- Research article
- Open Access
Seasonal aspects of sleep in the Djungarian hamster
© Palchykova et al; licensee BioMed Central Ltd. 2003
- Received: 24 February 2003
- Accepted: 19 May 2003
- Published: 19 May 2003
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.
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.
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.
- Djungarian hamster
- spectral analysis
Changes in photoperiod trigger seasonal adaptations in physiology and behaviour of many species . The adaptations are manifold and include changes in body weight, pelage colour and density, altered social and sexual behaviors, in many rodents gonadal regression and suppression of breeding, and in some species hibernation or episodes of daily torpor. In mammals, the main trigger for these changes is the shortening of the photoperiod that determines the duration of pineal melatonin secretion [1–11]. Seasonal changes in physiology can be facilitated by lowering of ambient temperature (TA) [12–15]. The encoding of seasonal time may involve clock genes, as suggested by the elevated expression of Per1 and Per2 genes in the SCN and pars tuberalis under a long photoperiod [16–19].
Few studies have addressed seasonal changes in sleep. Walker et al  reported annual changes in sleep in 4 golden mantled ground squirrels, with the largest amount of sleep in winter. Changes in sleep duration were found in 4 captive prosimians, Microcebus murinus, with major reductions of sleep in summer . In humans, under natural conditions in winter and under controlled short photoperiod conditions in the laboratory, sleep duration is increased when nights are long [22–24], but also changes restricted to timing and not duration of sleep have been reported . A behavioural study in elephants in captivity found an increase in sleep duration during the winter months . In contrast, in small rodents, including the rat, Siberian chipmunk, and Djungarian hamster, sleep duration was not affected by a change in photoperiod [27–31]. However, a marked redistribution of sleep occurred across 24 h when the animals were recorded in a long and a short photoperiod.
Seasonal differences in the vigilance states.
Hamsters in winter physiological state
Hamsters in summer physiological state
23.15 ± 0.94* °
27.43 ± 0.59°
624.03 ± 8.03
19.45 ± 0.90**
30.29 ± 0.81
640.16 ± 15.01
31.30 ± 0.90
29.17 ± 0.57°
702.13 ± 9.99
33.69 ± 0.93**
27.21 ± 0.48
685.50 ± 14.80
5.70 ± 0.33* °
5.00 ± 0.18° °
113.35 ± 4.58
6.93 ± 0.31**
4.35 ± 0.11
114.34 ± 2.89
Seasonal differences in duration and frequency of vigilance state episodes.
Hamsters in winter physiological state
Hamsters in summer physiological state
Episode duration (min)
6.35 ± 0.72
6.27 ± 0.47
6.21 ± 0.42
5.26 ± 0.47**
7.57 ± 0.81
6.75 ± 0.62
7.54 ± 0.31
7.39 ± 0.38
7.43 ± 0.35
7.94 ± 0.36
7.15 ± 0.31
7.40 ± 0.26
1.73 ± 0.07
1.67 ± 0.07
1.69 ± 0.06
2.08 ± 0.17***
1.64 ± 0.09
1.82 ± 0.12
Episode frequency (# per h)
4.15 ± 0.40
4.29 ± 0.29
4.25 ± 0.30
3.98 ± 0.25
4.20 ± 0.41
4.13 ± 0.34
4.48 ± 0.19
4.15 ± 0.23
4.26 ± 0.19
4.56 ± 0.19*
3.90 ± 0.23
4.12 ± 0.19
3.29 ± 0.20***
2.65 ± 0.15
2.86 ± 0.15
3.52 ± 0.27****
2.36 ± 0.14
2.75 ± 0.16
SWA in NREM sleep reflected the redistribution of TST in the light and dark period between the conditions. Thus, the LD amplitude increased significantly from winter to summer (Figure 2). No LD change in SWA in NREM sleep was observed in winter, while an increase of SWA was seen from the light to the dark period in summer. Within the SWA band, frequencies between 0.75-3.0 Hz increased significantly from winter to summer physiology (all hamsters: 378.07 ± 34.89 μV2 in winter and 537.67 ± 38.81 μV2 in summer, unpaired t-test, p < 0.01; n = 6: 386.05 ± 26.93 μV2 in winter and 493.96 ± 34.95 μV2 in summer, paired t-test, p = 0.068). An increase in EEG power was present in frequencies between 1.25 – 2.5 Hz also in REM sleep (not shown). Total EEG power (0.75–20.0 Hz) over all vigilance states did not differ between the hamsters in winter physiology and summer physiology (1368.34 ± 130.98 μV2 and 1650.48 ± 119.51 μV2, n = 10 and 11, respectively, unpaired t-test, p = 0.13; 1368.03 ± 128.19 μV2and 1513.63 ± 90.26 μV2, n = 6, paired t-test, p = 0.35).
