Comprehensive Physiology Wiley Online Library

Ontogenetic and Adaptive Adjustments in the Thermoregulatory System

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 Ontogenetic Adjustments in the Thermoregulatory System
1.1 Stability of Core Temperature during Ontogenesis
1.2 Changes in the Passive System and the Thermoregulatory Effort on Cold Exposure
1.3 Shift in Cutaneous Thermoregulatory Sensitivity
2 Similarities Between Thermoregulatory Peculiarities of Neonates and Thermally Acclimated Adults
2.1 Adaptive Deviations in Shivering and Sweating Threshold Temperatures
2.2 Stage of Maturity of the Thermoregulatory System at Birth
2.3 Effects of Maternal and Fetal Temperatures on the Neonate
3 Early Thermal Imprinting and Adult Temperature Acclimation
3.1 Thermal Acclimation—Early Imprinting
3.2 Acclimation vs. Maturation
3.3 Long‐Term Threshold Temperature Displacement
3.4 Short‐Term Threshold Temperature Displacement
3.5 Temperature lmprinting
3.6 Neurophysiological Correlates of Thermoadaptive Threshold Deviations
4 Effects of Hypoxia (Altitude) and Hypercapnia on Heat Balance
4.1 Acute and Chronic Hypoxia
4.2 Effects of Fetal Hypoxia on the Neonate
5 Summary
Figure 1. Figure 1.

Colonic temperatures in guinea pigs and rabbits in relation to age and ambient temperature (Ta). After data from references 20, 71.

Figure 2. Figure 2.

Metabolic responses in relation to ambient temperature and age in the guinea pig. Lower diagram: contribution of NST. From references 20, 22.

Figure 3. Figure 3.

Course of rectal temperatures and heat production in full‐term newborn infants. Ambient temperature up to the arrow 33°C, then 23°C. From reference 9.

Figure 4. Figure 4.

Relation of SMR to body mass and age in humans. From reference 11.

Figure 5. Figure 5.

Heat production necessary to maintain a given ΔT in human subjects of size 1, 2, 3. From reference 11, see text. ΔT, difference between body core (37°C) and environment (To). Size 1, adult; 2, 3 kg infant; 3, 1.5 kg infant.

Figure 6. Figure 6.

Survey of possible deviations of the thresholds for heat production and dissipation. Open circles indicate set‐point displacement. Tb, mean body temperature; Tes, esophageal temperature; SMR, standard metabolic rate.

Figure 7. Figure 7.

Minimal (basal or standard) and maximal metabolic rates in relation to ambient temperature in the neonate (N) and the adult (A).

Figure 8. Figure 8.

Left: Simultaneous responses of skin blood flow (heel) and heat production to a slight drop in mean skin temperature (Ts) evoked by a decrease in ambient temperature (Ta) from 32° to 28°C. Study in a 7 day old infant, 3,290 g. After references 9, 11, 26. Right: Relationship between Ts and heat production in adults and newborn infants and thermal conductance (peripheral blood flow) in relation to mean skin temperature in neonates and adults. Note onset of responses at higher body temperatures in the neonate 11.

Figure 9. Figure 9.

Shivering threshold curves for two groups of guinea pigs (aged 4–8 wk) reared at different environmental temperatures. Values obtained by independent changes of body surface temperature and temperature in the cervical vertebral canal. Diagram shows, for instance, that at a certain body surface temperature, which corresponds to a subcutaneous temperature of 37°C, shivering begins in warm‐adapted animals (◯) when hypothalamic temperature drops below 40°C. In cold‐adapted animals (•), however, shivering does not occur until hypothalamic temperature has reached a value slightly below 39°C. From reference 21.

Figure 10. Figure 10.

Cooling test in a young man. Shivering threshold is shifted to a lower level of mean body temperature at the second cooling phase after short rewarming (insert, right). Ta, ambient temperature; Tsk, mean skin temperature; Tb(ty), mean weighted body temperature (Tb(ty) = 0.9 X Tty + 0.1 x Tsk); Tty, tympanic temperature; EMA, electrical muscle activity from muscle latissimus dorsi; Vo2 oxygen uptake.

