Skip to main content

Control of Cardiac and Ventilation Frequencies During Hibernation in Ground Squirrels

  • Conference paper
Life in the Cold

Abstract

Entrance into hibernation is accompanied by a massive increase in parasympathetic tone which dramatically decreases heart rate. These changes parallel the fall in metabolism rather than the subsequent fall in body temperature. As body temperature does fall, parasymapathetic and sympathetic tones are slowly withdrawn and heart rate appears to become determined directly by complex interactions between metabolism, temperature and “state.” The dramatic increase in heart rate during arousal is due to a massive increase in sympathetic tone which also parallels the rise in metabolism and this tone is progressively withdrawn as body temperature subsequently rises. Ventilation rate, too, decreases during entrance and parallels the changes in metabolism. As body temperature falls, breathing frequency slows, depending on species, either by a prolongation of the pause between breaths giving rise to a pattern of slow evenly spaced breaths, or by a waxing and waning of breathing frequency giving rise to an episodic breathing pattern. In the latter case, the waxing and waning, and resulting episodic pattern, appear to be due to alternating descending positive and negative influences acting on the medullary breathing centres. In deep hibernation, “state” itself appears to have a direct role in regulating these episodes in addition to an indirect influence, related to the low body temperatures associated with hibernation. During arousal, a massive excitation of breathing frequency occurs which, again, is correlated to metabolism rather than temperature. The field has made substantial progress in describing the non-stochastic changes in heart rate and breathing pattern in hibernating animals, and the mechanisms underlying their immediate control. The central neural mechanisms underlying the interactions between metabolism, body temperature and “state”, and the manner in which these affect autonomic control processes, however, remain enigmatic.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Bianchi AL, Denavit-Saubie M, Champagnat J. (1995) Central control of breathing in mammals: neruonal circuitry, membrane properties, and neurotransmitters. Physiol. Rev. 75(1):1–46.

    PubMed  CAS  Google Scholar 

  • Biewald GA., Raths P (1959) Die chronotrope Vaguswirkung auf das Hamsterherz unter dem Einfluss von Winterschlaf und Hypothermie. Pflügers Arch. 268:530–544.

    Article  PubMed  CAS  Google Scholar 

  • Britton SW (1928) Effect of partial sympathectomy and vagotomy upon the course of hibernation in heterothermous animals. C. r. Acad. Sci. U.S.S.R. 73:1305–1308.

    Google Scholar 

  • Burlington RF, Milsom WK (1989) The cardiovascular system in hibernating mammals: recent advances. In: Malan A, Canguilhem B (eds) Living in the cold II. Paris: Colloque INSERM/John Libbey Eurotext Ltd. pp 235–242.

    Google Scholar 

  • Chatfield PO, Lyman CP (1950) Circulatory changes during process of arousal in the hibernating hamster. Am. J. Physiol. 163:566–574.

    PubMed  CAS  Google Scholar 

  • Eagles DA, Jacques LB, Taboada J, Wagner CW, Diakun TA (1988) Cardiac arrhythmias during arousal from hibernation in three species of rodents. Am.J.Physiol. 254:R102-R108.

    PubMed  CAS  Google Scholar 

  • Eliassen E (1960) Cardiovascular pressures in the hibernating hedgehog, with special regard to the pressure changes during arousal. Arbok Univ. Bergen, Mat-Naturvitensk. Ser. No.6:1–27.

    Google Scholar 

  • Harris MB, Milsom WK (1995) Parasympathetic influence on heart rate in euthermic and hibernating ground squirrels. J.Exp.Biol. 198:931–937.

    PubMed  CAS  Google Scholar 

  • Harris MB (1998) The control of breathing in the golden-mantled ground squirrel (Spermophilus lateralis). PhD Thesis, University of British Columbia.

    Google Scholar 

  • Johansen K (1961) Distribution of blood in the arousing hibernator. Acta Physiol. Scand. 2:379–386.

    Article  Google Scholar 

  • Johansen K, Krog J, Reite O (1964) Autonomic nervous influence on the heart of hypothermic hibernator. Ann. Acad. Sci. Fenn. Ser.A. 71:245–254.

    Google Scholar 

  • Johansson BW (1967) Heart and circulation in hibernators. In: Fisher KC, Dawe AR, Lyman CP, Schönbaum E, South FE (eds) Mammalian Hibernation III. Elsevier, New York, pp 200–218.

    Google Scholar 

  • Jones SB, Romano FD (1984) Functional characteristics and responses to adrenergic stimulation of isolated heart preparations from hypothermic and hibernating subjects. Cryobiol. 21:615–626.

    Article  CAS  Google Scholar 

  • Kirkebö A (1968) Cardiovascular investigations on hedgehogs during arousal from the hibernating state. Acta Physiol. Scand. 73:394–406.

    PubMed  Google Scholar 

  • Ling L, Karius DR, Speck DF (1994) Role of N-methyl-D-aspartate receptors in the pontine pneumotaxic mechanism in the cat. J. Appl. Physiol. 76(3):1138–1143.