The comparison of the 24-h EEG power spectrum between the two cortical derivations showed a frontal predominance in NREM sleep in the low frequency range both in the hamsters in winter physiology (1.25–2.5 Hz) and summer physiology (1.25–4.0 Hz). The difference between the derivations remained the same in the winter and summer physiology hamsters.
To establish whether small differences in TA or in brain temperature could have contributed to the differences in sleep, several correlations (Pearson product-moment correlation) were computed. No significant correlation was found between brain temperature and EEG parameters (total EEG power: r2 = 0.005, p = 0.77, n = 20, brain temperature data of one hamster were lacking; r2 = 0.25, p = 0.10, n = 12; LD SWA difference, r2 = 0.05, p = 0.34, n = 20 and r2 = 0.28, p = 0.08 n = 12; LD difference in the amount of NREM sleep, REM sleep and waking (n.s., not shown)). Also the correlations with TA were not significant (total EEG power, r2 = 0.03, p = 0.50, n = 20 and r2 = 0.02, p = 0.64 n = 12; LD SWA difference, r2 = 0.12, p = 0.132, n = 20 and r2 = 0.14, p = 0.24, n = 12; LD difference in the amount of NREM sleep, REM sleep and waking (n.s., not shown)).
The main change in sleep observed in hamsters recorded in a physiological state typical for winter and for summer was an enhancement of the sleep-wake amplitude. The total amount of vigilance states remained unchanged, while the polyphasic sleep-wake pattern was redistributed. These summer-winter differences are similar to those observed in hamsters recorded after a prolonged adaptation to a short photoperiod at 16°C or after adaptation to a long photoperiod at 22°C  or in hamsters that remained always at 14.5°C but were adapted first to a short and then to a long photoperiod . In the latter studies it remained open whether the changes were induced by the photoperiod or whether they have an endogenous component. Our results indicate that there is an endogenous component contributing to the seasonal changes in sleep.
The stability of sleep duration seems to be a feature of animals that exhibit a polyphasic sleep-wake pattern [27–31], since humans that typically have a monophasic sleep pattern, did increase sleep duration during the winter months [22–24]. The changes in SWA in NREM sleep reflected the changes in the amount of sleep within the light or dark period. In winter, when sleep was more evenly distributed between the light and dark period, SWA showed only a minimal LD amplitude. In contrast, in summer when the hamsters were more awake during the dark period, SWA exhibited concomitantly higher values compared to the light period. Thus, hamsters in the summer physiological state sleep less but more intensively during the dark period compared to their sleep in winter. These data are in accordance with the two-process model of sleep regulation that predicts that the homeostatic Process S, quantified by SWA reflects the previous sleep-wake history .
The sleep-wake redistribution between the winter and summer physiology animals was reflected also in the frequency and duration of vigilance state episodes. Waking episode duration was lower and the frequency of NREM sleep episodes was higher during the light period in summer physiology, when the hamsters slept more. No changes occurred in the hamsters in winter physiology when sleep was more evenly distributed over the 24 h.
Although day-length appears to be the primary environmental cue that the Djungarian hamster uses to initiate seasonally appropriate physiological and behavioural changes [2, 8, 14], ambient temperature and food restriction markedly affect the photoperiodic responses . In order to make sure that the changes we observed were reflecting endogenous mechanisms, several correlations were computed. Not even a trend between any of the effects on sleep and TA or brain temperature was observed. Also in a previous study, EEG power density in the slow-wave range had increased when hamsters were recorded first in a short photoperiod followed by a long photoperiod . In both studies other EEG frequencies were not affected. We have repeatedly observed a decrease of EEG power density over time in rats and hamsters chronically implanted with EEG electrodes. It is therefore unlikely that the present increase in SWA from winter to summer was due to technical artifacts.
In a previous paper we concluded that when the Djungarian hamster prepares for the harsh environment it will encounter during winter, it dissociates sleep homeostasis from the circadian clock . This was based on the data that showed that sleep homeostasis remained invariable in a long and short photoperiod, but the sleep-wake pattern had changed dramatically [31, 36]. Nevertheless, it was evident that the circadian clock remained functional, because other behavioural and physiological rhythms remained in synchrony with the light-dark cycle [32, 37], or free-ran in constant darkness . The present data show that when the animal's physiology returns to its summer characteristics while the short photoperiod and low TA are maintained, the circadian clock seems to regain control over the sleep-wake behaviour. This indicates that physiological changes occurring in the hamsters as they adapt to different photoperiods encompass also an interaction between the circadian clock and sleep homeostatic mechanisms.
