Circadian rhythms of body temperature and motor activity in rodents

Allali KE, Achaâban MR, Bothorel B, Piro M, Bouâouda H, Allouchi ME, Ouassat M, Malan A, Pévet P. Entrainment of the circadian clock by daily ambient temperature cycles in the camel (Camelus dromedarius). Am J Physiol Regul Integr Comp Physiol 304: R1044 -R1052, 2013. First published March 13, 2013 doi:10.1152/ajpregu.00466.2012.-In mammals the light-dark (LD) cycle is known to be the major cue to synchronize the circadian clock. In arid and desert areas, the camel (Camelus dromedarius) is exposed to extreme environmental conditions. Since wide oscillations of ambient temperature (Ta) are a major factor in this environment, we wondered whether cyclic Ta fluctuations might contribute to synchronization of circadian rhythms. The rhythm of body temperature (Tb) was selected as output of the circadian clock. After having verified that Tb is synchronized by the LD and free runs in continuous darkness (DD), we submitted the animals to daily cycles of Ta in LL and in DD. In both cases, the Tb rhythm was entrained to the cycle of Ta. On a 12-h phase shift of the Ta cycle, the mean phase shift of the Tb cycle ranged from a few hours in LD (1 h by cosinor, 4 h from curve peaks) to 7-8 h in LL and 12 h in DD. These results may reflect either true synchronization of the central clock by Ta daily cycles or possibly a passive effect of Ta on Tb. To resolve the ambiguity, melatonin rhythmicity was used as another output of the clock. In DD melatonin rhythms were also entrained by the T a cycle, proving that the daily T a cycle is able to entrain the circadian clock of the camel similar to photoperiod. By contrast, in the presence of a LD cycle the rhythm of melatonin was modified by the T a cycle in only 2 (or 3) of 7 camels: in these specific conditions a systematic effect of T a on the clock could not be evidenced. In conclusion, depending on the experimental conditions (DD vs. LD), the daily T a cycle can either act as a zeitgeber or not.camel; circadian clock; body temperature; daily ambient temperature; melatonin; nonphotic entrainment RHYTHMICITY in physiological processes is a fundamental property of all living organisms (32). A number of biological functions display daily and seasonal variations in a way to anticipate and adapt to the upcoming cycling changes in environment (light, temperature, food availability, etc.). In mammals, the circadian clock, located in the suprachiasmatic nuclei of the hypothalamus (SCN), is central for these adaptive processes. This clock is a strong autonomous oscillator cycling with a period close to 24 h under constant conditions (23) and entrained by environmental cues to an exact period of 24 h. Thus SCN play a pivotal role to control numerous circadian biological rhythms such as those of body temperature (T b ), melatonin, or behavioral features. In all mammals studied, the light-dark cycle is the most powerful synchronizer (zeitgeber) of the master clock (for a review see Ref. 15). T b rhythm represents a robust output of the clock, widely used in clinical research to determine pro...

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“…after phase advances and phase delays of the LD cycle as classically described in the literature (5,12,16).…”

Section: Circadian Nature Of the T B Rhythmmentioning

confidence: 99%

Entrainment of the circadian clock by daily ambient temperature cycles in the camel (Camelus dromedarius)

Allali

Achaâban

Bothorel

et al. 2013

American Journal of Physiology-Regulatory, Integrative and Comp

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“…SCN cultures from these animals express circadian oscillations of Per1-luc expression indefinitely, while oscillations in cultured peripheral tissues damp after several cycles (Yamazaki et al, 2000). The phases of central and peripheral circadian oscillators are held in specific relationships under light-dark (LD) cycles (Yamazaki et al, 2000;Abe et al, 1 To whom correspondence should be addressed: Michael Menaker Department of Biology, University of Virginia, Charlottesville, VA 22903; Tel: 434-982-5767; Fax: 434-982-5626; e-mail: mm7e@virginia Like SCN lesion, prolonged constant light (LL) exposure disrupts behavioral circadian rhythms in rodents, resulting first in an increase in circadian period and then in arrhythmicity (Honma et al, 1996, Benstaali et al, 2001Canal-Corretger et al, 2000). It has been suggested that this effect of LL might be the result of disrupting the coupling among SCN cells (Mason 1991; Zlomanazuck et al, 1991;Ohta et al, 2005).…”

Section: Introductionmentioning

confidence: 99%

Effects of Preparation Time on Phase of Cultured Tissues Reveal Complexity of Circadian Organization

