5
Comp. Biochem. PhysioL, 1972, VoL 43A, pp. 125 to 129. PergamonPress. Printed in Great Britain ANTERIOR HYPOTHALAMIC/PREOPTIC LESIONS IMPAIR NORMAL THERMOREGULATION IN HOUSE SPARROWS STEVEN H. MILLS* and JAMES EDWARD HEATH Department of Physiology and Biophysics, University of Illinois, Urbana, Illinois 61801 (Received 1 ffanuary 1972) Abstract--1. Cloacal temperature was monitored via a thermocouple in un- restrained house sparrows before and after lesions were placed in and near the anterior hypothalamic/preoptic area (AH/POA). 2. Bilateral lesions in the AH/POA of house sparrows significantly impaired maintenance of constant body temperature below the therrnoneutral zone. 3. Since this thermoresponsive area is required for thermoregulation, some degree of homology between the AH/POA of birds and mammals must exist. INTRODUCTION A THERMORESPONSIVE area in the mammalian brain is localized in the anterior hypothalamic/preoptic area (AH/POA). This area is associated with the motor- integrative centers of temperature regulation in mammals. Lesions in the AH/POA prevent these mammals from maintaining a constant body temperature even though they are able to shiver or pant in response to thermal stimulation. Lesions more posteriorly in the median forebrain bundle interfere with control of heat gain and heat loss mechanisms (Hammel, 1968). Until recently, birds have not been subjected to the types of studies which permit localization and characterization of temperature regulation. Heat loss and heat gain mechanisms are altered or abolished in birds with lesions in the optic thalamus, the diencephalon or near the anterior commissure and median forebrain bundle of the hypothalamus. Lesions in some of these areas interfere with several vital functions including temperature regulation in proportion to the amount of tissue destroyed (Feldman et al., 1957; Kanematsu et al., 1967; Lepkovsky et aL, 1968; Rogers & Lackey, 1923; Singh, 1959). The responses of birds with lesions in areas which have previously been assigned a localized property such as thermoresponsiveness have not been tested. Early studies demonstrated peripheral and central temperature sensitivity in birds. Thermal stimulation of the thalamus, viscera or spinal cord induced thermogenesis which was facilitated by peripheral thermal stimulation (Rogers, 1928; Randall, 1943). We have localized and described a thermoresponsive area in the brain of house sparrows which includes the AH]POA. Localized cooling in the * Present address: Space Sciences Research Center, Research Park, University of Missouri, Columbia, Missouri 65201. 125

Anterior hypothalamic/preoptic lesions impair normal thermoregulation in house sparrows

Embed Size (px)

Citation preview

Page 1: Anterior hypothalamic/preoptic lesions impair normal thermoregulation in house sparrows

Comp. Biochem. PhysioL, 1972, VoL 43A, pp. 125 to 129. Pergamon Press. Printed in Great Britain

ANTERIOR HYPOTHALAMIC/PREOPTIC LESIONS IMPAIR NORMAL THERMOREGULATION IN HOUSE

SPARROWS

STEVEN H. M I L L S * and JAMES EDWARD H E A T H

Department of Physiology and Biophysics, University of Illinois, Urbana, Illinois 61801

(Received 1 ffanuary 1972)

Abstract--1. Cloacal temperature was monitored via a thermocouple in un- restrained house sparrows before and after lesions were placed in and near the anterior hypothalamic/preoptic area (AH/POA).

2. Bilateral lesions in the AH/POA of house sparrows significantly impaired maintenance of constant body temperature below the therrnoneutral zone.

3. Since this thermoresponsive area is required for thermoregulation, some degree of homology between the AH/POA of birds and mammals must exist.

INTRODUCTION A THERMORESPONSIVE area in the mammalian brain is localized in the anterior hypothalamic/preoptic area (AH/POA). This area is associated with the motor- integrative centers of temperature regulation in mammals. Lesions in the AH/POA prevent these mammals from maintaining a constant body temperature even though they are able to shiver or pant in response to thermal stimulation. Lesions more posteriorly in the median forebrain bundle interfere with control of heat gain and heat loss mechanisms (Hammel, 1968). Until recently, birds have not been subjected to the types of studies which permit localization and characterization of temperature regulation. Heat loss and heat gain mechanisms are altered or abolished in birds with lesions in the optic thalamus, the diencephalon or near the anterior commissure and median forebrain bundle of the hypothalamus. Lesions in some of these areas interfere with several vital functions including temperature regulation in proportion to the amount of tissue destroyed (Feldman et al., 1957; Kanematsu et al., 1967; Lepkovsky et aL, 1968; Rogers & Lackey, 1923; Singh, 1959). The responses of birds with lesions in areas which have previously been assigned a localized property such as thermoresponsiveness have not been tested.

Early studies demonstrated peripheral and central temperature sensitivity in birds. Thermal stimulation of the thalamus, viscera or spinal cord induced thermogenesis which was facilitated by peripheral thermal stimulation (Rogers, 1928; Randall, 1943). We have localized and described a thermoresponsive area in the brain of house sparrows which includes the AH]POA. Localized cooling in the

* Present address: Space Sciences Research Center, Research Park, University of Missouri, Columbia, Missouri 65201.