Little is known about the mechanisms that underlie this interaction. Among the many adaptations to the short photoperiod, the most important advantage for survival the Djungarian hamster gains from the short photoperiod physiology is the change in metabolic rate . Recent developments in narcolepsy research integrate sleep and metabolism and suggest that changes in metabolic rate do influence sleep regulation . Also hormonal changes may be involved in the relation between sleep homeostasis and the circadian clock. For example it has been hypothesized that melatonin can serve both as a clock and as a calendar [1, 9, 40]. In the Djungarian hamster and the European hamster the duration and amplitude of melatonin secretion depends on photoperiod e.g. [6, 11, 41, 54], (A. Stieglitz, PhD thesis, 1995). When the duration of darkness was increased the onset of melatonin synthesis was delayed in both species, while the end corresponded to lights on in the Djungarian hamster only when adaptation to the photoperiod was sufficiently long [6, 11, 42]. Thus, in the European hamster an endogenous, seasonal component became evident in the short photoperiod, where the end of melatonin secretion was unrelated to the time of lights on. The evidence that melatonin may have a direct effect on sleep in the Djungarian hamster [43, 44] or in the rat [43, 55] is inconclusive.
Previous comparisons of the EEG power spectra in NREM sleep have shown a frontal predominance of the low EEG frequencies in humans [45–47], rats [48, 49], mice , and Djungarian hamsters . Interestingly, the frontal predominance in EEG power density in NREM sleep was not affected by the seasonal changes in the animal's physiology, supporting the interpretation that frontal predominance may reflect a functional component that is related to previous waking activities.
Our data show that light-dark differences in sleep-wake behavior and the time-course of EEG SWA recover when the hamsters spontaneously exhibit changes related to long photoperiod physiology. The circadian clock seems to regain control of the circadian sleep-wake distribution.
Adult Djungarian hamsters (Phodopus sungorus) raised under a natural photoperiod in summer, were kept individually in Macrolon cages (36 × 20 × 35 cm) with food and water available ad libitum, and maintained in a short photoperiod with 8-h light – 16-h dark (LD, light from 09:00 – 17:00 h; 7 Watt OSRAM DULUX EL energy saving lamp, approximately 30 lux). Mean ambient temperature (TA) was 15.5 ± 0.2°C.
When the weight reduction and the fur colour index (# 5–6 on the index scale 1–6, according to Figala et al ) as well as the gonadal regression indicated a strong adaptation to the short photoperiod (Figure 1), the 15 best adapted hamsters of a total of 32 were selected for i.p. implantation of temperature-sensitive transmitters (model X-M, Mini-mitter). At the age of 5.3 ± 0.4 months the hamsters (mean weight 26.6 ± 1.3 g, n = 15) were implanted under deep anaesthesia (Ketalar® 75 mg/kg, Parke-Davis; Rompun® 4 mg/kg, Bayer, i.p.) with gold-plated miniature screws (0.9 mm diameter) that served as EEG electrodes. Screws were placed epidurally over the right parietal cortex (2 mm lateral to midline and 2 mm posterior to bregma), right frontal cortex (2 mm lateral to midline and 2 mm anterior to bregma) and a reference electrode was placed over the cerebellum (2 mm posterior to lambda, on midline). A thermistor (Thermometrics, P20, R (25°C) = 1 kΩ, max. diam. = 0.5 mm, accuracy ± 0.05°C) was inserted horizontally between the skull and dura through a hole over the left frontal cortex (2–3 mm lateral to midline and 2 mm anterior to bregma) to measure cortical temperature (TCRT). Two gold wires (diameter 0.2 mm) inserted into the neck muscles served to record the electromyogram (EMG). The electrodes and thermistor were soldered to stainless steel wires and to a plug that was fixed to the skull with dental cement . Animals were connected to the cables and allowed to recover at least two weeks.
The two EEGs, EMG and TCRT were continuously recorded for 24-h when the animal's physiology was in 'winter' conditions (January – February). After 'summer' physiology was manifest in all animals, i.e. fur colour changed from white-grey to brown-grey and regrowth of gonads was evident, a second 24-h record was obtained in March. The short photoperiod and low TA were maintained throughout the entire experiment. Six hamsters contributed to both days, whereas four and five hamsters contributed with a recording in winter or summer, respectively.