From V. Schmidt, K. Brück, and P. Hinckel, unpublished data.
Figure 11. Figure 11.

Connectivity model. Tentative mode of thermoafferent systems with special reference to the adult guinea pig's thermoregu latory brain stem pathways, mainly originating in two lower brain stem centers. Projections from the subcoeruleus region (SC) ascend tointegrative interneuronal networks in the posterior hypothalamus determining the thresholds of heat production mechanisms. Excit atory pathways ascend from the subcoeruleus area to the heat production effector networks. Subcoeruleus cell groups are innervatedfrom skin cold receptors (CR). Trunk skin warm receptors (WR) havebeen shown to project to 5‐HT NRM cells. Projections from the NRM ascend to the integrative hypothalamic networks controlling shiveringand descend to the dorsal horn. Parallel pathways take conventionalroutes ascending from the WR via the dorsal horn to the nucleusreticularis gigantocellularis (NRG), to the nucleus raphe dorsalis and the adjacent central gray matter (PAG), and to the thalamus and sensory cortex. For further explanation see text. Symbols:—, inhibitory connections; ——⊲, excitatory connections.



Figure 1.

Colonic temperatures in guinea pigs and rabbits in relation to age and ambient temperature (Ta). After data from references 20, 71.



Figure 2.

Metabolic responses in relation to ambient temperature and age in the guinea pig. Lower diagram: contribution of NST. From references 20, 22.



Figure 3.

Course of rectal temperatures and heat production in full‐term newborn infants. Ambient temperature up to the arrow 33°C, then 23°C. From reference 9.



Figure 4.

Relation of SMR to body mass and age in humans. From reference 11.



Figure 5.

Heat production necessary to maintain a given ΔT in human subjects of size 1, 2, 3. From reference 11, see text. ΔT, difference between body core (37°C) and environment (To). Size 1, adult; 2, 3 kg infant; 3, 1.5 kg infant.



Figure 6.

Survey of possible deviations of the thresholds for heat production and dissipation. Open circles indicate set‐point displacement. Tb, mean body temperature; Tes, esophageal temperature; SMR, standard metabolic rate.



Figure 7.

Minimal (basal or standard) and maximal metabolic rates in relation to ambient temperature in the neonate (N) and the adult (A).



Figure 8.

Left: Simultaneous responses of skin blood flow (heel) and heat production to a slight drop in mean skin temperature (Ts) evoked by a decrease in ambient temperature (Ta) from 32° to 28°C. Study in a 7 day old infant, 3,290 g. After references 9, 11, 26. Right: Relationship between Ts and heat production in adults and newborn infants and thermal conductance (peripheral blood flow) in relation to mean skin temperature in neonates and adults. Note onset of responses at higher body temperatures in the neonate 11.



Figure 9.

Shivering threshold curves for two groups of guinea pigs (aged 4–8 wk) reared at different environmental temperatures. Values obtained by independent changes of body surface temperature and temperature in the cervical vertebral canal. Diagram shows, for instance, that at a certain body surface temperature, which corresponds to a subcutaneous temperature of 37°C, shivering begins in warm‐adapted animals (◯) when hypothalamic temperature drops below 40°C. In cold‐adapted animals (•), however, shivering does not occur until hypothalamic temperature has reached a value slightly below 39°C. From reference 21.



Figure 10.

Cooling test in a young man. Shivering threshold is shifted to a lower level of mean body temperature at the second cooling phase after short rewarming (insert, right). Ta, ambient temperature; Tsk, mean skin temperature; Tb(ty), mean weighted body temperature (Tb(ty) = 0.9 X Tty + 0.1 x Tsk); Tty, tympanic temperature; EMA, electrical muscle activity from muscle latissimus dorsi; Vo2 oxygen uptake.

