Daily activity patterns of a nocturnal and a diurnal rodent in a seminatural environment

The entrainment of circadian rhythms by light-dark (LD) cycles has been extensively investigated in laboratory studies. In almost all of these studies, organisms have not been allowed to modulate their exposure to the LD cycle. In the present study, the rhythm of running-wheel activity was investigated in nocturnal (domestic mice) and diurnal (Nile grass rats) rodents provided with light-tight nest boxes and maintained under long and short photoperiods. Photoperiod length had a significant effect on the duration of the daily active phase (alpha), on the phase angle of entrainment (psi), and on diurnality or nocturnality in both species. The availability of a nest box had a modest effect only on the variability of activity onsets. Neither in the nocturnal nor in the diurnal species was there any evidence of entrainment by frequency demultiplication or of entrainment without photic stimulation at either dawn or dusk. These results indicate that at least in the species studied, the ability of rodents to modulate their exposure to the LD cycle does not have a major effect on photic entrainment.     

Fos expression in the suprachiasmatic nucleus in response to light stimulation in a solitary and social species of African mole-rat (family Bathyergidae)

Mole-rats are strictly subterranean rodents that are rarely exposed to environmental light. They are well adapted to their environment and have reduced eyes and a severely regressed visual system. It has been shown, however, that mole-rats do exhibit endogenous circadian rhythms that can be entrained, suggesting an intact and functional circadian system. To determine whether light is the entraining agent in these animals, Fos expression in response to light pulses at different circadian times was investigated to obtain phase response curves. Light is integrated effectively in the suprachiasmatic nucleus of the Cape mole-rat (Georychus capensis), and Fos expression is gated according to the phase of the circadian clock. The Fos response in the Cape mole-rat was comparable to that of aboveground rodents. In contrast, the highveld mole-rat (Cryptomys hottentotus pretoriae) was less sensitive to light and did not show a selective Fos response according to the phase of the circadian cycle. Social species appear to be less sensitive to light than their solitary counterparts, which compares well with results from locomotor activity studies.     

PER2 rhythms in the amygdala and bed nucleus of the stria terminalis of the diurnal grass rat (Arvicanthis niloticus)

The suprachiasmatic nucleus (SCN) of the hypothalamus is the central pacemaker that controls circadian rhythms in mammals. In diurnal grass rats (Arvicanthis niloticus), many functional aspects of the SCN are similar to those of nocturnal rodents, making it likely that the difference in the circadian system of diurnal and nocturnal animals lies downstream from the SCN. Rhythms in clock genes expression occur in several brain regions outside the SCN that may function as extra-SCN oscillators. In male grass rats PER1 is expressed in the oval nucleus of the bed nucleus of the stria terminalis (BNST-ov) and in the central and basolateral amygdala (CEA and BLA, respectively); several features of PER1 expression in these regions of the grass rat brain differ substantially from those of nocturnal species. Here we describe PER2 rhythms in the same three brain regions of the grass rat. In the BNST-ov and CEA PER2 expression peaked early in the light period Zeitgeber time (ZT) 2 and was low during the early night, which is the reverse of the pattern of nocturnal rodents. In the BLA, PER2 expression was relatively low for most of the 24-h cycle, but showed an acute elevation late in the light period (ZT10). This pattern is also different from that of nocturnal rodents that show elevated PER2 expression in the mid to late night and into the early day. These results are consistent with the hypothesis that diurnal behavior is associated with a phase change between the SCN and extra-SCN oscillators.     

Restricted feeding and circadian activity rhythms of a predatory marsupial, Dasyuroides byrnei

There is considerable disagreement as to whether food availability entrains circadian activity rhythms in omnivorous laboratory rodents. However, in carnivorous mammals a restricted feeding regime could act as a zeitgeber because the predator should hold a periodism correlated to that of the prey. Nevertheless, a restricted feeding schedule does not dominate the LD cycle for entrainment of circadian activity rhythms of the nocturnal predator Dasyuroides byrnei, nor does it entrain the free-running activity rhythms in DD. Anticipatory wheel running prior to food availability was observed in most animals. Some evidence for weak coupling between LD-entrained and meal-associated oscillators was indicated by occurrences of relative coordination. This species does not appear to have a dominance hierarchy of zeitgebern different to that reported for laboratory rodents. One would have predicted that it would have been ecologically adaptive for cycles of food availability to be more important than the LD cycle in this species.     

