Journal of Applied Physiology
Vol. 83, No. 3, pp. 830-836, September 1997
CONTROL OF BREATHING, CIRCULATION, AND TEMPERATURE

Autonomic and behavioral thermoregulation in guinea pigs during postnatal maturation

James E. Fewell, Maria Kang, and Heather L. Eliason

Department of Physiology and Biophysics, The University of Calgary Health Sciences Centre, Calgary, Alberta, Canada T2N 4N1

ABSTRACT

INTRODUCTION

METHODS

RESULTS

DISCUSSION

ACKNOWLEDGEMENTS

FOOTNOTES

REFERENCES

ABSTRACT

Fewell, James E., Maria Kang, and Heather L. Eliason. Autonomic and behavioral thermoregulation in guinea pigs during postnatal maturation. J. Appl. Physiol. 83(3): 830-836, 1997.Serial experiments were carried out on seven chronically instrumented Hartley-strain guinea pigs at 1, 3, and 5 wk of age to define their autonomic and behavioral thermoregulatory profiles and to test the hypothesis that they have the mechanisms in place shortly after birth that allow them to optimize their energy expenditure for thermoregulation by selecting a thermal environment that requires the lowest metabolic oxygen requirements. Each animal was studied in both a thermocline to determine selected ambient temperature and in a metabolic chamber to determine the thermoregulatory response to forced changes in ambient temperature. In the thermocline, the guinea pigs at all postnatal ages selected an ambient temperature that placed core temperature, oxygen consumption, thermal conductance, heart rate, and respiratory rate at levels comparable to those observed at ambient temperatures in which minimal oxygen consumption occurred in the metabolic chamber. Thus our experiments provide evidence that guinea pigs have the neurophysiological mechanisms in place shortly after birth that allow them to optimize their energy expenditure for thermoregulation by selecting a thermal environment that corresponds to the lowest metabolic oxygen requirements.

core temperature; newborn

INTRODUCTION

GUINEA PIGS are born relatively mature. They can move around within minutes after birth, are pelted, have open eyes, and may not even have to suckle but can eat "real" food immediately (15). Similar to other newborn mammals, their primary requirements are food, protection, and warmth. Guinea pigs are homeotherms and employ both their somatomotor nervous system (e.g., behavioral thermogenesis, shivering thermogenesis) and the sympathetic portion of their autonomic nervous system (e.g., nonshivering thermogenesis, changes in vasomotor tone) as thermoregulatory effectors to maintain a stable core temperature. Newborn guinea pigs primarily utilize nonshivering thermogenesis in brown adipose tissue as opposed to shivering thermogenesis to generate heat during exposure to cold (7) and during febrigenesis (4).

Before birth, the guinea pig fetus grows in the warm environment of the uterus. In all species studied to date [i.e., humans (2, 17), baboons (14), sheep (1), dogs (2), and rabbits (10)], core temperature of the fetus is ~0.5°C higher than that of the mother. Immediately after birth, the newborn must expend energy not only for growth but also to maintain its core temperature at or near the central nervous system "set-point" temperature. Considering the high energy requirements for growth during early postnatal life and the fact that most newborns have limited food supplies, it would be advantageous for the newborn guinea pig to use behavioral thermogenesis rather than nonshivering thermogenesis as a thermoregulatory effector. This would avoid not only the hazards of hypothermia but also wastage of energy on heat production, and thus more would be available for growth. The present experiments were carried out to define the autonomic and behavioral thermoregulatory profiles of newborn and older guinea pigs to test the hypothesis that they have the mechanisms in place shortly after birth that allow them to optimize their energy expenditure for thermoregulation by selecting a thermal environment that requires the lowest metabolic oxygen requirements.

METHODS

Seven Hartley-strain guinea pigs were studied. Each pup was born by spontaneous vaginal delivery and was housed with its dam and siblings in an environmental chamber (22 ± 1°C, 20-30% relative humidity, and 12:12-h light-dark cycle) between experiments.

Surgical Preparation

Experimental Protocol

Experimental Apparatus

Experimental Measurements and Calculations

Statistical Analysis

RESULTS

Core temperature was significantly influenced in an overall fashion by ambient temperature (P = 0.000) but not by postnatal age (P = 0.530) (Fig. 1); there was not an interaction between ambient temperature and postnatal age on core temperature (P = 0.586). Core temperature increased and decreased, respectively, at all ages when the ambient temperature of the metabolic chamber was set above and below the ambient temperature at which minimal oxygen consumption occurred. Core temperatures measured when the animals were in the thermocline were similar to those measured when the animals were in the metabolic chamber at the ambient temperatures at which minimal oxygen consumption occurred at all ages. Core temperature increased at 5 wk compared with 1 and 3 wk both when the animals were in the thermocline and when the animals were in the metabolic chamber at the ambient temperature at which minimal oxygen consumption occurred. Selected ambient temperature did not change significantly with increasing age (mode: 33 ± 2, 33 ± 3, and 34 ± 2°C; mean: 32 ± 3, 32 ± 2, and 31 ± 2°C; mode/mean ± SD for weeks 1, 3, and 5, respectively).