From V. Schmidt, K. Brück, and P. Hinckel, unpublished data.


Figure 11.

Connectivity model. Tentative mode of thermoafferent systems with special reference to the adult guinea pig's thermoregu latory brain stem pathways, mainly originating in two lower brain stem centers. Projections from the subcoeruleus region (SC) ascend tointegrative interneuronal networks in the posterior hypothalamus determining the thresholds of heat production mechanisms. Excit atory pathways ascend from the subcoeruleus area to the heat production effector networks. Subcoeruleus cell groups are innervatedfrom skin cold receptors (CR). Trunk skin warm receptors (WR) havebeen shown to project to 5‐HT NRM cells. Projections from the NRM ascend to the integrative hypothalamic networks controlling shiveringand descend to the dorsal horn. Parallel pathways take conventionalroutes ascending from the WR via the dorsal horn to the nucleusreticularis gigantocellularis (NRG), to the nucleus raphe dorsalis and the adjacent central gray matter (PAG), and to the thalamus and sensory cortex. For further explanation see text. Symbols:—, inhibitory connections; ——⊲, excitatory connections.

References
 1. Abrams, R., D. Caton, L. Curet, C. Crenshaw, L. Mann, and D. H. Barron. Fetal brain‐maternal aorta temperature differences in sheep. Am. J. Physiol. 217: 1613–1622, 1969.
 2. Alexander, G., Body temperature control in mammalian young. Br. Med. Bull. 31: 62–68, 1975.
 3. Baldino, F., and H. M. Geller. Electrophysiological analysis of neuronal thermosensitivity in rat preoptic and hypothalamic tissue cultures. J. Physiol. (Lond.) 327: 173–184, 1982.
 4. Baraban, J. M., and G. K. Aghajanian. Suppression of firing activity of 5‐ HT neurons in the dorsal raphé by alpha‐adrenoceptor antagonists. Neuropharmacology 19: 355–363, 1980.
 5. Bianca, W., Animal response to meteorological stress as a function of age. Int. J. Biometeorol. 14: 119–131, 1970.
 6. Blatteis, C. M., Shivering and nonshivering thermogenesis during hypoxia. In: Bioenergetics, Proceedings of the International Symposium on Environmental Physiology, edited by R. E. Smith Bethesda, MD: FASEB, 1972, p. 151–160.
 7. Bligh, J., A. Silver, M. J. Bacon, and C. A. Smith. The central role of a cholinergic synapse in thermoregulation in the sheep. J. Therm. Biol. 3: 147–151, 1978.
 8. Bliss, T. V. P., and A. R. V. Gardner‐Medwin. Long lasting potentiation of synaptic transmission in the dentate area of the unanesthetized rabbit following stimulation of the perforant path. J. Physiol. (Lond.) 232: 357–374, 1973.
 9. Brück, K., Temperature regulation in the newborn infant. Biol. Neonat. 3: 65–119, 1961.
 10. Brück, K., Nonshivering thermogenesis and brown adipose tissue in relation to age, and their integration in the thermoregulatory system. In: Brown Adipose Tissue, edited by O. Lindberg. New York: Elsevier, 1970, p. 117–154.
 11. Brück, K., Heat production and temperature regulation. In: Perinatal Physiology, edited by U. Stave. New York: Plenum, 1978, p. 455–498.
 12. Brück, K., Basic mechanisms in thermal long‐term and short‐term adaptation. J. Therm. Biol. 11: 73–77, 1986.
 13. Brück, K., E. Baum, and H. P. Schwennicke. Cold adaptive modifications in man induced by repeated short‐term cold‐exposures and during a 10‐day and night cold‐exposure. Pflugers Arch. 363: 125–133, 1976.
