Seasonal aspects of sleep in the Djungarian hamster

BMC Neuroscience

Irene Tobler²  Tom Deboer¹  Svitlana Palchykova² 

[1] Department of Neurophysiology, Leiden University Medical Centre, Leiden, The Netherlands;Institute of Pharmacology and Toxicology, University of Zürich, Zürich, Switzerland

关键词: photoperiod;    spectral analysis;    sleep;    seasonality;    Djungarian hamster;    EEG;   

Others  :  1223233
DOI  :  10.1186/1471-2202-4-9

 received in 2003-02-24, accepted in 2003-05-19,  发布年份 2003

【 摘 要 】

Background

Changes in photoperiod and ambient temperature trigger seasonal adaptations in the physiology and behaviour of many species, including the Djungarian hamster. Exposure of the hamsters to a short photoperiod and low ambient temperature leads to a reduction of the polyphasic distribution of sleep and waking over the light and dark period. In contrast, a long photoperiod enhances the daily sleep-wake amplitude leading to a decline of slow-wave activity in NREM sleep within the light period. It is unknown whether these changes can be attributed specifically to photoperiod and/or ambient temperature, or whether endogenous components are contributing factors. The influence of endogenous factors was investigated by recording sleep in Djungarian hamsters invariably maintained at a low ambient temperature and fully adapted to a short photoperiod. The second recording was performed when they had returned to summer physiology, despite the maintenance of the 'winter' conditions.

Results

Clear winter-summer differences were seen in sleep distribution, while total sleep time was unchanged. A significantly higher light-dark cycle modulation in NREM sleep, REM sleep and waking was observed in hamsters in the summer physiological state compared to those in the winter state. Moreover, only in summer, REM sleep episodes were longer and waking bouts were shorter during the light period compared to the dark period. EEG power in the slow-wave range (0.75–4.0 Hz) in both NREM sleep and REM sleep was higher in animals in the summer physiological state than in those in the 'winter' state. In winter SWA in NREM sleep was evenly distributed over the 24 h, while in summer it decreased during the light period and increased during the dark period.

Conclusion

Endogenous changes in the organism underlie the differences in sleep-wake redistribution we have observed previously in hamsters recorded in a short and long photoperiod.

【 授权许可】

   
2003 Palchykova et al; licensee BioMed Central Ltd. This is an Open Access article: verbatim copying and redistribution of this article are permitted in all media for any purpose, provided this notice is preserved along with the article's original URL.

【 图 表 】

Figure 1.

Figure 2.