Data acquisition and analysis
The EEG and EMG signals were amplified (amplification factor approx. 2,000), conditioned by analogue filters (high-pass filter: -3 dB at 0.016 Hz; low-pass filter: -3 dB at 40 Hz, less than -35 dB at 128 Hz) sampled with 512 Hz, digitally filtered (EEG: low-pass FIR filter 25 Hz; EMG: band-pass FIR filter 20–50 Hz) and stored with a resolution of 128 Hz. EEG power spectra were computed for 4-s epochs by a Fast Fourier Transform (FFT) routine. Adjacent 0.25-Hz bins were averaged into 0.5-Hz (0.25 – 5.0 Hz) and 1.0-Hz (5.25–25.0 Hz) bins. The EMG was full-wave rectified and integrated over 4-s epochs, TCRT and TA inside the cage were sampled at 4-s intervals. Before each recording the EEG and EMG channels were calibrated with a 10 Hz sine wave, 300 μV peak-to-peak signal.
The three vigilance states NREM sleep, REM sleep and waking were scored for 4-s epochs as in previous studies [30, 53]. Vigilance states were determined off-line by visual inspection of the parietal and frontal EEG and EMG records and EEG power in the slow-wave range (0.75–4.0 Hz). Epochs containing EEG artifacts in both derivations or in a single derivation were excluded from spectral analyses of both EEG derivations (14.2 ± 0.9 SEM % of recording time. Artifacts occurred mainly during active waking: 24.4 ± 1.8 SEM % of waking). Vigilance states could always be determined.
The duration and frequency of vigilance state episodes were determined according to criteria described previously [30, 53]. Differences in the EEG spectrum between the winter and summer recording were tested by ANOVA for repeated measures (rANOVA) or ANOVA. Whenever ANOVA reached significance, differences were evaluated by post hoc two-tailed paired t-tests within days or by unpaired t-test between two days. LD differences were tested with post hoc two-tailed paired t-tests within days or by unpaired t-test between two days.
All statistical comparisons of data from recordings performed in hamsters in winter and summer physiology were performed twice, once for the n = 6 hamsters which had been recorded both in winter and summer physiology (paired tests), and once for the entire group (n = 10–11; unpaired tests).
We thank Dr. G. Heldmaier for providing us with the hamsters and Dr. A. Borbély for critical reading of the manuscript. The study was supported by the Swiss National Science Foundation grant nr. 3100-053005.97/2.
- Bartness TJ, Goldman BD: Mammalian pineal melatonin: a clock for all seasons. Experientia. 1989, 45: 939-945.PubMedView ArticleGoogle Scholar
- 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.View ArticleGoogle Scholar
- Hoffmann K: Testicular involution in short photoperiods inhibited by melatonin. Naturwissenschaften. 1974, 61: 364-365.PubMedView ArticleGoogle Scholar
- Hoffmann K: Effects of short photoperiods on puberty, growth and moult in the Djungarian hamster (Phodopus sungorus). J Reprod Fertil. 1978, 54: 29-35.PubMedView ArticleGoogle Scholar
- 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.PubMedView ArticleGoogle Scholar
- 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.PubMedView ArticleGoogle Scholar
- Tamarkin L, Baird CJ, Almeida OF: Melatonin: a coordinating signal for mammalian reproduction?. Science. 1985, 227: 714-720.PubMedView ArticleGoogle Scholar
- 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.PubMedView ArticleGoogle Scholar
- Reiter RJ: The melatonin rhythm: both a clock and a calendar. Experientia. 1993, 49: 654-664.PubMedView ArticleGoogle Scholar
- Goldman BD: The Siberian hamster as a model for study of the mammalian photoperiodic mechanism. Adv Exp Med Biol. 1999, 460: 155-164.PubMedView ArticleGoogle Scholar
- 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.PubMedView ArticleGoogle Scholar
- 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.View ArticleGoogle Scholar
- 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.View ArticleGoogle Scholar
- 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.PubMedView ArticleGoogle Scholar
- 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.PubMedView ArticleGoogle Scholar
- 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. 10.1073/pnas.96.17.9938.PubMedPubMed CentralView ArticleGoogle Scholar
- 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. 10.1046/j.1460-9568.2000.00173.x.PubMedView ArticleGoogle Scholar
- 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.PubMedView ArticleGoogle Scholar
- 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. 10.1073/pnas.212517599.PubMedPubMed CentralView ArticleGoogle Scholar
- Walker JM, Haskell EH, Berger RJ, Heller HC: Hibernation and circannual rhythms of sleep. Physiol Zool. 1980, 53: 8-11.View ArticleGoogle Scholar
- Barre V, Petterrousseaux A: Seasonal-Variations in Sleep-Wake Cycle in Microcebus murinus. Primates. 1988, 29: 53-64.View ArticleGoogle Scholar
- Wirz-Justice A, Wever RA, Aschoff J: Seasonality in freerunning circadian rhythms in man. Naturwissenschaften. 1984, 71: 316-319.PubMedView ArticleGoogle Scholar
- Wehr TA: The durations of human melatonin secretion and sleep respond to changes in daylength (photoperiod). J Clin Endocrinol Metab. 1991, 73: 1276-1280.PubMedView ArticleGoogle Scholar
- 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.PubMedGoogle Scholar
- Kohsaka M, Fukuda N, Honma K, Honma S, Morita N: Seasonality in human sleep. Experientia. 1992, 48: 231-233.PubMedView ArticleGoogle Scholar
- Tobler I: Behavioral sleep in the Asian elephant in captivity. Sleep. 1992, 15: 1-12.PubMedGoogle Scholar
- 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.View ArticleGoogle Scholar
- Dijk DJ, Daan S: Sleep EEG spectral analysis in a diurnal rodent: Eutamias sibiricus. J Comp Physiol [A]. 1989, 165: 205-215.View ArticleGoogle Scholar
- 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.Google Scholar
- 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.View ArticleGoogle Scholar
- 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.PubMedView ArticleGoogle Scholar
- 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.PubMedView ArticleGoogle Scholar
- 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.PubMedView ArticleGoogle Scholar
- 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. 10.1098/rspb.1998.0325.View ArticleGoogle Scholar
- Borbély AA: A two process model of sleep regulation. Hum Neurobiol. 1982, 1: 195-204.PubMedGoogle Scholar
- Deboer T, Tobler I: Slow waves in the sleep electroencephalogram after daily torpor are homeostatically regulated. Neuroreport. 2000, 11: 881-885.PubMedView ArticleGoogle Scholar
- Heldmaier G, Steinlechner S: Seasonal pattern and energetics of short daily torpor in the Djungarian hamster, Phodopus sungorus. Oecologia. 1981, 48: 265-270.View ArticleGoogle Scholar
- 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. 1989, John Libbey Eurotext Ltd, 53-61.Google Scholar
- Taheri S, Zeitzer JM, Mignot E: The role of hypocretins (orexins) in sleep regulation and narcolepsy. Annu Rev Neurosci. 2002, 25: 283-313. 10.1146/annurev.neuro.25.112701.142826.PubMedView ArticleGoogle Scholar
- 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.PubMedView ArticleGoogle Scholar
- 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.PubMedView ArticleGoogle Scholar
- 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. 10.1016/0304-3940(85)90437-9.PubMedView ArticleGoogle Scholar
- 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. 10.1016/S0031-9384(98)00125-5.PubMedView ArticleGoogle Scholar
- Deboer T, Tobler I: Chronic administration of melatonin reduces REM sleep in the Djungarian hamster (Phodopus sungorus). Neurosci Lett. 1997, 231: 118-122. 10.1016/S0304-3940(97)00522-3.PubMedView ArticleGoogle Scholar
- Werth E, Achermann P, Borbély AA: Brain topography of the human sleep EEG: antero-posterior shifts of spectral power. Neuroreport. 1996, 8: 123-127.PubMedView ArticleGoogle Scholar
- 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.PubMedGoogle Scholar
- Finelli LA, Borbély AA, Achermann P: Functional topography of the human nonREM sleep electroencephalogram. Eur J Neurosci. 2001, 13: 2282-2290. 10.1046/j.0953-816x.2001.01597.x.PubMedView ArticleGoogle Scholar
- 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. 10.1016/S1388-2457(99)00020-6.PubMedView ArticleGoogle Scholar
- 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.PubMedView ArticleGoogle Scholar
- Huber R, Deboer T, Tobler I: Topography of EEG dynamics after sleep deprivation in mice. Journal of Neurophysiology. 2000, 84: 1888-1893.PubMedGoogle Scholar
- Palchykova S, Deboer T, Tobler I: Selective sleep deprivation after daily torpor in the Djungarian hamster. J Sleep Res. 2002, 11: 313-319. 10.1046/j.1365-2869.2002.00310.x.PubMedView ArticleGoogle Scholar
- Figala J, Hoffmann K, Goldau G: Zur Jahresperiodik beim Dsungarischen Zwerghamster Phodopus sungorus Pallas. Oecologia. 1973, 12: 89-118.View ArticleGoogle Scholar
- 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.View ArticleGoogle Scholar
- Horton TH, Yellon SM: Aging, Reproduction and the melatonin Rhythm in the Siberian Hamster. J. Biol Rhythms. 2001, 16: 243-253.PubMedView ArticleGoogle Scholar
- 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.PubMedView ArticleGoogle Scholar
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