 14. Brück, K., and M. Brück. Der Energieumsatz hypothermer Frühgeborener. Klin. Wochenschr. 38: 1125–1130, 1960.
 15. Brück, K., and P. Hinckel. Thermoregulatory noradrenergic and serotonergic pathways to hypothalamic units. J. Physiol. (Lond.) 304: 193–202, 1980.
 16. Brück, K., and P. Hinckel. Thermoafferent systems and their adaptive modifications. Pharmacol. Ther. 17: 357–381, 1982.
 17. Brück, K., and P. Hinckel. Thermal afferent systems to the hypothalamus and thermal adaptation. J. Therm. Biol. 9: 7–10, 1984.
 18. Brück, K., A. H. Parmelee, and M. Brück. Neutral temperature range and range of “thermal comfort” in premature infants. Biol. Neonat. 4: 32–51, 1962.
 19. Brück, K., and H. P. Schwennicke. Interaction of superficial and hypothalamic thermosensitive structures in the control of non‐shivering thermogenesis. Int. J. Biometeorol. 15: 156–161, 1971.
 20. Brück, K., and B. Wünenberg. Uber die Modi der Thermogenese beim neugeborenen Warmblüter. Untersuchungen am Meerschweinchen. Pflugers Arch. 282: 362–375, 1965.
 21. Brück, K., and W. Wünnenberg. Meshed control of two effector systems: nonshivering and shivering thermogenesis. In: Physiological and Behavioral Temperature Regulation, edited by J. D. Hardy. Springfield, IL: Thomas, 1970, p. 562–580.
 22. Brück, K., W. Wünnenberg, and E. Zeisberger. Comparison of cold‐adaptive metabolic modifications in different species with special reference to the miniature pig. Federation Proc. 28: 1035–1040, 1969.
 23. Brück, K., and E. Zeisberger. Adaptive changes in thermoregulation and their neurophysiological basis. Pharmacol. Ther. 35: 163–215, 1987.
 24. Buetow, K. C., and S. W. Klein. Effect of maintenance of “normal” skin temperature on survival of infants of low body weights. Pediatrics 34: 163–170, 1964.
 25. Cross, K. W., G. S. Dawes, and J. C. Mott. Anoxia, oxygen consumption and cardial output in newborn lambs and adult sheep. J. Physiol. (Lond.) 146: 316–343, 1959.
 26. Dawes, G. S., H. N. Jacobson, C. Mott, and H. J. Shelley. Some observations on fetal and newborn rhesus monkeys. J. Physiol. (Lond.) 152: 271–298, 1960.
 27. Dawkins, M. J. R., and D. Hull. Brown adipose tissue and the response of newborn rabbit to cold. J. Physiol. (Lond.) 172: 216–238, 1964.
 28. Dawson, N. J., A. A. Young, and D. G. C. Ormrod. Is there a critical period during which environment modifies the developing thermoregulatory system?. In: Thermal Physiology, edited by J. R. S. Hales. New York: Raven, 1984, p. 109–112.
 29. Day, R. L., L. Caliguiri, and M. Kelley. Body temperature and survival of premature infants. Pediatrics 34: 171–181, 1964.
 30. Doi, K., and A. Kuroshima. Lasting effect of infantile cold experience on cold tolerance in adult rats. Jpn. J. Physiol. 28: 139–150, 1979.
 31. Eccles, J. C., The Understanding of the Brain. New York: McGraw‐Hill, 1977.
 32. Elsasser, W. M., The Physical Foundation of Biology. Oxford: Pergamon, 1958.
 33. Ferguson, A. V., W. L. Veale, and K. E. Cooper. Evidence of environmental influence on the development of thermoregulation in the rat. Can. J. Physiol. Pharmacol. 59: 91–95, 1980.
 34. Gelineo, S., Development ontogénétique de la thermoregulation chez le chien. Bull. Acad. Serbe Sci. 18: 97–102, 1957.
