m p e r a t u r e s this unit was sensitive to h e a t i n g of the P0A with a p o s i t i v e thermal coefficient; the t h e r m o s e n s i t i v i t y of this unit, however, was e v i d e n t l y higher when the skin was warmed. The response to low preoptic
108 temperatures was also influenced by the temperatures of the body surface. At T s ~ 36~ the unit was inactivated at Thy : 2o~ while at Tsk : 21oc this neurone showed a discharge frequency of 3 Imp./s even at Thy = 18~176
~ 40
TEMPERATURES /""--1/Preoptic Region
~
Subcutis - -
Fig. 2 shows the average static responses to local thermal stimulation of 2o preoptic units recorded at Tsk = 36oc (solid line). Of these, only 7 could be additionally tested at Tsk = 2o~ (broken line), as in most cases single unit recordings were disturbed by vigorous shivering when skin temperature was lowered. A comparison of both response curves demonstrates that the temperature range in which the neurones are responsive is shifted more than 5~ to lower values by skin cooling. This effect is based on a loss of thermal sensitivity of the u n i t s i.e. the steepness of the temperatureimpulse rate characteristic of the hypothalamic neurones is significantly reduced at low Tsk. Discussion
20 I
I
---
FIRING RATE
Impls
I
I
I
40
45
t~
30 20 10
5
10 35 Minutes
It seems to be possible that not only cutaneous cold receptors modify the temperature response curves of preoptic units but also other extrahypothalamic thermoreceptive structures, i.e. the spinal cord. Furthermore, seasonal variations of the thermosensitivity of preoptic units should be taken into consideration.
Fig. 1 Responses of a preoptic neurone to local thermal stimulation at Tsk : 21~ and Tsk = 36 ~ C.
]mpls 80
60
Ts. =36 e C / N =20
References
1t /
10
20 Preoptic
Region
30 Temperature
j"
Although the present studies do not simulate temperature conditions during hibernation, they may help to elucidate the mode of action of preoptic thermoreceptire structures during hibernation. Influenced by a high activity of cutaneous cold receptors as it occurs in hibernating animals ( 6 ), preoptic thermoreceptive structures seem to be capable of sensing core temperatures even in deep hibernation. Thus, the present studies are a neurophysiological supplement to previously reported experiments in hibernating animals, in which thermoregulatory reactions could be evoked by thermal stimulation of the POA (2, 3, 5, 7, 8).
N=7
40 ~
Fig.2 Average temperature responses of preoptic neurones at Tsk : 36~ (solid line) and Tsk : 2o~ (broken line). Vertical bars indicate S.E. At preoptic region temperatures marked by an asterisk the differences in the firing rates are significant (P ~ o,ooi).
i. Boulant,J.A.,Hardy,J.D.: The effect of spinal and skin temperatures on the firing rate and thermosensitivity of preoptic neurones.J.Physiol. (Lond.) 24~, 639-66o (1974) 2. Heath,J.E.,Williams,B.A.,Mills,S.H., Kluger,M.J.: The responsiveness of the preoptic-anterior hypothalamus to temperature in vertebrates. In: Hibernation and hypothermia, perspectives and challenges, edited by F.E.South,J.P. Harmon, J.S.Willis, E.T.Pengelley and N.R.Alpert. Amsterdam: Elsevier 1972 3. Heller,H.C.,Colliver,G.W.: CNS regulation of body temperature during hibernation. Am.J.Physiol. 227, 583-589 (1974)
109
4. Hellon,R.F.: The stimulation of hypothalamic neurones by changes in ambient temperature. Pfl~gers Arch.321, 56-66 (197o) 5. Lyman,C.P., O'Brien,R.C.: Sensitivity to low temperature in hibernating rodents. Am.J.Physiol. 222, 864-869 (1972) 6. Raths,P., Hensel,H.: Cutane Thermoreceptoren bei Winterschl~fern.Pfldgets Arch. 293, 281-3o2 (1967) 7. South,F.E.,Hartner,W.C.: Hibernation and activ thermoregulation: Responses to manipulation of the temperature of the preoptic region in the marmot. Cryobiology 8, 389 (1971)
8. South,F.E., Hartner,W.C., Luecke,R. H.: Responses to preoptic temperature manipulation in the awake and hibernating marmot. Am.J.Physiol. 229, 15o-16o (1975) 9. Wit,A., Wang,S.C.: Temperature-sensitive neurons in preoptic-anterior hypothalamic region: Effects of increasing ambient temperature. Am.J.Physiol. 215, 1151-1159 (1968) io. Wdnnenberg,W., Merker,G., Speulda,E.: Thermosensitivity of preoptic neurones in a hibernator (golden hamster) and a non-hibernator (guinea pig) Pfldgers Arch. 363, 119-123 (1976 Received May 4,1977