    PubMed  CAS  Google Scholar 

  • Lyman CP (1958) Oxygen consumption, body temperature and heart rate of woodchucks entering hibernation. Am.J.Physiol. 194(1):83–91.

    PubMed  CAS  Google Scholar 

  • Lyman CP (1965) Circulation in mammalian hibernation. In: Dow P, Hamilton WF (eds) Handbook of Physiology Sect. 2: Circ. 3. Am. Physiol. Soc. Washington, DC, pp 1967–1989.

    Google Scholar 

  • Lyman CP (1982) The hibernating state. In: Lyman CP, Willis JS, Malan A, Wang LCH (eds) Hibernation and torpor in mammals and birds. Academic Press, New York, pp12–53.

    Chapter  Google Scholar 

  • Lyman CP, O’Brien RC (1960) Circulatory changes in the thirteen-lined ground squirrel during the hibernating cycle. Bull. Mus. Comp. Zool. 124: 353–372.

    Google Scholar 

  • Lyman CP, O’Brien RC (1963) Autonomic control of circulation during the hibernating cycle in ground squirrels. J. Physiol. (London) 168: 477–499.

    CAS  Google Scholar 

  • Malan A (1982) Respiration and acid base state in hibernation. In: Lyman CP, Willis JS, Malan A, Wang LCH (eds) Hibernation and torpor in mammals and birds. Academic Press, New York, pp 12–53.

    Google Scholar 

  • McArthur MD, Milsom WK (1991) Changes in ventilation and respiratory sensitivity associated with hibernation in columbian (Spermophilus columbianus) and golden-mantled (Spermophilus lateralis) ground squirrels. Physiol. Zool. 64(4):940–959.

    Google Scholar 

  • Milsorn WK, Burlington RF, Burleson ML (1993) Vagal influence on heart rate in hibernating ground squirrels. J.Exp.Biol. 185:25–32.

    Google Scholar 

  • Milsom WK, Osborne S, Chan PF, Hunter JD, MacLeod JZ (1993) Sleep, hypothermia, and hibernation: Metabolic rate and the control of breathing pattern in goden-mantled ground squirrels. In: Carey C, Florant GL (eds) Life in the cold: ecological, physiological, and molecular mechanisms. Westview Press, Boulder, pp233–240.

    Google Scholar 

  • Milsom WK, Harris MB, Reid SG (1997) Do descending influences alternate to produce episodic breathing? Resp. Phys. 110:307–317.

    Article  CAS  Google Scholar 

  • Osborne S, Milsom WK (1993) Ventilation is coupled to metabolic demands during progressive hypothermia in rodents. Resp Phys. 92:305–318.

    Article  CAS  Google Scholar 

  • Popovic V (1964) Cardiac output in hibernating ground squirrels. Am.J.Physiol. 207(6):1345–1348.

    PubMed  CAS  Google Scholar 

  • St. John WM (1977) Integration of peripheral and central chemoreceptor stimuli by pontine and meduallary respiratory centers. Ged. Proc 36(10): 2421–2427.

    Google Scholar 

  • St. John WM, Zhou D. (1991) Rostral pontile mechanisms regulate durations of expiratory phases. J. Appl. Physiol. 71(6): 2133–2137.

    Google Scholar 

  • Senturia JB, Campbell TA, Caprette DR (1986) Cardiovascular changes in hibernation and hypothermia. In: Heller H.C, Masacchia XJ, Wang LCH (eds) Living in the cold: physiological and biochemical adaptations. Elsevier, New York, pp 557–564.

    Google Scholar 

  • Strumwasser F (1959) Thermoregulatory, brain and behavioral mechanisms during entrance into hibernation in the squirrel, Citellus beecheyi. Am.J.Physiol. 196:15–22.

    PubMed  CAS  Google Scholar 

  • Strumwasser F (1960) Some physiological principles governing hibernation in Citellus beecheyi. Bull. Mus. Comp. Zool. 124: 285–320.

    Google Scholar 

  • Twente JW, Twente JA (1978) Autonomic regulation of hibernation by Citellus and Eptesicus. In: Wang LCH, Hudson JW (eds) Strategies in the cold: Natural Torpor and Thermogenesis. Academic Press, New York, pp 327–373.

    Chapter  Google Scholar 

  • Wang LCH, Hudson JW (1971) Temperature regulation in normothermic and hibernating eastern chipmunk, Tamias striatus. Comp. Biochem. Physiol. A 38A: 59–90.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2000 Springer-Verlag Berlin Heidelberg

About this paper

Cite this paper

Zimmer, M.B., Harris, M.B., Milsom, W.K. (2000). Control of Cardiac and Ventilation Frequencies During Hibernation in Ground Squirrels. In: Heldmaier, G., Klingenspor, M. (eds) Life in the Cold. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-662-04162-8_17

Download citation

  • DOI: https://doi.org/10.1007/978-3-662-04162-8_17

  • Publisher Name: Springer, Berlin, Heidelberg

  • Print ISBN: 978-3-642-08682-3

  • Online ISBN: 978-3-662-04162-8

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics