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Search for rhythmicity during hibernation in the European hamster

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Abstract

Temporal patterns of hibernation were studied by continuous monitoring of body temperature by radiotelemetry over 6 months in European hamsters, Cricetus cricetus, at constant temperature and photoperiod. Entrances into hibernation occurred mostly at the end of the night (0000–0800 hours), while arousals were randomly distributed between day and night. This is at variance with a control of bout duration by a clock with a period of 24 h. Consequently, the timing of entrances implies a phase-resetting of the circadian clock on each arousal. Persistence of circadian rhythmicity with a period different from 24 h during deep hibernation was investigated examining whether the durations of torpor bouts were integer multiples of a constant period. A non-parametric version of the classical contingency test of periodicity was developed for this purpose. Periods ranging from 21 to 29 h were tested. Nine animals out of ten showed at least one significant period in this range (P<0.01), either below 24 h (21.8±0.5 h, n=4) or above (27.3±0.5 h, n=7). However, we have found a theoretical model of bout durations for which the contingency test of periodicity sometimes gives false significant results. This indicates that the power of the test is weak. With this reservation our results suggest that a circadian oscillator controls the duration of a bout of hibernation, which would occur after an integer, but variable and possibly temperature-dependent number of cycles.

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Abbreviations

δb :

a contingency test (see Appendix)

SCN:

suprachiasmatic nuclei

τ:

period

T b :

body temperature

References

  • Batschelet E (1981) Circular statistics in biology. Academic Press, London

    Google Scholar 

  • Benson JA, Jacklet JW (1977) Circadian rhythm of output from neurons in the eye of Aplysia. I. Effects of deuterium oxide and temperature. J Exp Biol 70:151–166

    Google Scholar 

  • Canguilhem B (1977) Rythmes circannuels du poids et du sommeil hibernal chez le Hamster d'Europe. Rôle de la photopériode, de la température, de la thyroïde et des monoamines cérébrales. Thèse Doct. Sci. Université Louis Pasteur, Strasbourg

  • Conover WJ (1980) Practical nonparametric statistics. Wiley, New York

    Google Scholar 

  • Daan S (1973) Periodicity of heterothermy in the garden dormouse, Eliomys quercinus (L.). Neth J Zool 23:239–265

    Google Scholar 

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

    Google Scholar 

  • Florant G, Rivera DL, Lawrence AK, Tamarkin L (1984) Plasma melatonin concentrations in hibernating marmots: absence of plasma melatonin rhythm. Am J Physiol 247:R1062-R1066

    Google Scholar 

  • French AR (1977) Periodicity of recurrent hypothermia during hibernation in the pocket mouse, Perognathus longimembris. J Comp Physiol 115:87–100

    Google Scholar 

  • Fuller WA (1976) Introduction to statistical time series. John Wiley, New York

    Google Scholar 

  • Gibbs FP (1981) Temperature dependence of rat circadian pacemaker. Am J Physiol 241:R17-R20

    Google Scholar 

  • Gibbs FP (1983) Temperature dependence of the hamster circadian pacemaker. Am J Physiol 244:R607-R610

    Google Scholar 

  • Heller HC, Krilowicz BL, Kilduff TS (1989) Neural mechanisms controlling hibernation. In: Malan A, Canguilhem B (eds) Living in the cold — La vie au froid. INSERM/J Libbey Eurotext, Paris, pp 447–460

    Google Scholar 

  • Kayser C (1965) Le rythme nycthéméral de la dépense d'énergie chez les hibernants en sommeil hivernal. Arch Sci Physiol 19:369–413

    Google Scholar 

  • Kayser C, Heusner A, Stussi T (1964) Y a-t-il conservation du rythme nycthéméral de la dépense d'énergie pendant le sommeil hivernal? C R Soc Biol 158:1140–1144

    Google Scholar 

  • Kilduff TS, Miller JD, Radeke CM, Sharp FR, Heller HC (1990) 14C-2-Deoxyglucose uptake in the ground squirrel brain during entrance to and arousal from hibernation. J Neurosci 10:2463–2475

    Google Scholar 

  • Kristoffersson R, Soivio A (1964) Hibernation of the hedgehog (Erinaceus europaeus L.). The periodicity of hibernation of undisturbed animals during the winter in a constant ambient temperature. Ann Acad Sci Fenn, Ser A, IV 76:1–11

    Google Scholar 

  • Lee TM, Holmes WG, Zucker I (1990) Temperature dependence of circadian rhythms in golden-mantled ground squirrels. J Biol Rhythms 5:25–34

    Google Scholar 

  • Lellouch J, Lazar P (1985) Méthodes statistiques en expérimentation biologique. Flammarion Médecine-Sciences, Paris

    Google Scholar 

  • Lyman CP (1982) Sensitivity to arousal. In: Lyman CP et al. (eds) Hibernation and torpor in mammals and birds. Academic Press, New York, pp 77–91

    Google Scholar 

  • Lyman CP, Willis JS, Malan A, Wang LCH (eds) (1982) Hibernation and torpor in mammals and birds. Academic Press, New York

