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Is 5-hydroxytryptamine concerned in avian thermoregulation?
J. therm. Biol.. Vol. 4. pp. 219 to 221 Per~lamon Press Ltd 1979. Printed in Great Britain
IS 5-HYDROXYTRYPTAMINE CONCERNED IN AVIAN THERMOREGULATION? B. M. FREEMAN Houghton Poultry Research Station, Houghton, Huntingdon PEI7 2DA, Cambs. England (Receired 28 Noeemher 1978; accepted 15 March 1979) Abstract--1. In the newly-hatched domestic fowl, 5-HT creatinine sulphate (300pg/kg, intraabdominally) caused a fall in body temperature at high and low environmental temperatures. 2. The results are consistent with the hypothesis that 5-HT is an excitatory transmitter, acting on the warm receptor-heat loss pathway. INTRODUCTION
BLIGH et al. (1971) have pointed out the importance of the ambient temperature in experiments designed to determine the thermoregulatory response to the monoamines. 5-Hydroxytryptamine (5-HT) has been proposed as the excitatory neurotransmitter in the heat loss effector mechanisms of mammals (Feldberg & Myers, 1963, 1964, 1965; Bligh & Cottle, 1969; Bligh et al., 1971). In birds this monoamine has been found to have variable results (Table 1). Part of the variability can perhaps be explained in terms of age of the bird and route of injection, but the most important factor may well be the ambient temperature at which the experiments were done. In this note the effect of 5-HT on the body temperature of the newly hatched domestic fowl (Gallus domesticus) was determined at three environmental temperatures, 20, 35 and 40°C, these representing a cold, a thermally neutral and a hot environment, respectively.
bryonic period, therefore, monamines applied peripherally have both peripheral and central effects, allowing tentative conclusions to be made about their roles in the central control of thermoregulation. The results of the experiments are presented in Fig. 1 and Table 2. It will be noted that 5-HT caused significant falls in Tb compared with control birds at both high and low ambient temperatures. There was no effect on Tb at thermal neutrality. These findings confirm and extend those of Freeman (1970a). It appears that no similar studies on the domestic fowl have been published but it is noteworthy that 5-HT causes hypothermia in pigeons exposed to cold (Hissa & Rautenberg, 1975). The variability of the response of the fowl to 5-HT when kept in a thermally neutral environment is perplexing. Allen & Marley (1967) reported 5-HT to increase Tb when the bird was 12 days old but to have the opposite effect in the 15-day-old. In the present experiment 5-HT had no significant effect on Tb (Table 2). It is probable that part of the discrepancy
MATERIALS AND METHODS 41 -
The experiments were done on newly-hatched chicks of the Houghton Poultry Research Station's Light Sussex breed. They were not sexed and were not fed during the experiment. No chick was exposed to more than one environment. The birds were housed in an environmental cabinet (Egan & Butler, 1972) throughout the experiment, the temperature of which was controlled to within I deg C. Chicks received either saline (154raM) or 5-HT intraabdominally (300pg/kg: given as 5-HT creatinine sulphate). Colonic temperature (Tb) was measured using a thermistor probe (Yellow Spring Instruments) inserted through the cloaca to a standard depth (15 ram). The chicks were kept separated during the experiments.
