Comprehensive Physiology Wiley Online Library

Hibernation in Mammals: Central Nervous System Function

Full Article on Wiley Online Library


The sections in this article are:

1 The Hibernation Cycle and Maintenance of Homeostatic Mechanisms
2 Sensory and Higher‐Order Processing During Hibernation
3 The Orderly Sequence of Events During Arousal from and Entrance Into Hibernation
4 Neuroactive Agents and Hibernation
5 Unanswered Questions
 1. Azmitia, E. C., and M. Segal. An autoradiographic analysis of the differential ascending projections of the dorsal and median raphe nuclei in the rat. J. Comp. Neurol. 179: 641–668, 1978.
 2. Beckman, A. L., and C. Llados‐Eckman. Antagonism of brain opioid peptide action reduces hibernation bout duration. Brain Res. 328: 201–205, 1985.
 3. Beckman, A. L., and E. Satinoff. Arousal from hibernation by intrahypothalamic injections of biogenic amines in ground squirrels. Am. J. Physiol. 222: 875–879, 1972.
 4. Beckman, A. L., E. Satinoff, and T. L. Stanton. Characterization of midbrain component of the trigger for arousal from hibernation. Am. J. Physiol. 230: 368–375, 1976.
 5. Beckman, A. L., and T. L. Stanton. Properties of the CNS during the state of hibernation. In: The Neural Basis of Behavior, edited by A. L. Beckman. New York: Spectrum, 1982, p. 19–45.
 6. Belousov, A. B., and J. V. Belousova. State‐dependent and state‐independent effects of thyrotropin‐releasing hormone on medial septum neural activity in the brain slices of waking and hibernating ground squirrels. Neuroscience 50: 857–866, 1992.
 7. Belousov, A. B., and O. S. Vinogradova. Modeling the regulation of theta‐rhythm by increasing afferent inflow in septal slices. Neurosci. and Behav. Biol. 20: 437–445, 1990.
 8. Canguilhem, B., E. Kemph, G. Mack, and P. Schmitt. Regional studies of brain serotonin and norepinephrine in the hibernating, awakening or active European hamster, Cricetus cricetus, during winter. Comp. Biochem. Physiol. 57c: 175–179, 1977.
 9. Canguilhem, B., J. L. Miro, E. Kemph, and P. Schmitt. Does serotonin play a role in entrance into hibernation? Am. J. Physiol. 251 (Regulatory Integrative Comp. Physiol. 20): R755–R761, 1986.
 10. Carey, C., G. L. Florant, B. A. Wunder, and B. Horwitz, editors. Life in the Cold: Ecological, Physiological and Molecular Mechanisms. San Francisco: Westview Press, 1993.
 11. Chatfield, P. O., and C. P. Lyman. Subcortical electrical activity in the golden hamster during arousal from hibernation. Elec‐troencephalogr. Clin. Neurophysiol. 6: 403–408, 1954.
 12. Darrow, J. M., M. J. Duncan, A. Bartke, A. Bona‐Gallo, and B. D. Goldman. Influence of photoperiod and gonadal steroids on hibernation in the European hamster. J. Comp. Physiol. A. 163: 339–348, 1988.
 13. Duncan, R. J. S., and M. D. Tricklebank. On the stimulation of tryptophan in the brain of hamsters during hibernation. J. Neurochem. 31: 553–556, 1978.
 14. Goldman, S. S., and J. S. Willis. Cold resistance of the brain during hibernation II. Na‐K‐activated ATPase. Cryobiology 10: 218–224, 1973.
 15. Haak, L. L., E. Mignot, T. S. Kilduff, W. C. Dement, and H. C. Heller. Regional changes in central monoamine and metabolite levels during the hibernation cycle in the golden‐mantled ground squirrel. Brain Res. 563: 215–220, 1991.
 16. Hall, A. C., M. W. Wolowyk, L. C. H. Wang, and J. C. Ellory. The effects of temperature on Ca2+ transport in red cells from a hibernator (Spermophilus Richardsonii). J. Therm. Biol. 12: 61–63, 1987.
