Skip to main content
SpringerLink
Log in

Is Hibernation Facilitated by an Inhibition of Arousal?

  • Conference paper
Life in the Cold

Abstract

Seasonal hibernation is a poorly understood phenomenon and the details of how hibernation induction, maintenance and arousal are controlled are, for the most part, enigmatic. Hibernating golden-mantled ground squirrels, Spermophilus lateralis, were treated with MK801, a non-competitive antagonist of the NMDA-type glutamate receptor, as part of a larger investigation of the role of these receptors in the control of breathing in this species. Drug treatment prompted arousal from hibernation at a dose of 5.0 mg/kg, but not at a dose of 0.5 mg/kg. We have previously demonstrated that similar treatment prevents sleep and sleep-like states of cortical arousal in unanesthetized and anesthetized squirrels. As removal of NMDAtype glutamatergic activation resulted in arousal, the data suggest that arousal is normally actively inhibited; glutamatergic inhibition facilitates stable hibernation and NMDA-type glutamatergic blockade results in a disinhibition of arousal mechanisms, resulting in arousal from hibernation. The similarity between the present results and those pertaining to sleep in non-hibernating squirrels supports the theoretical homology between hibernation and sleep. This research was supported by the Natural Sciences and Engineering Research Council of Canada, and results have been submitted for peer-reviewed publication in primary literature.

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

Access this chapter

Log in via an institution
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

  • Azuma S, Kodama T, Honda K, and Inoue S (1996) State-dependent changes of extracellular glutamate in the medial preoptic area in freely behaving rats. Neurosci Lett 214(2–3):179–82

    Article  PubMed  CAS  Google Scholar 

  • Beckman AL, and Satinoff E (1972) Arousal from hibernation by intrahypothalamic injection of biogenic amines in ground squirrels. Am J Physiol 222:875–879

    PubMed  CAS  Google Scholar 

  • Beckman AL and Stanton TL (1976) Changes in CNS responsiveness during hibernation. American Journal of Physiology 231:810–816

    PubMed  CAS  Google Scholar 

  • Beckman AL, Stanton TL and Satinoff E (1976a) Characterization of midbrain components of the trigger for arousal from hibernation. Am J Physiol 230:368–375

    PubMed  CAS  Google Scholar 

  • Beckman AL, Stanton TL and Satinoff E (1976b) Inhibition of the CNS trigger process for arousal from hibernation. Am J Physiol 230:1018–1025

    PubMed  CAS  Google Scholar 

  • Berger RJ (1984) Slow wave sleep, shallow torpor and hibernation: homologous states of diminished metabolism and body temperature. Biol Psych 19:305–326

    Article  CAS  Google Scholar 

  • Bliss TVP and Collingridge GL (1993) A synaptic model of memory: long term potentiation in the hippocampus. Nature 361:31–9

    Article  PubMed  CAS  Google Scholar 

  • Burlet S, Leger L and Cespuglio R (1999) Nitric oxide and sleep in the rat: a puzzling relationship. Neurosci 92(2):627–639

    Article  CAS  Google Scholar 

  • Collingridge G and Singer W (1991) Excitatory amino acid receptors and synaptic plasticity. In: The Pharmacology of Excitatory Amino Acids. Trends in Pharmacological Science Special Report. Elsevier, Cambridge, UK, pp. 42–48

    Google Scholar 

  • Cespuglio R, Burlet S and Faradji-Prevautel H (1999) 5-Hydroxyindoles compounds and nitric oxide voltammetric detection in the rat brain: changes occurring throughout the sleep-wake cycle. J Neural Trans 105(2–3):205–15

    Article  Google Scholar 

  • Dark J, Kilduff TS, Heller HC, Licht P and Zucker I (1990) Suprachiasmatic nuclei influence hibernation rhythms of golden-mantled ground squirrels. Brain Res 509:111–118.

    Article  PubMed  CAS  Google Scholar 

  • Dzoljic MR, de Vries R and van Leeuwen R (1996) Sleep and nitroc oxide: effects of 7-nitro indazole, inhibitor of brain nitric oxide synthase. Brain Res 718:145–150

    Article  PubMed  CAS  Google Scholar 

  • Garthwaite J and Boulto CL (1995) Nitric oxide signaling in the central nervous system. Ann Rev Physiol 57:683–706

    Article  CAS  Google Scholar 

  • Geiser F and Kenagy GJ (1988) Torpor duration in relation to temperature and metabolism in hibernating ground squirrels. Physiol Zoo:161442–449

    Google Scholar 

  • Harald HH, Schmidt W and Ulrich W (1994) NO at work. Cell 78:919–925.