i
20°C
35°C
40°C
37
8 a5
RESULTS AND DISCUSSION Normally monoamines that are applied peripherally are unable to penetrate the blood-brain barrier and therefore do not have any central effect. However, the blood-brain barrier of the newly-hatched chick is relatively permeable to monoamines (Callingham & Cass, 1966; Spooner et al., 1966; Hanig et al., 1970; Hanig & Seifter, 1973). The permeability of the barrier declines rapidly with age and is probably mature within a month of hatching. In the early postem-
33-
i
o
;
3'o Time
;
3'o
(mini
Fig. 1. Changes in colonic temperatures of birds injected intra-abdominally with 5-HT creatinine sulphate (300/~g active base/'kg) (e) or with saline (O) and exposed to three different ambient temperatures. Each point is the mean + SEM of 20 observations. 219
B. M. FREEMAN
220
Table 1. Effect of 5-HI on the body temperature (Tb) of three avian species Species
Effect++ on Tb
Age*
Route+
1 12 15
ia iv ia
~c
Freeman (1970a)
T tn
Allen & Marley (1967)
A A
3v ih
Ttn "1, Ttn§, - - tn~ /
Marley & Nistico (1975)
Pigeon (Columba livia)
A A
ih ia
~ c,--h ],e, "fh
Hissa & Rautenberg (19751 Hissa et al. (1975)
Japanese quail (Coturnix coturnix japonica)
A
ia
~ tn
Freeman (1970b)
Domestic fowl (Gallus domesticus)
~m
Reference
/
* Age in days; A = adult. t ia = intra-abdominal; ih = intra-hypothalamic; iv = intravenous; 3v = third ventricle. ,+The arrow indicates the direction of change in body temperature; - - = no effect. The letters following refer to the ambient temperature: tn = thermally neutral; c = below thermal neutrality; t, = above thermal neutrality. Increase with 5-HT hydrogen maleinate, no effect with 5-HT creatinine sulphate. Table 2. Effect of intra-abdominal 5-HT on the colonic temperature of chicks exposed to three ambient temperatures. Results expressed as the difference between saline-injected and 5-HT-injected birds + SE of difference Time (min)
Thermal neutrality (35)C)
Cold (20C)
Heat (40C)
0 30 60
0.0 _+ 0.07 0.0 +_ 0.13 0.2 _ 0.17
0.0 _+ 0.07 0.1 + 0.23 -0.7 _+ 0.31"
0.0 _+ 0.08 -0.5 + 0.18+ -0.7 +_ 0.16~
* P < 0.05. I P < 0.01. ~P < 0.001.
can be explained in terms of differences in the preparations of 5-HT (Roberts & Straughan, 1967). 5-HT hydrogen maleinate caused hypothermia in the experiments of Marley & Nisticb (1975) whereas 5-HT creatinine sulphate was without effect. This latter result is thus consistent with the present finding and that of Hissa & Rautenberg (1975) who used the pigeon. In view of the consistency of response to 5-HT at high and low ambient temperatures it seems reasonable to conclude that 5-HT has a role in the central control of thermoregulation. The demonstration of relatively high concentrations of this m o n o a m i n e in the hypothalamus (Juorio & Vogt, 1967) is consistent with this conclusion. That Tb falls following treatment of the newly-hatched chick with 5-HT creatinine sulphate suggests that the monoamine is an excitatory transmitter of the warm receptor-heat loss pathway.
REFERENCES
ALLEN D. J. & MARLEV E. (1967) Effect of sympathomimetic and allied amines on temperature and oxygen consumption in chickens. Br. J. Pharmac. Chemother. 31, 290-312. BLIGU J. & COTrLE W. H. (1969) The influence of ambient temperature on thermoregulatory responses to intraventricularly-injected monoamines in sheep, goats and rabbits. Experientia 25, 608-609. BLtGH J., COTTLE W. H. & MASKREY M. (1971) Influence of ambient temperature on the thermoregulatory re-
sponses to 5-hydroxytryptamine. noradrenaline and acetylcholine injected into the lateral cerebral ventricles of sheep, goats and rabbits. J. Physiol.. Lond. 212, 377-391. CALLINGHAM B. A. & CASS R. (19661 Catecholamines in the chick. In Physiology of the Domestic Fowl (Edited by HORTON-SMITH C. & AMOROSOE. C.), pp. 279-285. Oliver & Boyd, Edinburgh. EGAN B. J. & BUTLER E. J. (1972) Controlled environment systems for experimental animals- 1. A unidirectional air flow brooder for chicks. Lab. Anita. 6, 23-31. FELDBERG W. & MYERS R. D. (1963) A new concept of temperature regulation by amines in the hypothalamus. Nature, Lond. 200, 1325. FELDnER6 W. & MYERS R. D (1964) Effects on temperatures of amines injected into the cerebral ventricles. A new concept of temperature regulation. J. Physiol., Lond. 173, 226-237. FELDnERG W. & MYERS R. D. (1965) Changes in temperature produced by microinjections of amines into the anterior hypothalamus of cats. J. Physiol., Lond. 177, 239-245. FREEMAN B. M. (1970a)Thermoregulatory mechanisms of the neonate fowl. Comp. Biochem. Physiol. 33, 219-230. FREEMAN B. M. (1970b) Some aspects of thermoregulation in the adult Japanese quail (Coturnix eoturnix japonica). Comp. Biochem. Physiol. 34, 871-881. FREEMANB. M. (1978) Metabolic responses of the neonatal fowl, Gallus domesticus, to short-term heat stress. J. therm. Biol. 3, 49-50. HANIG J. P. & SEIFTER J. (1973) The effects of parenteral administration of catecholamines, serotonin and histamine on behaviour and levels of these amines in the brain of the neonate chick. Archs int. Pharmocodyn. Ther. 202, 38-47.