 35. Gunn, R. R., K. T. Ball, and P. D. Gluckman. Withdrawal of placental prostaglandins permits thermogenic responses in fetal sheep brown adipose tissue. J. Appl. Physiol.: Respir. Environ. Exerc. Physiol. 74: 998–1004, 1993.
 36. Hammel, H. T., H. C. Heller, and F. R. Sharp. Probing the rostral brain stem of anaesthetized, unanesthetized, and exercising dogs and of hibernating and euthermic ground squirrels. Federation Proc. 32: 1588–1597, 1973.
 37. Hardy, J. D., Physiology of temperature regulation. Physiol. Rev. 41: 521–606, 1961.
 38. Hardy, J. D., Posterior hypothalamus and the regulation of body temperature. Federation Proc. 32: 1564–1571, 1973.
 39. Hellon, R. F., Central transmitters and thermoregulation. In: Essays on Temperature Regulation, edited by J. Bligh and R. Moore. Amsterdam: North Holland, 1972, p. 71–85.
 40. Hemingway, A., and G. G. Nahas. Effect of hypoxia on the metabolic response to cold. J. Appl. Physiol. 5: 267–272, 1952.
 41. Hensel, H., Thermoreception and Temperature Regulation. New York: Academic, 1981.
 42. Hensel, H., Thermal Sensations and Thermoreceptors in Man. Springfield, IL: Thomas, 1982.
 43. Hensel, H., K. H. Andres, and M. V. During. Structure and function of cold receptors. Pflugers Arch. 352: 1–10, 1974.
 44. Hensel, H., K. Brück, and P. Raths. Homeothermic organisms. In: Temperature and Life, edited by H. Precht, J. Christophersojn, H. Hensel, and W. Larcher. Berlin: Springer, 1973, p. 503–761.
 45. Hessemer, V., A. Feh, and K. Brück. Effects of passive heat adaptation and moderate sweatless conditioning on responses to cold and heat. Eur. J. Appl. Physiol. 55: 281–289, 1986.
 46. Hey, E. N., and G. Katz. Evaporative water loss in the new‐born baby. J. Physiol. (Lond.) 200: 605–619, 1969.
 47. Hey, E. N., G. Katz, and B. O'Connell. The total thermal insulation of the newborn baby. J. Physiol. (Lond.) 207: 683–698, 1970.
 48. Hill, J. R., The oxygen consumption of newborn and adult mammals: its dependence on the oxygen tension in the inspired air and on the environmental temperature. J. Physiol. (Lond.) 149: 346–373, 1959.
 49. Hinckel, P., and W. T. Perschel. Influence of cold and warm acclimation on neuronal responses in the lower brain stem. Can. J. Physiol. Pharmacol. 65: 1281–1289, 1987.
 50. Hinckel, P., and K. Schröder‐Rosenstock. Central thermal adaptation of lower brain stem units in the guinea pig. Pflugers Arch. 395: 344–346, 1982.
 51. Hinckel, P., and K. Schröder‐Rosenstock. Central short‐term cold adaptation in the guinea pig. Pflugers Arch. 398: 259–261, 1983.
 52. Hissa, R., Postnatal development of thermoregulation in the Norwegian lemming and the golden hamster. Ann. Zool. 5: 345–383, 1968.
 53. Hubel, D. H., and T. N. Wiesel. The period of susceptibility to the physiological effects of unilateral eye closure in kittens. J. Physiol. (Lond.) 206: 419–436, 1970.
 54. Hull, D., Oxygen consumption and body temperature of newborn rabbits and kittens exposed to cold. J. Physiol. (Lond.) 177: 192–202, 1965.
 55. Hull, D., The preferred environmental temperature of newborn rabbits. Biol. Neonat. 50: 323–330, 1986.
 56. Jensen, A., Repetitive reduction of uterine blood flow and its influence on fetal transcutaneous PO2 and cardiovascular variables. J. Dev. Physiol. 7: 75–78, 1985.
 57. Jessen, C., and E. Simon. Spinal cord and hypothalamus as core sensors of temperature in the conscious dog. III. Identity of functions. Pflugers Arch. 324: 217–226, 1971.