 17. Hamill, N. J., M. D. McGinn, and J. M. Horowitz. Auditory brainstem responses in ground squirrels arousing from hibernation. J. Comp. Physiol. B. 159: 167–172, 1989.
 18. Heller, H. C., Hibernation: neural aspects. Annu. Rev, Physiol. 41: 305–321, 1979.
 19. Heller, H. C., and G. W. Colliver. CNS regulation of body temperature during hibernation. Am. J. Physiol 227: 583–589, 1974.
 20. Heller, H. C., J. Walker, G. Florant, S. F. Glotzbach, and R. J. Berger. Sleep and hibernation: electrophysiological and thermoregulatory homologies. In: Strategies in Cold: Natural Torpidity and Thermogenesis, edited by L. Wang and J. Hudson. New York: Academic Press, 1978, p. 225–266.
 21. Hermes, M. L. H. J., R. M. Buijs, M. Masson‐Pevet, T. P. Van Der Woude, P. Pevet, R. Brenkle, and R. Kirsch. Central vasopressin infusion prevents hibernation in the European hamster (Cricetus cricetus). Proc. Natl. Acad. Sci. USA 86: 6408–6411, 1989.
 22. Horrigan, D. J., and J. M. Horowitz. Thermal dependence of serotonergic modulation of neural activity in the hamster. J. Comp. Physiol. A. 167: 79–88, 1990.
 23. Kilduff, T. S., S. S. Bowersox, K. F. Faull, L. Zeller‐DeAmicis, C. M. Radeke, R. D. Ciaranello, H. C. Heller, J. D. Barchas, and W. C. Dement. Modulation of the striatal dopaminergic system during the hibernation cycle. J. Neurosci. 7: 2732–2736, 1987.
 24. Kilduff, T. S., J. D. Miller, C. M. Radeke, F. R. Sharp, and H. C. Heller. 14C‐2‐Deoxyglucose uptake in the ground squirrel brain during entrance to and arousal from hibernation. J. Neurosci. 10: 2463–2475, 1990.
 25. Kilduff, T. S., B. F. O'Hara, E. L. Sutin, F. L. Watson, L. Bitting, and H. C. Heller. Immediate early gene expression in brain across the hibernation cycle. In: Life in the Cold: Ecological, Physiological, and Molecular Mechanisms, edited by C. Carey, G. L. Florant, B. A. Wunder, and B. Horwitz. Boulder: Westview Press, 1993, p. 305–313.
 26. Kilduff, T. S., F. R. Sharp, and H. C. Heller. Relative 2‐deoxy‐glucose uptake of the paratrigeminal nucleus increases during hibernation. Brain Res. 262: 117–123, 1986.
 27. Krelstein, M. S., M. P. Thomas, and J. M. Horowitz. Thermal effects on long‐term potentiation in the hamster hippocampus. Brain Res. 520: 115–122, 1990.
 28. Krilowicz, B. L., S. F. Glotzbach, and H. C. Heller. Neuronal activity during sleep and complete bouts of hibernation. Am. J. Physiol. 255 (Regulatory Integrative Comp. Physiol. 24): R1008–R1019, 1988.
 29. Kristoffersson, R., and A. Soivio. Hibernation in the hedgehog (Erinaceus europaeus L.): Changes in respiratory pattern, heart rate and body temperature in response to gradually decreasing or increasing ambient temperature. Ann. Acad. Sci. Fenn., Ser. Ar 82: 1–17, 1964.
 30. Kudryavtseva, N. N., and N. K. Popova. Serotonin concentration in various parts of the brain during hibernation and waking. Bull. Exp. Med. Biol. 75: 44–47, 1973.
 31. Lin, L., and E. B. Pivorun. Analysis of serotonin, dopamine, and their metabolities in the caudate putamen, the suprachiasmatic nucleus and the median raphe nucleus of euthermic and torpid deermice, Peromyscus maniculatus. Pharm. Biochem. Behav. 33: 309–314, 1989.
 32. Lyman, C. P., J. S. Willis, A. Malan, and L. C. H. Wang. Hibernation and Torpor in Mammals and Birds. New York: Academic Press, 1982, p. 1–317.