【 参考文献 】

• [1]Bartness TJ, Goldman BD: Mammalian pineal melatonin: a clock for all seasons. Experientia 1989, 45:939-945.
• [2]Hoffmann K: The influence of photoperiod and melatonin on testis size, body weight, and pelage colour in the Djungarian hamster (Phodopus sungorus). J Comp Physiol 1973, 85:267-282.
• [3]Hoffmann K: Testicular involution in short photoperiods inhibited by melatonin. Naturwissenschaften 1974, 61:364-365.
• [4]Hoffmann K: Effects of short photoperiods on puberty, growth and moult in the Djungarian hamster (Phodopus sungorus). J Reprod Fertil 1978, 54:29-35.
• [5]Arendt J, Symons AM, Laud C: Pineal function in the sheep: Evidence for a possible mechanism mediating seasonal reproductive activity. Experientia 1981, 37:584-586.
• [6]Illnerova H, Hoffmann K, Vanecek J: Adjustment of pineal melatonin and N-acetyltransferase rhythms to change from long to short photoperiod in the Djungarian hamster Phodopus sungorus. Neuroendocrinology 1984, 38:226-231.
• [7]Tamarkin L, Baird CJ, Almeida OF: Melatonin: a coordinating signal for mammalian reproduction? Science 1985, 227:714-720.
• [8]Lerchl A, Schlatt S: Influence of photoperiod on pineal melatonin synthesis, fur color, body weight, and reproductive function in the female Djungarian hamster, Phodopus sungorus. Neuroendocrinology 1993, 57:359-364.
• [9]Reiter RJ: The melatonin rhythm: both a clock and a calendar. Experientia 1993, 49:654-664.
• [10]Goldman BD: The Siberian hamster as a model for study of the mammalian photoperiodic mechanism. Adv Exp Med Biol 1999, 460:155-164.
• [11]Vivien-Roels B, Pitrosky B, Zitouni M, Malan A, Canguilhem B, Bonn D, Pevet P: Photoperiodic control of the seasonal variations in the daily pattern of melatonin synthesis in the European hamster, Cricetus cricetus. Ann N Y Acad Sci 1998, 839:386-388.
• [12]Elliott JA, Bartness TJ, Goldman BD: Role of short photoperiod and cold exposure in regulating daily torpor in Djungarian hamsters. J Comp Physiol [A] 1987, 161:245-253.
• [13]Stieglitz A, Steinlechner S, Ruf T, Heldmaier G: Cold prevents the light induced inactivation of pineal N-acetyltransferase in the Djungarian hamster, Phodopus sungorus. J Comp Physiol [A] 1991, 168:599-603.
• [14]Ruf T, Stieglitz A, Steinlechner S, Blank JL, Helmaier G: Cold exposure and food restriction facilitate physiological responses to short photoperiod in Djungarian hamsters (Phodopus sungorus). J Exp Zool 1993, 267:104-112.
• [15]Larkin JE, Jones J, Zucker I: Temperature dependence of gonadal regression in Syrian hamsters exposed to short day lengths. Am J Physiol Regul Integr Comp Physiol 2002, 282:R744-R752.
• [16]Messager S, Ross AW, Barrett P, Morgan PJ: Decoding photoperiodic time through Per1 and ICER gene amplitude. Proc Natl Acad Sci U S A 1999, 96:9938-9943.
• [17]Nuesslein-Hildesheim B, O'Brien JA, Ebling FJ, Maywood ES, Hastings MH: The circadian cycle of mPER clock gene products in the suprachiasmatic nucleus of the siberian hamster encodes both daily and seasonal time. Eur J Neurosci 2000, 12:2856-2864.
• [18]Daan S, Albrecht U, van der Horst GT, Illnerova H, Roenneberg T, Wehr TA, Schwartz WJ: Assembling a clock for all seasons: are there M and E oscillators in the genes? J Biol Rhythms 2001, 16:105-116.
• [19]Lincoln G, Messager S, Andersson H, Hazlerigg D: Temporal expression of seven clock genes in the suprachiasmatic nucleus and the pars tuberalis of the sheep: evidence for an internal coincidence timer. Proc Natl Acad Sci U S A 2002, 99:13890-13895.
• [20]Walker JM, Haskell EH, Berger RJ, Heller HC: Hibernation and circannual rhythms of sleep. Physiol Zool 1980, 53:8-11.
• [21]Barre V, Petterrousseaux A: Seasonal-Variations in Sleep-Wake Cycle in Microcebus murinus. Primates 1988, 29:53-64.
• [22]Wirz-Justice A, Wever RA, Aschoff J: Seasonality in freerunning circadian rhythms in man. Naturwissenschaften 1984, 71:316-319.
• [23]Wehr TA: The durations of human melatonin secretion and sleep respond to changes in daylength (photoperiod). J Clin Endocrinol Metab 1991, 73:1276-1280.
• [24]Wehr TA, Moul DE, Barbato G, Giesen HA, Seidel JA, Barker C, Bender C: Conservation of photoperiod-responsive mechanisms in humans. Am J Physiol 1993, 265:R846-R857.
• [25]Kohsaka M, Fukuda N, Honma K, Honma S, Morita N: Seasonality in human sleep. Experientia 1992, 48:231-233.
• [26]Tobler I: Behavioral sleep in the Asian elephant in captivity. Sleep 1992, 15:1-12.
• [27]Borbély AA, Neuhaus HU: Daily pattern of sleep, motor activity and feeding in the rat: effects of regular and gradually extended photoperiods. J Comp Physiol [A] 1978, 124:1-14.
• [28]Dijk DJ, Daan S: Sleep EEG spectral analysis in a diurnal rodent: Eutamias sibiricus. J Comp Physiol [A] 1989, 165:205-215.