5-HT and avian thermoregulation HANIG J. P., AIELIO E. & SEIF'rER J. (1970) Permeability of the blood-brain barrier to parenteral 5-hydroxytryptamine in the neonate chick. Eur. J. Pharmac. 12, 180-182. HIssA R., SAARELAS. & PYORNILgA. (1975) Thermoregulatory effects of peripheral injections of monoamines on the pigeon. Comp. Biochem. Physiol. SIC, 235-241. JUORIO A. V. & VOGT M. (1967) Monoamines and their metabolites in the avian brain. J. Physiol., Lond. 189, 489-5 ! 8. MAaLEY E. & NISTIC6 G. (1975) Tryptamines and some other substances affecting waking and sleep in fowls. Br. J. Pharmac. 53, 193-205.
221
ROBERTSM. H. T. & STRAUGHAND. W. (1967) Excitation and depression of cortical neurones by 5-hydroxytryptamine. ,I. Physiol., Load. 193, 269-294. SPOONER C. E, WINTERSW. D. & MANDELLA. J. (1966) DL-Norepinephrine-7[H ~] uptake, water content, and thiocyanate space in the brain during maturation. Fedn. Proc. Fedn Am. Socs exp. Biol. 25, 451.
Key Word lndex--5-hydroxytryptamine, domestic fowl, thermoregulation.
IS 5-HYDROXYTRYPTAMINE CONCERNED IN AVIAN THERMOREGULATION? B. M. FREEMAN Houghton Poultry Research Station, Houghton, Huntingdon PEI7 2DA, Cambs. England (Receired 28 Noeemher 1978; accepted 15 March 1979) Abstract--1. In the newly-hatched domestic fowl, 5-HT creatinine sulphate (300pg/kg, intraabdominally) caused a fall in body temperature at high and low environmental temperatures. 2. The results are consistent with the hypothesis that 5-HT is an excitatory transmitter, acting on the warm receptor-heat loss pathway. INTRODUCTION
BLIGH et al. (1971) have pointed out the importance of the ambient temperature in experiments designed to determine the thermoregulatory response to the monoamines. 5-Hydroxytryptamine (5-HT) has been proposed as the excitatory neurotransmitter in the heat loss effector mechanisms of mammals (Feldberg & Myers, 1963, 1964, 1965; Bligh & Cottle, 1969; Bligh et al., 1971). In birds this monoamine has been found to have variable results (Table 1). Part of the variability can perhaps be explained in terms of age of the bird and route of injection, but the most important factor may well be the ambient temperature at which the experiments were done. In this note the effect of 5-HT on the body temperature of the newly hatched domestic fowl (Gallus domesticus) was determined at three environmental temperatures, 20, 35 and 40°C, these representing a cold, a thermally neutral and a hot environment, respectively.