125

Page 2: Anterior hypothalamic/preoptic lesions impair normal thermoregulation in house sparrows

126 STm~¢ H. MILLS AND JAMES EDWARD HEATH

preoptic area elicited an increase in oxygen consumption and heat conservation while localized heating decreased oxygen consumption and facilitated heat loss. Localized thermal stimulation in areas outside the preoptic area, such as the fore- brain and ventral hypothalamus, did not elicit predictable changes in thermo- regulatory parameters (Mills & Heath, 1970; Mills & Heath, 1972). We will show that this thermoresponsive area of the avian brain is required for thermoregulation.

MATERIALS AND METHODS Adult male house sparrows, Passer domesticus, with a mean weight of 25"5 +_ 3"2 g w e r e

captured locally during May and June. All birds were maintained with food and water ad//b. in flight cages at 22°C on a 12-12 hr light cycle.

A small bird adaptor for the calibrated Kopf stereotaxic apparatus was used to secure the bird's skull. Ether was administered throughout the procedure. The scalp was incised, and a hole bored 0"7 mm lateral to the midline, and 8"5 mm posterior from the midline junction of the bill with the skull. Bilateral electrolytic lesions were placed in and near the anterior hypothalamus, preoptic area and forebrain of these birds after testing them for thermo- regulatory ability.

Thermoregulatory ability of each bird was tested by placing it in a temperature controlled cabinet and recording its body temperature over a range of air temperatures. Activity was restricted by the small size of the 24 x 15 x 10 cm chamber and minimized by using a one- way observation window. Body temperature was monitored 1 cm within the cloaca with a thermocouple while air temperature was slowly increased or decreased at a mean rate of 6"8°C/hr over the range of 10-40°C.

RESULTS AND DISCUSSION T h e AH/POA is located with respect to other brain structures in sagittal view

0.5 mm laterally from the midline in Fig. 1A. Sagittal composites of lesion posi- tions in the brain of birds are represented with their respective responses to air temperature in Figs. 1B and 1C. T h e composite from four birds with lesions in the forebrain represents sham-operated controls. T h e composite in Fig. 1C from three birds with lesions in the AH/POA represents birds with lesions in the thermo- responsive area.

Body temperatures of sparrows sampled at 10-min intervals during slowly changing air temperature are recorded in Fig. 1A, 1B and 1C. Normal birds maintain body temperature relatively constant over the range of 10-32°C air temperature (Fig. 1A). Fig. 1B represents the responses of birds with forebrain lesions to a range of air temperatures. T h e linear regression of this relationship has a slope of 0.06. T h e body temperatures of normal birds (Fig. 1A) and of birds with lesions in the forebrain (Fig. 1B) have distributions which are parallel and independent of air temperature below 32°C. However, body temperatures of forebrain-lesioned birds tend to be lower than those of normal birds below the thermoneutral zone. T h e open circles in Fig. 1A represent the mean body tem- perature of twelve non-lesioned house sparrows reported by Hudson & Kimsey

Page 3: Anterior hypothalamic/preoptic lesions impair normal thermoregulation in house sparrows

A N T E R I O R H Y P O T H A L A M I C / P R E O P T I C L E S I O N S I N H O U S E S P A R R O W S

~ - . . . . . " , ' . -~ '2~ . 8 It "J 4 0 ~ oo°1o., • .Io • • - • o B, • o°~ o o. • • ° -

36

32

3O

28

I- I t I I I I l l I I I I I I I

44~- FOREBRAIN LESIONED • • ° • o B 42[- . . . . • . • .•

~ 3a ~ -.." . . - ' . "-- . ~- 34 ~ 3z ~ 3o ~ 28 ~ M

I I I I I I I I I L I I t i

,q4 AH /POA LESIONED . . "J~''~'C-- • • l

:

34 • ° •° "• ° • l ~°

32 , ° ° ° ° °

I I I I T I I I 1 I I I .L I I I I ] Io I z 14 16 B 20 zz 24 zs zs 3o 3z 34 36 38 40 4 2 4 4

A i r T e m p e r a t u r e ( °C )

FIG. 1. Body temperatures of lesioned and non-lesioned house sparrows are repre- sented with the appropriate sagittal composite of their brain indicating lesion loca- tions. The closed circles (O) represent body temperatures sampled at 10-rain intervals while changing air temperature by 6"8°C/hr. The lines represent the linear regression of these distributions. The open circles (O) represent previously re- ported mean responses (Hudson & Kimsey, 1966). AH, anterior hypothalamus; APH, area parahippocampalis; CA, commissura anterior; CO, chiasma opticum; LPO, lobus parolfactorius; HA, hyperstriatum accessorittm; HV, hyperstriatum ventrale; NC, neostriatum caudale; POA, nucleus preopticus anterior; DM, nucleus dorsomedialis thalami; V. ventriculus. (Abbreviations from Karten &

Hodos, 1967.)