• [29]Franken P, Tobler I, Borbély AA: Varying Photoperiod in the Laboratory Rat – Profound Effect on 24-H Sleep Pattern but No Effect on Sleep Homeostasis. Am J Physiol Regul Integr Comp Physiol 1995, 269:R691-R701.
• [30]Deboer T, Tobler I: Shortening of the photoperiod affects sleep distribution, EEG and cortical temperature in the Djungarian hamster. J Comp Physiol [A] 1996, 179:483-492.
• [31]Deboer T, Tobler I: Vigilance state episodes and cortical temperature in the Djungarian hamster: the influence of photoperiod and ambient temperature. Pflugers Arch 1997, 433:230-237.
• [32]Deboer T, Vyazovskiy VV, Tobler I: Long photoperiod restores the 24-h rhythm of sleep and EEG slow-wave activity in the Djungarian hamster (Phodopus sungorus). J Biol Rhythms 2000, 15:429-436.
• [33]Reiter RJ: Evidence for refractoriness of the pituitary-gonadal axis to the pineal gland in golden hamsters and its possible implications in annual reproductive rhythms. Anat Rec 1972, 173:365-371.
• [34]Loudon AS, Ihara N, Menaker M: Effects of a circadian mutation on seasonality in Syrian hamsters (Mesocricetus auratus). Proc R Soc Lond B Biol Sci 1998, 265:517-521.
• [35]Borbély AA: A two process model of sleep regulation. Hum Neurobiol 1982, 1:195-204.
• [36]Deboer T, Tobler I: Slow waves in the sleep electroencephalogram after daily torpor are homeostatically regulated. Neuroreport 2000, 11:881-885.
• [37]Heldmaier G, Steinlechner S: Seasonal pattern and energetics of short daily torpor in the Djungarian hamster, Phodopus sungorus. Oecologia 1981, 48:265-270.
• [38]T Ruf, S Steinlechner, G Heldmaier: Rhythmicity of body temperature and torpor in the Djungarian hamster, Phodopus sungorus. In Living in the cold II. Edited by A Malan, B Canguilhem. John Libbey Eurotext Ltd; 1989:53-61.
• [39]Taheri S, Zeitzer JM, Mignot E: The role of hypocretins (orexins) in sleep regulation and narcolepsy. Annu Rev Neurosci 2002, 25:283-313.
• [40]Pitrosky B, Kirsch R, Vivien-Roels B, Georg-Bentz I, Canguilhem B, Pevet P: The photoperiodic response in Syrian hamster depends upon a melatonin-driven circadian rhythm of sensitivity to melatonin. J Neuroendocrinol 1995, 7:889-895.
• [41]Garidou ML, Vivien-Roels B, Pevet P, Miguez J, Simonneaux V: Mechanisms regulating the marked seasonal variation in melatonin synthesis in the European hamster pineal gland. Am J Physiol Regul Integr Comp Physiol 2003, 284:R1043-R1052.
• [42]Hoffmann K, Illnerova H, Vanecek J: Comparison of pineal melatonin rhythms in young adult and old Djungarian hamsters (Phodopus sungorus) under long and short photoperiods. Neurosci Lett 1985, 56:39-43.
• [43]Huber R, Deboer T, Schwierin B, Tobler I: Effect of melatonin on sleep and brain temperature in the Djungarian hamster and the rat. Physiol Behav 1998, 65:77-82.
• [44]Deboer T, Tobler I: Chronic administration of melatonin reduces REM sleep in the Djungarian hamster (Phodopus sungorus). Neurosci Lett 1997, 231:118-122.
• [45]Werth E, Achermann P, Borbély AA: Brain topography of the human sleep EEG: antero-posterior shifts of spectral power. Neuroreport 1996, 8:123-127.
• [46]Cajochen C, Foy R, Dijk DJ: Frontal predominance of a relative increase in sleep delta and theta EEG activity after sleep loss in humans. Sleep Res Online 1999, 2:65-69.
• [47]Finelli LA, Borbély AA, Achermann P: Functional topography of the human nonREM sleep electroencephalogram. Eur J Neurosci 2001, 13:2282-2290.
• [48]Schwierin B, Achermann P, Deboer T, Oleksenko A, Borbély AA, Tobler I: Regional differences in the dynamics of the cortical EEG in the rat after sleep deprivation. Clinical Neurophysiology 1999, 110:869-875.
• [49]Vyazovskiy VV, Borbély AA, Tobler I: Interhemispheric sleep EEG asymmetry in the rat is enhanced by sleep deprivation. Journal of Neurophysiology 2002, 88:2280-2286.
• [50]Huber R, Deboer T, Tobler I: Topography of EEG dynamics after sleep deprivation in mice. Journal of Neurophysiology 2000, 84:1888-1893.
• [51]Palchykova S, Deboer T, Tobler I: Selective sleep deprivation after daily torpor in the Djungarian hamster. J Sleep Res 2002, 11:313-319.
• [52]Figala J, Hoffmann K, Goldau G: Zur Jahresperiodik beim Dsungarischen Zwerghamster Phodopus sungorus Pallas. Oecologia 1973, 12:89-118.
• [53]Deboer T, Franken P, Tobler I: Sleep and cortical temperature in the Djungarian hamster under baseline conditions and after sleep deprivation. J Comp Physiol [A] 1994, 174:145-155.
• [54]Horton TH, Yellon SM: Aging, Reproduction and the melatonin Rhythm in the Siberian Hamster. J. Biol Rhythms 2001, 16:243-253.
• [55]Tobler I, Jaqqi K, Borbely AA: Effects of melatonin and the melatonin receptor agonist S-20098 on the vigilance states, EEG spectra and the cortical temperature in the rat. J. Pineal Res 1994, 16:26-32.