Yoshikawa¹,

Yamazaki

Menaker

2005

J Biol Rhythms

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The phases of central (SCN) and peripheral circadian oscillators are held in specific relationships under LD cycles, but in the absence of external rhythmic input may damp or drift out of phase with each other. Rats exposed to prolonged constant light become behaviorally arrhythmic, perhaps as a consequence of dissociation of phases among SCN cells. We asked whether individual central and peripheral circadian oscillators were rhythmic in LL treated arrhythmic rats and, if rhythmic, what were the phase relationships among them. We prepared SCN, pineal gland, pituitary and cornea cultures from transgenic Per1-luc rats whose body temperature and locomotor activity were arrhythmic, and from several groups of rhythmic rats held in LD, DD, and short-term LL. We measured mPer1 gene expression by recording light output with sensitive photomultipliers. Most of the cultures from all groups displayed circadian rhythms. This could reflect persistent rhythmicity in vivo prior to culture, or, alternatively, rhythmicity that may have been initiated by the culture procedure. To test this we cultured tissues at two different times 12 h apart and asked whether phase of the rhythm was related to culture time. The pineal, pituitary and SCN cultures showed partial or complete dependence of phase on culture time, while peak phases of the cornea cultures were independent of culture time in rhythmic rats, and were randomly distributed regardless of culture time in arrhythmic animals. These results suggest that in behaviorally arrhythmic rats oscillators in the pineal, pituitary and SCN had been arrhythmic or severely damped in vivo while the cornea oscillator was free-running. The peak phases of the SCN cultures were particularly sensitive to some aspect of the culture procedure since rhythmicity of SCN cultures from robustly rhythmic LDentrained rats was strongly influenced when the procedure was carried out at any time except the second half of the day. Keywords circadian organization; Period1; constant light; suprachiasmatic nucleus; pineal; pituitary; cornea; culture While the molecular mechanisms that generate circadian oscillations within cells have been extensively studied (Reppert and Weaver 2002;Lowrey and Takahashi, 2004), understanding of the mechanisms that connect the molecular framework to physiological function and behavior is still limited (Buijs et al., 2003). We have approached these questions using a transgenic rat model carrying a luciferase gene under the control of the mouse Period1 (Per1) promoter. SCN cultures from these animals express circadian oscillations of Per1-luc expression indefinitely, while oscillations in cultured peripheral tissues damp after several cycles (Yamazaki et al., 2000). The phases of central and peripheral circadian oscillators are held in specific relationships under light-dark (LD) cycles (Yamazaki et al., 2000;Abe et al., 1 To whom correspondence should be addressed: Michael Menaker Department of Biology, University of Virginia, Charlottesville, VA 22903; Tel: 434-982-5767; F...

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“…As a consequence, the light-dark cycle reliably exposes daily and seasonal time and is considered the primary zeitgeber (environmental cue) that entrains daily physiological and behavioural rhythms (Benstaali et al 2001;Reppert and Weaver 2002). Since the availability of environmental resources change in concurrence with changing levels of illumination across the day, the temporal organization of the locomotor activity rhythm of a species is vital.…”

Section: Introductionmentioning

confidence: 99%

“…Mammalian daily locomotor activity rhythms have been extensively used in studying photic entrainment of the circadian timing system and in unraveling its underlying mechanisms (Aschoff, 1981;Benstaali et al, 2001). A small number of laboratory-reared mammalian species (e.g.…”

Section: Introductionmentioning

confidence: 99%

Locomotor activity in the Namaqua rock mouse (Micaelamys namaquensis): entrainment by light manipulations

et al. 2014

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The locomotor activity rhythms of wild-caught Namaqua rock mice (Micaelamys namaquensis Smith, 1834) were examined under four light cycle regimes in order to quantitatively describe the daily expression of locomotor activity and to study the innate relationship between activity and the light-dark cycle. Activity was always significantly higher at night than in the day: 1) The LD1 light cycle (12L: 12D) established a distinct light-entrained and strongly nocturnal activity rhythm (99.11% nocturnal activity). The activity onset was prompt (ZT 12.2 ± 0.04) and activity continued without any prominent peaks or extended times of rest until the offset of activity at ZT 23.73 ± 0.08. 2). Evidence for the internal maintenance of locomotor activity was obtained from the constant dark cycle (DD) in which locomotor activity free ran (mean τ = 23.89 h) and 77.58% of the activity was expressed during the subjective night. 3) During re-entrainment (LD2; 12L: 12D), a nocturnal activity rhythm was re-established (98.65% nocturnal activity) and, 4) the inversion of the light cycle (DL; 12D: 12L) evoked a shift in activity that again revealed dark-induced locomotor activity (95.69% nocturnal activity). Females were consistently more active than males in all of the light cycles, but only under the DD and LD2 cycles were females significantly more active than males. Although this species is considered nocturnal from field observations, information regarding its daily expression of activity and the role of light in its entrainment is lacking. To the best of our knowledge this study is the first to report quantitatively on the species' daily rhythm of activity and to investigate its relationship to the light-dark cycle.

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Circadian rhythms of body temperature and motor activity in rodents

Cited by 98 publications

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Entrainment of the circadian clock by daily ambient temperature cycles in the camel (Camelus dromedarius)

Entrainment of the circadian clock by daily ambient temperature cycles in the camel (Camelus dromedarius)

Effects of Preparation Time on Phase of Cultured Tissues Reveal Complexity of Circadian Organization

Locomotor activity in the Namaqua rock mouse (Micaelamys namaquensis): entrainment by light manipulations

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