    Google Scholar 

  • Harris MB and Milsom WK (1994) The ventilatory response to hypercapnia in hibernating golden-mantled ground squirrels, Spermophilus lateralis. Physiol Zool 67:739–755

    Google Scholar 

  • Heller HC (1979) Hibernation: neural aspects. Ann Rev Physiol 41:305–21

    Article  CAS  Google Scholar 

  • Heller HC and Glotzbach SF (1977) Thermoregulation during sleep and hibernation. In: Robetshaw D (ed.) International review of physiology, environmental physiology II, vol. 15, University Park Press, Baltimore, pp 147–88

    Google Scholar 

  • Heller HC, Glotzbach SF, Grahn D and Radeke C (1988) Sleep-dependent changes in the thermoregulatory system. In: Clinical Physiology of Sleep. American Physiological Society, Bethesda, pp. 145–158

    Google Scholar 

  • Huettner JE, and Bean BP (1988) Block of N-methyl-D-aspartate-activated current by the anticonvulsant MK-801: selective binding to open channels. Proc Nat Acad Sci USA 85: 1307–1311

    Article  PubMed  CAS  Google Scholar 

  • Kajimura N, Uchiyama M, Takayama Y, Uchida S, Uema T, Kato M, Sekimoto M,. Watanabe T, Nakajima T, Horikoshi S, Ogawa K, Nishikawa M, Hiroki M, Kudo Y, Matsuda H, Okawa M and Takahashi K (1999) Activity of midbrain reticular formation and neocortex during the progression of human non-rapid eye movement sleep. J neurosci 19(22):10065–10073

    PubMed  CAS  Google Scholar 

  • Kapas L, Fang J and Krueger JM (1994) Inhibition of nitric oxide synthesis inhibits rat sleep. Brain Res 664:189–196

    Article  PubMed  CAS  Google Scholar 

  • Kekesi KA, Dobolyi A, Salfay O, Nyitrai G and Juhasz G (1997) Slow wave sleep is accompanied by release of certain amino acids in the thalamus of cats. Neuroreport 8(5):1183–6

    Article  PubMed  CAS  Google Scholar 

  • Kilduff, TS, Krilowicz B, Milsom WK, Trachel L and Wang LCH (1993) Sleep and mammalian hibernation: Homologous adaptations and homologous processes ? Sleep 16(4):372–386

    PubMed  CAS  Google Scholar 

  • Kilduff TS, Miller JD, Radeke CM, Sharp FR and Heller HC (1990) [kC-]2-deoxyglucose uptake in ground squirrel brain during entrance to and arousal from hibernation. J Neurosci 10: 2463–2475

    PubMed  CAS  Google Scholar 

  • Kilduff TS, Sharp FR and Heller CH(1982) [1C-]2-deoxyglucose uptake in ground squirrel brain during hibernation. J Neurosci 2: 143–157

    PubMed  CAS  Google Scholar 

  • Leonard TO and Lydic R (1997) Pontine nitric oxide modulates acetylcholine release, rapid eve movement sleep generation. and respiratory rate. J Neurosci 17(2):774–785

    PubMed  CAS  Google Scholar 

  • Lyman CP (1982) Sensitivity to arousal, and Recent theories of hibernation. In: Lyman CP, Willis JS, Malan A and Wang LCS (eds.) Hibernation and Torpor in Mammals and Birds. Academic Press, New York. 77–91, 283–301

    Chapter  Google Scholar 

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

    CAS  Google Scholar 

  • Maquet P, Degueldre C, Delfiore G, Aerts J, Peters J, Luxen A and Franck G (1997). Functional neuroanatomy of human slow wave sleep. J Neurosci 17(8):2807–2812

    PubMed  CAS  Google Scholar 

  • Mayer ML and Miller RJ (1991) Excitatory amino acid receptors, second messengers and regulation of intracellular Ca2+ in mammalian neurons. In: The Pharmacology of Excitatory Amino Acids. Trends in Pharmacological Science Special Report, Elsevier, Cambridge, UK, pp. 36–42