Pflugers Arch, 370, 107 109 (1977)
EuropeanJournal of Physiology 9 by Springer-Verlag 1977
Thermosensitivity of Preoptic Neurones in a Hibernator at High and Low Ambient Temperatures* E. S P E U L D A and W. W U N N E N B E R G Zoologisches Institut der Universil~it Kie], Lehrstuhl f/ir Zoophysiologie, Hegewischstrasse 3, D-2300 Kiel, Federal Repubtic of Germany Summary: The effect of ambient t e m p e r a t u re on the t h e r m o s e n s i t i v i t y of preoptic n e u r o n e s was studied in euthermic golden hamsters. At skin temperatures (Tsk) of 2o~ preoptic units were still responsive to h y p o t h a l a m i c temperatures ( T _ ) b e l o w lo~ while, at T.s~, ~ 36~ thes8 y neurones became inactmve at Thy = 15 C on the average. These studies s u g g e s t that t h e r m o r e c e p t i v e preoptic neurones, i n f l u e n c e d by a high activity of cutaneous c o l d - r e c e p t o r s , are capable of sensing core t e m p e r a t u r e s even in deep h i b e ~ nation. Key words: T e m p e r a t u r e r e g u l a t i o n - Hib e r n a t i o n - Preoptic region - T h e r m o s e n sitive neurones - Skin temperature. Introduction T h e r m o r e s p o n s i v e preoptic neurones in euthermic golden hamsters m a i n t a i n their function even at h y p o t ~ a l a m i c temperatures r a n g i n g from 15-2o-C, while corresponding structures in a n o n - h i b e r n a t o r (guinea pig) are i n a c t i v a t e @ by h y p o t h a lamic t e m p e r a t u r e s b e l o w 30 C ( lo ). A l t h o u g h these studies show that in a hibernator preoptic neurones i n v o l v e d in temperature r e g u l a t i o n r e s p o n d to local temperatures far below those of the euthermic state, s e n s i t i v i t y to t e m p e r a t u res as m e a s u r e d during deep h i b e r n a t i o n could not be d e m o n s t r a t e d in these experiments. On the basis of the hypothesis that in h i b e r n a t o r s preoptic t h e r m o r e s p o n s i v e units are capable of sensing temperatures in deep hibernation, the present experiments were u n d e r t a k e n to investigate the factors which could modify the temperature response curves of preoptic neurones in such a way that they are sensitive to core t e m p e r a t u r e s r a n g i n g from o-lo~ Such m o d i f i c a t i o n of p r e o p t i c unit therm o s e n s i t i v i t y might be e f f e c t e d by alterations of the a c t i v i t y of e x t r a h y p o t h a l a mic t h e r m o r e c e p t i v e structures, which were shown to have an influence on the +) S u p p o r t e d by the Deutsche g e m e i n s c h a f t , Wu 63/2
Forschungs-
temperature-impulse of t h e r m o r e s p o n s i v e
rate c h a r a c t e r i s t i c preoptic units (1,4,
9). Methods The e x p e r i m e n t s were carried out in 25 euthermic golden hamsters (weighing lo7-148 g). The animals were a n a e s t h e t i zed with urethane (1 g/kg i.p.), tracheotomized and placed in a s t e r e o t a x i c instrument. For thermal s t i m u l a t i o n of the preoptic region (POA) a fine thermode device was used as d e s c r i b e d p r e v i o u s l y ( l o ) . Temperatures of the POA, as well as skin temperatures, were m e a s u r e d by thermocouples and r e c o r d e d continuously. In order to control Tsk the animals were wrapped in a thin plastic coat and immersed (up to the head) in a temperature-regulated, w e l l - s t i r r e d w a t e r bath. Single unit activity was p i c k e d up by stainless steel m i c r o e l e c t r o d e s , amplifled and recorded on m a g n e t i c tape. Analysis of discharge frequency was made with ~he help of a pulse height analyser (Single Channel Analyser, Hewlett and Packard 5583 A) and a Hewlett and P a c k a r d Universal Counter (5325 B). The positions of t h e r m o r e s p o n s i v e units were marked and localized h i s t o l o gically. Results A total of 73 units of the POA were held under o b s e r v a t i o n long enough to complete several h e a t i n g and c o o l i n g cycles.2o of these p r o v e d to be sensitive to local thermal stimulation. As an example Fig. 1. shows a s e c t i o n of the course of an experiment in w h i c h the response of a preoptic single unit to local thermal s t i m ~ lation was tested at Tsk = 21oc (1st part, Fig. 1) and Tsk = 36oc (2nd part, Fig. 1). At both skin t e m p e r a t u r e s this unit was sensitive to h e a t i n g of the P0A with a p o s i t i v e thermal coefficient; the t h e r m o s e n s i t i v i t y of this unit, however, was e v i d e n t l y higher when the skin was warmed. The response to low preoptic