 58. Laburn, H. P., D. Mitchell, and K. Goelst. Fetal and maternal body temperatures measured by radiotelemetry in near‐term sheep during thermal stress. J. Appl. Physiol.: Respir. Environ. Exerc. Physiol. 72: 894–900, 1992.
 59. Misgeld, U., M. R. Klee, J. M. Sarvey, and M. L. Zeise. Role of inhibition in heterosynaptic postactivation potentiation of CA 3 neurons in vitro. Adv. Physiol. Sci. 36: 155–164, 1981.
 60. Moore, R. E., Oxygen consumption and body temperature in newborn kittens subjected to hypoxia and reoxygenation. J. Physiol. (Lond.) 149: 500–518, 1959.
 61. Mount, L. E., The Climatic Physiology of the Pig. London: Arnold, 1968.
 62. Padbury, J. F., D. H. Polk, J. P. Newnham, and R. W. Lam. Neonatal adaptation: greater sympathoadrenal response in preterm than full‐term fetal sheep at birth. Am. J. Physiol. 248 (Endocrinol. Metab. 11): E443–E449, 1985.
 63. Power, G. G., J. R. Gunn, B. M. Johnston, and P. D. Gluckman. Oxygen supply and the placenta limit thermogenic responses in fetal sheep. J. Appl. Physiol.: Respir. Environ. Exerc. Physiol. 63: 1896–1901, 1987.
 64. Raynaud, J., J. P. Martineaud, O. P. Bhatnagar, H. Viellefond, and J. Durand. Body temperature during rest and exercise in residents and sojourners in hot climate. Int. J. Biometeorol. 20: 309–317, 1976.
 65. Schingnitz, G., Discharge pattern of central thermoresponsive neurons after local blockade of the stimulated skin area. Pflugers Arch. 384: R25, 1980.
 66. Smith, R. E., and B. A. Horwitz. Brown fat and thermogenesis. Physiol. Rev. 49: 330–425, 1969.
 67. Sulyok, E., E. Jéquier, and L. S. Prod'hom. Thermal balance of the newborn infant in a heat‐gaining environment. Pediatr. Res. 7: 888–900, 1973.
 68. Sundin, U., Brown fat thermoregulation in developing hamsters (Mesocricetus auratus). A GDP‐binding study. Biol. Neonat. 39: 141–149, 1981.
 69. Sundin, U., and B. Cannon. GDP‐binding to the brown fat mitochondria of developing and cold‐adapted rats. Comp. Biochem. Physiol. 65B: 463–471, 1980.
 70. Taylor, P. M., Oxygen consumption in newborn rats. J. Physiol. (Lond.) 154: 153–168, 1960.
 71. Varnai, I., M. Farkas, and S. Donhoffer. Thermoregulatory heat production and the regulation of body temperature in the newborn rabbit. Acta Physiol. Hung. 38: 299–315, 1970.
 72. Wetzler, K., and E. Frank. Chemische Wärmeregulation gegen Kälte und Hitze im Sauerstoffmangel. Pflugers Arch. 250: 439–464, 1948.
 73. Wünnenberg, W., and K. Brück. Studies on the ascending pathways from the thermosensitive region of the spinal cord. Pflugers Arch. 321: 233–241, 1970.
 74. Wünnenberg, W., and J. D. Hardy. Response of single units of the posterior hypothalamus to thermal stimulation. J. Appl. Physiol. 33: 547–552, 1972.
 75. Wünnenberg, W., CNS regulation of body temperature in hibernators and nonhibernators. In: Living in the Cold, edited by K. C. Heller. New York: Elsevier, 1986, p. 185–192.

Contact Editor

Submit a note to the editor about this article by filling in the form below.

* Required Field

How to Cite

K. Brück, P. Hinckel. Ontogenetic and Adaptive Adjustments in the Thermoregulatory System. Compr Physiol 2011, Supplement 14: Handbook of Physiology, Environmental Physiology: 597-611. First published in print 1996. doi: 10.1002/cphy.cp040127