    Google Scholar 

  • Monaghan DT and Cotman CW (1985) Distribution of N-methyl-ID-aspartate-sensitive L[3H]glutamate-binding sites in rat brain. J Neurosci 5:2902–2919

    Google Scholar 

  • Monti JM, Hantos H, Ponzoni A, Monti D and Banchero P (1999) Role of nitric oxide in sleep regulation: effects of L-NAME, an inhibitor of nitric oxide synthase, on sleep in rats. Behav Brain Res 100(1–2):197–205

    Article  PubMed  CAS  Google Scholar 

  • Moruzzi G and Magoun HW (1949) Brainstem reticular formation and activation of the EEG. Electroenceph clin neurophysiol 1:455–473

    PubMed  CAS  Google Scholar 

  • O’Hara BF, Andretic R, Heller HC, Carter DB and Kilduff TS (1995) GABAA, GABAB, and NMDA receptor subunit expression in the suprachiasmatic nucleus and other brain regions. Mol Brain Res 28:239–250

    Article  PubMed  Google Scholar 

  • O’Hara BF, Watson FL, Srere HK, Kumar H, Wiler SW, Welch SK, Bitting L, Heller HC and Kilduff TS (1999) Gene expression in the brain across the hibernating cycle. J Neurosci 19(10):3781–3790

    PubMed  Google Scholar 

  • Pengelley ET and Fisher KC (1961) Rhythmical arousal from hibernation in the golden-mantled ground squirrel, Citellus lateralis tescorum. Can J Zool 39:105–120

    Article  Google Scholar 

  • Petralia RS, Yokotani N and Wenthold RJ (1994a) Light and electron microscope distribution of the NMDA receptor subunit NMDAR1 in the rat nervous system using selective antipeptide antibody. J Neurosci 14(2):667–696

    PubMed  CAS  Google Scholar 

  • Petralia RS, Wang YX and Wenthold RJ (1994b) The NMDA receptor subunits NR2A and NR2B show histological and ultrastructural localization patterns similar to those of NR1. J Neurosci 14(10):6102–6120

    PubMed  CAS  Google Scholar 

  • Steriade M and McCarley R(1990) Brainstem control of wakefulness and sleep. Plenum, New York.

    Book  Google Scholar 

  • Strumwasser F (1959) Factors in the pattern, timing and pred ict a b il i ty of h ibernation in the squirrel Citellus beecheyi Am J Physiol 196:8–14

    PubMed  CAS  Google Scholar 

  • Twente JW and Twente J(1968a) Progressive irritability of hibernating Citellus lateralis Comp Biochem Physiol 25: 475–483

    Article  PubMed  CAS  Google Scholar 

  • Twente JW and Twente J (1968b) Seasonal variation in the hibernating behavior of Citellus lateralis. In: Fischer KC, Dawe AW, Lyman CP, Schonbaum E and South FE (eds) Proceedings of the 3rd International Symposium on Natural Mammalian Hibernation,. Vol. III. Oliver & Boyd, Edinburgh, pp 47–63

    Google Scholar 

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

    Chapter  Google Scholar 

  • Williams JA, Vincent SR and Reiner PB (1997)Nitric oxide production in rat thalamus changes with behavioral state, local depolarization, and brainstem stimulation. J Neurosci 17(1):420–427

    PubMed  CAS  Google Scholar 

  • Willis JS(1982) The mystery of periodic arousal. In: Lyman CP, Willis JS, Malan A and Wang LCH (eds.) Hibernation and Torpor in Mammals and Birds. Academic Press, New York, pp. 92–103

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Zoology, University of British Columbia, 6270 University Blvd., Vancouver, BC, V6T 1Z4, Canada

    Michael B. Harris & William K. Milsom

Authors
  1. Michael B. Harris
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. William K. Milsom
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. Department of Biology, Philipps University, 35032, Marburg, Germany

    Gerhard Heldmaier  & Martin Klingenspor  & 

Rights and permissions

Reprints and permissions

Copyright information

© 2000 Springer-Verlag Berlin Heidelberg

About this paper

Cite this paper

Harris, M.B., Milsom, W.K. (2000). Is Hibernation Facilitated by an Inhibition of Arousal?. In: Heldmaier, G., Klingenspor, M. (eds) Life in the Cold. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-662-04162-8_26

Download citation

  • DOI: https://doi.org/10.1007/978-3-662-04162-8_26

  • 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

Search

Navigation