 33. Malan, A., Acid‐base regulation during hibernation. In: Acid‐base Regulation and Body Temperature, edited by H. Rahn and O. Prakash. Boston, MA: Nijhoff, 1985, p. 33–53.
 34. Malan, A., H. Arens, and A. Waechter. Pulmonary respiration and acid‐base state in hibernating marmots and hamsters. Respir. Physiol. 17: 45–61, 1973.
 35. Malan, A., J. L. Rodeau, and F. Daull. Intracellular pH in hibernating hamsters. Cryobiology 18: 100–101, 1981.
 36. Mihailovic, L. T., Cortical and subcortical electrical activity in hibernation and hypothermia. In: Hibernation and Hypothermia, Perspectives and Challenges, edited by F. E. South, J. P. Hannon, J. R. Willis, E. T. Pengelley, and N. R. Alpert. Amsterdam: New York, 1972, p. 487–533.
 37. Milsom, W. K., Intermittent breathing in vertebrates. Annu. Rev. Physiol. 53: 87–105, 1991.
 38. Miro, J. L., B. Canguilhem, and P. Schmitt. Serotonine cerebrale et sommeil hibernal. Brain Res. 170: 387–391, 1979.
 39. Moore, R. Y., and A. E. Halaris. Hippocampal innervation by serotonin neurons of the midbrain raphe in the rat. J. Comp. Neurol. 164: 171–184, 1975.
 40. Novotna, R., L. Jansky, and Z. Drahota. Effect of hibernation on serotonin metabolism in the brain stem of the golden hamster (Mesocricetus auratus). Gen. Pharmacol. 6: 23–26, 1975.
 41. South, F. E., V. M. Miller, and W. C. Hartner. Neuronal models of temperature regulation in euthermic and hibernating mammals: an alternate model for hibernation. In: Strategies in the Cold, edited by L. C. H. Wang and J. W. Hudson. New York, San Francisco, London: Academic Press, 1978, p. 187–224.
 42. Stanton, T. L., S. B. Caine, and A. Winokur. Seasonal and state‐dependent changes in brain TRH receptors in hibernating ground squirrels. Brain Res. Bull. 28: 877–886, 1992.
 43. Stanton, T. L., J. C. Daley III, and S. K. Salzman. Prolongation of hibernation bout duration by continuous intracerebroventricular infusion of melatonin in hibernating ground squirrels. Brain Res. 413: 350–355, 1987.
 44. Stanton, T. L., A. Winokur, and A. L. Beckman. Reversal of natural CNS depression by TRH action in the hippocampus. Brain Res. 181: 470–475, 1980.
 45. Strumwasser, F., Regulatory mechanisms, brain activity and behavior during deep hibernation in the squirrel, Citellus beecheyi. Am. J. Physiol. 196: 23–30, 1959.
 46. Uuspaa, V. J., The 5–hydroxytryptamine content of the brain and some other organs of the hedgehog (Erinaceus europaeus) during activity and hibernation. Experientia 19: 156–158, 1963.
 47. Walker, J. M., E. H. Haskell, R. J. Berger, and H. C. Heller. Hibernation at moderate temperatures: a continuation of slow wave sleep. Experientia 37: 726–728, 1981.
 48. Wang, L. C. H., Mammalian hibernation: an escape from the cold. In: Advances in Comparative and Environmental Physiology 2, edited by R. Gilles. Berlin: Springer‐Verlag, 1988, p. 1–45.
 49. Wünnenberg, W., Physiologie des Winterschlafes Hamburg and Berlin: Verlag Paul Parey, Germany, 1990, 1–98.
 50. Wünnenberg, W., G. Kuhnen, and R. Laschefski‐Sievers. CNS regulation of body temperature in hibernators and non‐hibernators. In: Living in the Cold, edited by H. C. Heller, X. J. Musacchia, L. C. H. Wang. Amsterdam: 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

John M. Horowitz, David J. Horrigan. Hibernation in Mammals: Central Nervous System Function. Compr Physiol 2011, Supplement 14: Handbook of Physiology, Environmental Physiology: 533-539. First published in print 1996. doi: 10.1002/cphy.cp040123