108 temperatures was also influenced by the temperatures of the body surface. At T s ~ 36~ the unit was inactivated at Thy : 2o~ while at Tsk : 21oc this neurone showed a discharge frequency of 3 Imp./s even at Thy = 18~176
~ 40
TEMPERATURES /""--1/Preoptic Region
~
Subcutis - -
Fig. 2 shows the average static responses to local thermal stimulation of 2o preoptic units recorded at Tsk = 36oc (solid line). Of these, only 7 could be additionally tested at Tsk = 2o~ (broken line), as in most cases single unit recordings were disturbed by vigorous shivering when skin temperature was lowered. A comparison of both response curves demonstrates that the temperature range in which the neurones are responsive is shifted more than 5~ to lower values by skin cooling. This effect is based on a loss of thermal sensitivity of the u n i t s i.e. the steepness of the temperatureimpulse rate characteristic of the hypothalamic neurones is significantly reduced at low Tsk. Discussion
20 I
I
---
FIRING RATE
Impls
I
I
I
40
45
t~
30 20 10
5
10 35 Minutes
It seems to be possible that not only cutaneous cold receptors modify the temperature response curves of preoptic units but also other extrahypothalamic thermoreceptive structures, i.e. the spinal cord. Furthermore, seasonal variations of the thermosensitivity of preoptic units should be taken into consideration.
Fig. 1 Responses of a preoptic neurone to local thermal stimulation at Tsk : 21~ and Tsk = 36 ~ C.
]mpls 80
60
Ts. =36 e C / N =20
References
1t /
10
20 Preoptic
Region
30 Temperature
j"
Although the present studies do not simulate temperature conditions during hibernation, they may help to elucidate the mode of action of preoptic thermoreceptire structures during hibernation. Influenced by a high activity of cutaneous cold receptors as it occurs in hibernating animals ( 6 ), preoptic thermoreceptive structures seem to be capable of sensing core temperatures even in deep hibernation. Thus, the present studies are a neurophysiological supplement to previously reported experiments in hibernating animals, in which thermoregulatory reactions could be evoked by thermal stimulation of the POA (2, 3, 5, 7, 8).
N=7
40 ~
Fig.2 Average temperature responses of preoptic neurones at Tsk : 36~ (solid line) and Tsk : 2o~ (broken line). Vertical bars indicate S.E. At preoptic region temperatures marked by an asterisk the differences in the firing rates are significant (P ~ o,ooi).
i. Boulant,J.A.,Hardy,J.D.: The effect of spinal and skin temperatures on the firing rate and thermosensitivity of preoptic neurones.J.Physiol. (Lond.) 24~, 639-66o (1974) 2. Heath,J.E.,Williams,B.A.,Mills,S.H., Kluger,M.J.: The responsiveness of the preoptic-anterior hypothalamus to temperature in vertebrates. In: Hibernation and hypothermia, perspectives and challenges, edited by F.E.South,J.P. Harmon, J.S.Willis, E.T.Pengelley and N.R.Alpert. Amsterdam: Elsevier 1972 3. Heller,H.C.,Colliver,G.W.: CNS regulation of body temperature during hibernation. Am.J.Physiol. 227, 583-589 (1974)
109
4. Hellon,R.F.: The stimulation of hypothalamic neurones by changes in ambient temperature. Pfl~gers Arch.321, 56-66 (197o) 5. Lyman,C.P., O'Brien,R.C.: Sensitivity to low temperature in hibernating rodents. Am.J.Physiol. 222, 864-869 (1972) 6. Raths,P., Hensel,H.: Cutane Thermoreceptoren bei Winterschl~fern.Pfldgets Arch. 293, 281-3o2 (1967) 7. South,F.E.,Hartner,W.C.: Hibernation and activ thermoregulation: Responses to manipulation of the temperature of the preoptic region in the marmot. Cryobiology 8, 389 (1971)
8. South,F.E., Hartner,W.C., Luecke,R. H.: Responses to preoptic temperature manipulation in the awake and hibernating marmot. Am.J.Physiol. 229, 15o-16o (1975) 9. Wit,A., Wang,S.C.: Temperature-sensitive neurons in preoptic-anterior hypothalamic region: Effects of increasing ambient temperature. Am.J.Physiol. 215, 1151-1159 (1968) io. Wdnnenberg,W., Merker,G., Speulda,E.: Thermosensitivity of preoptic neurones in a hibernator (golden hamster) and a non-hibernator (guinea pig) Pfldgers Arch. 363, 119-123 (1976 Received May 4,1977