Oxygen consumption was significantly influenced in an overall fashion by ambient temperature (P = 0.000) and postnatal age (P = 0.029) (Fig. 2); there was not an interaction between ambient temperature and postnatal age on oxygen consumption (P = 0.084). The minimal rate of oxygen consumption occurred at ambient temperatures of 32, 34, and 36°C, respectively, during weeks 1, 3, and 5 of postnatal life, respectively, as the ambient temperature was varied from 14 to 36°C in the metabolic chamber. Oxygen consumption rates measured when the animals were in the thermocline were similar to those measured when the animals were in the metabolic chamber at the ambient temperatures at which minimal oxygen consumption occurred at all ages. Neither oxygen consumption measured in the thermocline nor oxygen consumption measured in the metabolic chamber at the ambient temperature at which minimal oxygen consumption occurred was influenced by postnatal age. The lower critical temperature increased from ~24°C during weeks 1 and 3 of postnatal life to ~28°C during week 5 of postnatal life.

Thermal conductance was significantly influenced in an overall fashion by ambient temperature (P = 0.000) but not by postnatal age (P = 0.068) (Fig. 3); there was not an interaction between ambient temperature and postnatal age on thermal conductance (P = 0.247). Thermal conductances measured when the animals were in the thermocline were similar to those measured when the animals were in the metabolic chamber at the ambient temperatures at which minimal oxygen consumption occurred at all ages. Thermal conductance increased at week 5 compared with weeks 1 and 3 both when the animals were in the thermocline and when the animals were in the metabolic chamber at the ambient temperature at which minimal oxygen consumption occurred. The threshold for an increase in thermal conductance decreased from ~32°C in the 1-wk-old guinea pigs to ~30°C in the 3- and 5-wk-old guinea pigs.

Heart rate was significantly influenced in an overall fashion by ambient temperature (P = 0.000) and postnatal age (P = 0.031) (Fig. 4); there was a significant interaction between ambient temperature and postnatal age on heart rate (P = 0.010). Heart rates measured when the animals were in the thermocline were similar to those measured when the animals were in the metabolic chamber at the ambient temperatures at which minimal oxygen consumption occurred at a given postnatal age. Heart rate increased at weeks 3 and 5 compared with week 1 of postnatal age when the animals were in the thermocline and when the animals were in the metabolic chamber at the ambient temperature at which minimal oxygen consumption occurred.

Respiratory rate was significantly influenced in an overall fashion by ambient temperature (P = 0.000) and by postnatal age (P = 0.031) (Fig. 5); there was a significant interaction between ambient temperature and postnatal age on respiratory rate (P = 0.000). Respiratory rates measured when the animals were in the thermocline were similar to those measured when the animals were in the metabolic chamber at the ambient temperatures at which minimal oxygen consumption occurred at a given postnatal age. Respiratory rate increased at week 5 compared with weeks 1 and 3 of postnatal age when the animals were in the thermocline and when the animals were in the metabolic chamber at the ambient temperature at which minimal oxygen consumption occurred.

DISCUSSION

Our experiments provide new information about thermoregulatory control during postnatal maturation in guinea pigs. Novel findings in our study were that 1) guinea pigs at all postnatal ages selected an ambient temperature in the thermocline that placed core temperature, oxygen consumption, thermal conductance, heart rate, and respiratory rate at levels comparable to those observed at ambient temperatures at which minimal oxygen consumption occurred in the metabolic chamber; 2) guinea pigs at all postnatal ages selected an ambient temperature in the thermocline that was above their lower critical temperature and was similar to the threshold temperature for an increase in thermal conductance as determined in the metabolic chamber; and 3) 1-wk-old guinea pigs maintained their core temperature better than did 3- and 5-wk-old guinea pigs as ambient temperature was decreased below their lower critical temperature.