127

Birds with lesions in the AH/POA do not maintain a constant body temperature when air temperature is decreased (Fig. 1C). The linear regression of this distribu- tion has a slope of 0-53. Sparrows with lesions in this area have body temperatures which are significantly lower ( P < 0.05) than birds with no lesions or b irdswi th

Page 4: Anterior hypothalamic/preoptic lesions impair normal thermoregulation in house sparrows

128 STm~a~ H. MILLS AND JAMSS EDWARD HEATH

lesions in the forebrain. Thus, the AH/POA contain structures required for facilitation of the peripherally elicited thermoregulatory responses.

Several causes for loss in thermoregulatory ability in lesioned birds are possible: (1) presence of a lesion anywhere in the brain, (2) interruption of inputs to the thermoregulatory center or (3) destruction of the thermoregulatory center. In this study, we were interested in the effect of disrupting the input from central receptors although we may have simultaneously destroyed thermoregulation. Since lesions in the forebrain did not destroy thermoregulation, the response of birds to lesions in the AH/POA was not due to the surgery or non-specific destruction of brain tissue.

Central nervous sensitivity is a common property of the AH/POA of birds and mammals. In most mammals studied, the area in the brain which is thermo- responsive is involved in thermoregulation (Hammel, 1968). However, there is an area in the brain of bats which is thermoresponsive but not required for thermo- regulation (Kluger & Heath, 1971a, b).

Although Rautenberg (1969, 1971) has suggested that spinal thermal re- sponsiveness is a major factor driving thermoregulation in birds, we have demon- strated a thermoresponsive area in the avian brain which is required for thermo- regulation. Since thermoregulation can be destroyed with lesions in the thermo- responsive area of house sparrows as well as many mammals, some degree of homology between central nervous regulation of body temperature in birds and mammals must exist.

`4cknowledgement--This work was supported in part by N.S.F. grant GB 13797 and a departmental research assistantship.

REFERENCES Fm.DMAN S. E., LARSSON S., DIMICK M. K. & LEPKOVSKY S. (1957) Aphagia in chickens.

Am. ~. Physiol. 191, 259-261. HAMMEL H. T. (1968) Regulation of internal body temperature..4. Rev. Physiol. 30,

641-709. HUDSON J. W. & KIMS~" S. L. (1966) Temperature regulation and metabolic rhythms of the

house sparrow, Passer domesticus. Comp. Biochem. Physiol. 17, 203-217. KANEMATSU S., KII M., SONODA T. ~ KATO Y. (1967) Effects of hypothalamic lesions on

body temperature in the chicken, flap.ft, vet. Sci. 29, 95-104. I~aTarq H. J. & HOBOS W. (1967) .4 Stereotaxic Atlas of the Brain of the Pigeon (Columba

livia). The Johns Hopkins Press, Baltimore. KLUCFat M. J. & HEATH J. E. (1971a) Fluctuations in the preoptic-anterior hypothalamic

temperature in the bat ( Eptesiens fusens). Comp. Biochem. Physiol. 40, 809-814. KLUGm~ M. J. & HEATH J. E. (1971b) Effect of preoptic anterior hypothalamic lesions on

thermoregulation in the bat. `4m..7. Physiol. 221, la, a. 149. LEPKOVSKY S., SNAP/N N. & FtmATA F. (1968) Temperature regulation and appetitive be-

havior in chickens with hypothalamie lesions. Physiol. Behav. 3, 911-915. MILLS S. H. & HEATH J. E. (1970) Thermoresponsiveness of the preoptie region of the brain

in house sparrows. Science 168, 1008-1009. MmLs S. H. & HEATH J. E. (1972) Responses to thermal stimulation of the preoptic area in

the house sparrow, Passer domesticus. Am. jq. Physiol. (In press.)

Page 5: Anterior hypothalamic/preoptic lesions impair normal thermoregulation in house sparrows

ANTERIOR HYPOTHALANIIC/PREOPTIC LESIONS IN HOUSE SPARROWS 129

RANDALL W. C. (1943) Alterations in response to changing body temperature following artificial fever and chilling. Proc. Soc. exp. Biol. Med. 52, 240--245.

RAISTENBERa W. (1969) Die Bedeutung der zentralnervosen Thermosensitivitiit fiir die Temperaturregulation der Taube. Z. vergl. Physiol. 62, 235-266.

RAUTENBERG W. (1971) The influence of the skin temperature on the thermoregulatory system of pigeons, ft. Physiol., Paris 63, 346-398.

ROOERS F. T. (1928) Studies of the brain stem--XI. The effects of artificial stimulation and traumatism of the avian thalamus. Am. ft. Physiol. 86, 639--650.

ROOERS F. T. • LACKEY R. W. (1923) Studies of the brain s tem--VII . The respiratory exchange and heat production after destruction of body temperature-regulatory centers of thalamus. Am. ft. Physiol. 66, 453-460.

SINGH M. P. (1959) Observations on the organization of the panting center in avian brain. XXlst Int. Congress Physiol. Sci., Buenos Aires.

Key Word Index---Hypothalamus; preoptie area; electrolytic lesions; thermoregulation; body temperature; Passer domesticus.