bryonic period, therefore, monamines applied peripherally have both peripheral and central effects, allowing tentative conclusions to be made about their roles in the central control of thermoregulation. The results of the experiments are presented in Fig. 1 and Table 2. It will be noted that 5-HT caused significant falls in Tb compared with control birds at both high and low ambient temperatures. There was no effect on Tb at thermal neutrality. These findings confirm and extend those of Freeman (1970a). It appears that no similar studies on the domestic fowl have been published but it is noteworthy that 5-HT causes hypothermia in pigeons exposed to cold (Hissa & Rautenberg, 1975). The variability of the response of the fowl to 5-HT when kept in a thermally neutral environment is perplexing. Allen & Marley (1967) reported 5-HT to increase Tb when the bird was 12 days old but to have the opposite effect in the 15-day-old. In the present experiment 5-HT had no significant effect on Tb (Table 2). It is probable that part of the discrepancy
MATERIALS AND METHODS 41 -
The experiments were done on newly-hatched chicks of the Houghton Poultry Research Station's Light Sussex breed. They were not sexed and were not fed during the experiment. No chick was exposed to more than one environment. The birds were housed in an environmental cabinet (Egan & Butler, 1972) throughout the experiment, the temperature of which was controlled to within I deg C. Chicks received either saline (154raM) or 5-HT intraabdominally (300pg/kg: given as 5-HT creatinine sulphate). Colonic temperature (Tb) was measured using a thermistor probe (Yellow Spring Instruments) inserted through the cloaca to a standard depth (15 ram). The chicks were kept separated during the experiments.
i
20°C
35°C
40°C
37
8 a5
RESULTS AND DISCUSSION Normally monoamines that are applied peripherally are unable to penetrate the blood-brain barrier and therefore do not have any central effect. However, the blood-brain barrier of the newly-hatched chick is relatively permeable to monoamines (Callingham & Cass, 1966; Spooner et al., 1966; Hanig et al., 1970; Hanig & Seifter, 1973). The permeability of the barrier declines rapidly with age and is probably mature within a month of hatching. In the early postem-
33-
i
o
;
3'o Time
;
3'o
(mini
Fig. 1. Changes in colonic temperatures of birds injected intra-abdominally with 5-HT creatinine sulphate (300/~g active base/'kg) (e) or with saline (O) and exposed to three different ambient temperatures. Each point is the mean + SEM of 20 observations. 219
B. M. FREEMAN
220
Table 1. Effect of 5-HI on the body temperature (Tb) of three avian species Species
Effect++ on Tb
Age*
Route+
1 12 15
ia iv ia
~c
Freeman (1970a)
T tn
Allen & Marley (1967)
A A
3v ih
Ttn "1, Ttn§, - - tn~ /
Marley & Nistico (1975)
Pigeon (Columba livia)
A A
ih ia
~ c,--h ],e, "fh
Hissa & Rautenberg (19751 Hissa et al. (1975)
Japanese quail (Coturnix coturnix japonica)
A
ia
~ tn
Freeman (1970b)
Domestic fowl (Gallus domesticus)
~m
Reference
/
* Age in days; A = adult. t ia = intra-abdominal; ih = intra-hypothalamic; iv = intravenous; 3v = third ventricle. ,+The arrow indicates the direction of change in body temperature; - - = no effect. The letters following refer to the ambient temperature: tn = thermally neutral; c = below thermal neutrality; t, = above thermal neutrality. Increase with 5-HT hydrogen maleinate, no effect with 5-HT creatinine sulphate. Table 2. Effect of intra-abdominal 5-HT on the colonic temperature of chicks exposed to three ambient temperatures. Results expressed as the difference between saline-injected and 5-HT-injected birds + SE of difference Time (min)
Thermal neutrality (35)C)
Cold (20C)
Heat (40C)
0 30 60
0.0 _+ 0.07 0.0 +_ 0.13 0.2 _ 0.17
0.0 _+ 0.07 0.1 + 0.23 -0.7 _+ 0.31"
0.0 _+ 0.08 -0.5 + 0.18+ -0.7 +_ 0.16~
* P < 0.05. I P < 0.01. ~P < 0.001.
can be explained in terms of differences in the preparations of 5-HT (Roberts & Straughan, 1967). 5-HT hydrogen maleinate caused hypothermia in the experiments of Marley & Nisticb (1975) whereas 5-HT creatinine sulphate was without effect. This latter result is thus consistent with the present finding and that of Hissa & Rautenberg (1975) who used the pigeon. In view of the consistency of response to 5-HT at high and low ambient temperatures it seems reasonable to conclude that 5-HT has a role in the central control of thermoregulation. The demonstration of relatively high concentrations of this m o n o a m i n e in the hypothalamus (Juorio & Vogt, 1967) is consistent with this conclusion. That Tb falls following treatment of the newly-hatched chick with 5-HT creatinine sulphate suggests that the monoamine is an excitatory transmitter of the warm receptor-heat loss pathway.