    Google Scholar 

  • Menaker M (1961) The free running period of the bat clock: seasonal variations at low body temperature. J Cell Comp Physiol 57:81–86

    Google Scholar 

  • Menaker M, Wisner S (1983) Temperature compensated circadian clock in the pineal of Anolis. Proc Natl Acad Sci USA 80:6119–6121

    Google Scholar 

  • Moore RY, Eichler VB (1972) Loss of a circadian adrenal corticosterone rhythm following suprachiasmatic lesions in the rat. Brain Res 42:201–206

    Google Scholar 

  • Pohl H (1961) Temperaturregulation und Tagesperiodik des Stoffwechsels bei Winterschläfern. Z Vergl Physiol 45:109–153

    Google Scholar 

  • Pohl H (1967) Circadian rhythms in hibernation and the influence of light. In: Fisher KC et al. (eds) Mammalian hibernation III. Oliver and Boyd, Edinburgh, pp 140–151

    Google Scholar 

  • Pohl H (1987) Cireadian pacemaker does not arrest in deep hibernation. Evidence for desynchronization from the light cycle. Experientia 43:293–294

    Google Scholar 

  • Rawson KS (1960) Biological clocks Cold Spring Harbor Symposia on Quantitative Biology. The Biological Laboratory, New York

    Google Scholar 

  • Ruby N, Ibuka N, Barnes B, Zucker I (1989) Suprachiasmatic nuclei influence torpor and circadian temperature rhythms in hamsters. Am J Physiol 257:R210-R215

    Google Scholar 

  • Ruf T, Heldmaier G (1987) Computerized body temperature telemetry in small animals: use of simple equipment and advanced noise suppression. Comput Biol Med 17:331–340

    Google Scholar 

  • Saint-Girons MC (1965) On the persistence of circadian rhythms in hibernating mammals. In: Aschoff J (ed) Circadian clocks. North-Holland, Amsterdam, pp 321–323

    Google Scholar 

  • South FE, Breazile JE, Dellmah HD, Epperly AD (1969) Sleep, hibernation and hypothermia in the yellow-bellied marmot (M. flaviventris). In: Musacchia XJ, Saunders JF (eds) Depressed metabolism. American Elsevier, New York, pp 277–310

    Google Scholar 

  • Steinlechner S, Heldmaier G, Weber C, Ruf T (1986) Role of photoperiod: pineal gland interaction in torpor control. In: Heller HC et al. (eds) Living in the cold. Elsevier, New York, pp 301–307

    Google Scholar 

  • Stephan FK, Zucker I (1972) Circadian rhythms in drinking behavior and locomotor activity of rats are eliminated by hypothalamic lesions. Proc Natl Acad Sci USA 69:1583–1586

    Google Scholar 

  • Strumwasser F (1959a) Factors in the pattern, timing and predictability of hibernation in the squirrel, Citellus beecheyi. Am J Physiol 196:8–14

    Google Scholar 

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

    Google Scholar 

  • Strumwasser F, Schlechte FR, Streeter J (1967) The internal rhythms of hibernators. In: Fisher KC et al. (eds) Mammalian hibernation III. Oliver and Boyd, Edinburgh, pp 110–139

    Google Scholar 

  • Sweeny BM, Hastings JW (1960) Biological clocks. Cold Spring Harbor Symposia on Quantitative Biology, The Biological Laboratory, New York

    Google Scholar 

  • Twente JW, Twente JA (1965) Effect of core temperature upon duration of hibernation of Citellus lateralis. J Appl Physiol 20:411–416

    Google Scholar 

  • Twente JW, Twente J (1987) Biological alarm clock arouses hibernating big brown bat Eptesicus fuscus. Can J Zool 65:1668–1674

    Google Scholar 

  • Twente JW, Twente J, Moy RM (1977) Regulation of arousal from hibernation by temperature in three species of Citellus. J Appl Physiol 42:191–195

    Google Scholar 

  • Vaňeček J, Janský L, Illnerová H, Hoffmann K (1985) Arrest of the circadian pacemaker driving the pineal melatonin rhythm in hibernating golden hamsters, Mesocricetus auratus. Comp Biochem Physiol 80A:21–23

    Google Scholar 

  • Walker JM, Glotzbach SF, Berger RJ, Heller HC (1977) Sleep and hibernation in ground squirrels (Citellus spp.): electrophysiological observations. Am J Physiol 233:R213-R221

    Google Scholar 

  • Willis JS (1982) The mystery of periodic arousal. In: Lyman CP et al. (eds) Hibernation and torpor in mammals and birds. Academic Press, New York, pp 91–103

    Google Scholar 

  • Zucker I, Bosches M, Dark J (1983) Suprachiasmatic nuclei influence circannual and circadian rhythms of ground squirrels. Am J Physiol 244:R472-R480

    Google Scholar 

Download references

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Canguilhem, B., Malan, A., Masson-Pévet, M. et al. Search for rhythmicity during hibernation in the European hamster. J Comp Physiol B 163, 690–698 (1994). https://doi.org/10.1007/BF00369521

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