These data provide evidence that guinea pigs have the neurophysiological mechanisms in place shortly after birth that allow them to optimize their energy expenditure for thermoregulation by selecting a thermal environment that corresponds to the lowest metabolic oxygen requirements that occur over the temperature range of 14 to 36°C. This may have important ramifications for survival and for growth because it will avoid not only the hazards of hypothermia but also wastage of energy on heat production, and thus more will be available for growth. This factor is of considerable importance, for most newborn mammals have limited food reserves. Estimates of energy expenditures for growth in rapidly growing precocial species may be as much as 30-35% of the basal metabolic rate (13). Whether or not the newborn guinea pig can achieve these optimal conditions of core temperature and oxygen consumption in an environment where ambient temperature is below that in which minimal oxygen consumption occurs by utilizing behavioral thermoregulation (i.e., by huddling with its mother and siblings) remains to be determined.

It has previously been suggested that the "comfortable temperature" for the newborn is often intolerable for the adult (11). This does not appear to be the case for the precocial guinea pig because Gordon (9) has previously shown that the selected ambient temperature for an adult male guinea pig [i.e., mode 32°C; mean 31 ± 4 (SD) °C] is only a degree or two below that observed in the present study. If one compares the thermoregulatory profiles for the adult as reported by Gordon (9) with that of the newborn in this species, core temperature and the lower critical temperature appear to differ. In the adult, the core temperature is 38.9 ± 0.2°C at the ambient temperature at which minimal oxygen consumption occurs (9), whereas in our study core temperature under similar conditions was 39.2 ± 0.2, 39.5 ± 0.3, and 40.1 ± 0.5°C at 1, 3, and 5 wk of age, respectively. In the adult, the lower critical temperature is ~20°C (9), whereas in the present study we found the lower critical temperature to be ~24°C during weeks 1 and 3 of postnatal life to ~28°C during week 5 of postnatal life. The threshold for an increase in thermal conductance, however, appears to be similar in the adult (9) and young guinea pig during postnatal maturation (i.e., ~30-32°C).

Although we did not measure evaporative water loss, if one assumes that the pattern of thermal conductance follows the pattern of evaporative water loss in the young guinea pig as it does in the adult (9), then the thermoneutral zone, defined as the range of ambient temperature within which the metabolic rate is at a minimum and within which temperature regulation (i.e., a stable core temperature) is achieved by nonevaporative physical processes alone (5, 12), is ~20-28°C in the adult guinea pig and ~24-30, ~24-30, and 28-30°C during weeks 1, 2, and 3 of postnatal life, respectively. At ambient temperatures below the lower critical temperature, 1-wk-old guinea pigs maintained their core temperature, whereas 3- and 5-wk-old guinea pigs did not. Core temperature decreased below ambient temperatures of 20 and 24°C, respectively, in the 3- and 5-wk-old guinea pigs. Similarly, Dawes and Mestyan (8) found that guinea pigs were able to maintain their core temperature on exposure to cold within 2 days after birth, and often much earlier. Interestingly, Gordon (9) found that core temperature fell in adult guinea pigs when the ambient temperature was decreased below their lower critical temperature. The remarkable ability of the 1-wk-old guinea pig to maintain its core temperature as ambient temperature was decreased below the lower critical temperature may be related to the peak capacity for heat generation by nonshivering thermogenesis in brown adipose tissue that this precocial species has shortly after birth (15).

Basal heart rate and respiratory rate, measured in the thermocline or at the ambient temperature at which minimal oxygen consumption occurred, increased with postnatal age. The pattern of change of heart rate mirrored the pattern of change of oxygen consumption as ambient temperature was varied. This is not surprising, considering that heart rate is a determinant of cardiac output, and an increase in cardiac output would be the primary mechanism by which oxygen supply (i.e., systemic oxygen transport) would be increased to meet an increase in oxygen demand. The pattern of change of respiratory rate mirrored the pattern of change of oxygen consumption as ambient temperature was decreased but increased over and above a pattern of stable oxygen consumption at the higher ambient temperatures most likely in an attempt to dissipate heat.

In summary, our study provides new information on the autonomic and behavioral thermoregulatory profiles of newborn guinea pigs and how they compare to that of the adult as well as providing evidence that guinea pigs have mechanisms in place shortly after birth that allow them to optimize their energy expenditure for thermoregulation by selecting a thermal environment that corresponds to the lowest metabolic oxygen requirements.

ACKNOWLEDGEMENTS

The authors thank Dr. Francine G. Smith for critical review of this manuscript.

FOOTNOTES

Address for reprint requests: J. E. Fewell, Heritage Medical Research Bldg., 206, The Univ. of Calgary, 3330 Hospital Drive, N.W., Calgary, Alberta, Canada T2N 4N1 (E-mail: fewell{at}acs.ucalgary.ca).

Received 17 January 1997; accepted in final form 7 May 1997.

REFERENCES