REFERENCES
ALLEN D. J. & MARLEV E. (1967) Effect of sympathomimetic and allied amines on temperature and oxygen consumption in chickens. Br. J. Pharmac. Chemother. 31, 290-312. BLIGU J. & COTrLE W. H. (1969) The influence of ambient temperature on thermoregulatory responses to intraventricularly-injected monoamines in sheep, goats and rabbits. Experientia 25, 608-609. BLtGH J., COTTLE W. H. & MASKREY M. (1971) Influence of ambient temperature on the thermoregulatory re-
sponses to 5-hydroxytryptamine. noradrenaline and acetylcholine injected into the lateral cerebral ventricles of sheep, goats and rabbits. J. Physiol.. Lond. 212, 377-391. CALLINGHAM B. A. & CASS R. (19661 Catecholamines in the chick. In Physiology of the Domestic Fowl (Edited by HORTON-SMITH C. & AMOROSOE. C.), pp. 279-285. Oliver & Boyd, Edinburgh. EGAN B. J. & BUTLER E. J. (1972) Controlled environment systems for experimental animals- 1. A unidirectional air flow brooder for chicks. Lab. Anita. 6, 23-31. FELDBERG W. & MYERS R. D. (1963) A new concept of temperature regulation by amines in the hypothalamus. Nature, Lond. 200, 1325. FELDnER6 W. & MYERS R. D (1964) Effects on temperatures of amines injected into the cerebral ventricles. A new concept of temperature regulation. J. Physiol., Lond. 173, 226-237. FELDnERG W. & MYERS R. D. (1965) Changes in temperature produced by microinjections of amines into the anterior hypothalamus of cats. J. Physiol., Lond. 177, 239-245. FREEMAN B. M. (1970a)Thermoregulatory mechanisms of the neonate fowl. Comp. Biochem. Physiol. 33, 219-230. FREEMAN B. M. (1970b) Some aspects of thermoregulation in the adult Japanese quail (Coturnix eoturnix japonica). Comp. Biochem. Physiol. 34, 871-881. FREEMANB. M. (1978) Metabolic responses of the neonatal fowl, Gallus domesticus, to short-term heat stress. J. therm. Biol. 3, 49-50. HANIG J. P. & SEIFTER J. (1973) The effects of parenteral administration of catecholamines, serotonin and histamine on behaviour and levels of these amines in the brain of the neonate chick. Archs int. Pharmocodyn. Ther. 202, 38-47.
5-HT and avian thermoregulation HANIG J. P., AIELIO E. & SEIF'rER J. (1970) Permeability of the blood-brain barrier to parenteral 5-hydroxytryptamine in the neonate chick. Eur. J. Pharmac. 12, 180-182. HIssA R., SAARELAS. & PYORNILgA. (1975) Thermoregulatory effects of peripheral injections of monoamines on the pigeon. Comp. Biochem. Physiol. SIC, 235-241. JUORIO A. V. & VOGT M. (1967) Monoamines and their metabolites in the avian brain. J. Physiol., Lond. 189, 489-5 ! 8. MAaLEY E. & NISTIC6 G. (1975) Tryptamines and some other substances affecting waking and sleep in fowls. Br. J. Pharmac. 53, 193-205.
221
ROBERTSM. H. T. & STRAUGHAND. W. (1967) Excitation and depression of cortical neurones by 5-hydroxytryptamine. ,I. Physiol., Load. 193, 269-294. SPOONER C. E, WINTERSW. D. & MANDELLA. J. (1966) DL-Norepinephrine-7[H ~] uptake, water content, and thiocyanate space in the brain during maturation. Fedn. Proc. Fedn Am. Socs exp. Biol. 25, 451.
Key Word lndex--5-hydroxytryptamine, domestic fowl, thermoregulation.