Circadian rhythms of locomotor activity in naked mole-rats (Heterocephalus glaber)

A wide variety of organisms exhibit various circadian rhythms in their behavior and physiology. Circadian rhythms are regulated by internal clocks that are generally entrained primarily by the environmental light:dark (L:D) cycle. There have been few studies of circadian rhythms in fossorial species that inhabit an environment where day-night variations are minimal and where exposure to light occurs infrequently. In this study, circadian patterns of wheel-running activity were examined in naked mole-rats (Heterocephalus glaber). Naked mole-rats are fossorial and eusocial, living in colonies of 60-70 animals with only one breeding female. Most individual mole-rats that ran on wheels (65%) exhibited robust circadian rhythms of locomotor activity, entrained to various L:D cycles, and free-ran in constant darkness (DD) with taus averaging 23.5 h. The remainder of the animals either free-ran or were arrhythmic under the various L:D cycles. Mole-rats generally failed to entrain to non-24-h T-cycles with period lengths ranging from T=23 h to T=25 h. There was considerable inter-individual variation in the circadian patterns of locomotor activity in naked mole-rats as is observed in other subterranean mammals that have been studied. In contrast to the results obtained when mole-rats were individually housed with access to running wheels, circadian rhythms of general locomotor activity were typically not observed for animals monitored while they were housed in a colony setting. However, clear nocturnal rhythms of general locomotor activity were displayed by four males while residing in their home colonies. Two of these males exhibited the physical appearance of a disperser morph - subordinate individuals that are believed to leave their home colonies to achieve reproductive opportunities elsewhere. All four of these males were among the largest males in their respective colonies. These results demonstrate that although naked mole-rats are not frequently exposed to light, the species has retained the capacity to exhibit locomotor patterns of circadian rhythmicity and has the ability to entrain to 24-h L:D cycles. The possible adaptive function of this circadian capacity is discussed.     

Lability and diversity of circadian rhythms of cotton rats Sigmodon hispidus

Cotton rats (Sigmodon hispidus) were maintained from birth in constant LD 14:10 photoperiods and temperatures. Wheel running was diurnal for 6 of 13 juvenile rats and nocturnal for most others. Most diurnal rats eventually added nocturnal activity components. In constant darkness the activity rhythms of adult rats free-ran with a period of 23.2 +/- 0.3 h; in constant illumination the period was 24.7 +/- 0.1 h, in conformation to Aschoff's rule for nocturnal rodents. Some previously nocturnal adult rats eventually adopted stable diurnal activity cycles and other were successively nocturnal, diurnal for 6 mo, and then nocturnal again while maintained in the LD 14:10 photoperiod. The existence of multiple activity types, as well as the spontaneous inversions from nocturnal to diurnal status substantiate and extend field observations of this species. Seasonal inversions from nocturnal to diurnal activity, previously attributed to fluctuating environmental conditions, may also be subject to regulation by endogenous processes. It is suggested that spontaneous phase reversals in activity reflect changes in entrainment of circadian pacemakers by the light-dark cycle or altered relations between such pacemakers and the overt activity rhythm.     

Circadian phase alteration by GABA and light differs in diurnal and nocturnal rodents during the day

These studies investigated the circadian effects of light and gamma aminobutyric acid-A (GABAA) receptor activation in the suprachiasmatic nucleus (SCN) of the diurnal unstriped Nile grass rat (Arvicanthis niloticus). Microinjection of the GABAA agonist muscimol into the SCN during the day produced phase shifts that were opposite in direction to those previously reported in nocturnal rodents. In addition, light had no significant effect on the magnitude of muscimol-induced phase delays during the daytime. Injection of muscimol during the night, however, significantly inhibited light-induced phase delays and advances in a manner similar to that previously reported in nocturnal rodents. Therefore, the circadian effects of GABAA receptor activation are similar in diurnal and nocturnal species during the night but differ significantly during the day.     

Daily rhythms in PER1 within and beyond the suprachiasmatic nucleus of female grass rats (Arvicanthis niloticus)

Although circadian rhythms of males and females are different in a variety of ways in many species, their mechanisms have been primarily studied in males. Furthermore, rhythms are dramatically different in diurnal and nocturnal animals but have been studied predominantly in nocturnal ones. In the present study, we examined rhythms in one element of the circadian oscillator, the PER1 protein, in a variety of cell populations in brains of diurnal female grass rats. Every 4 h five adult female grass rats kept on a 12-h light/dark (LD) cycle were perfused and their brains were processed for immunohistochemical detection of PER1. Numbers of PER1-labeled cells were rhythmic not only within the suprachiasmatic nucleus (SCN), the locus of the primary circadian clock in mammals, but also in the peri-suprachiasmatic region, the oval nucleus of the bed nucleus of the stria terminalis, the central amygdala, and the nucleus accumbens. In addition, rhythms were detected within populations of neuroendocrine cells that contain tyrosine hydroxylase. The phase of the rhythm within the SCN was advanced compared with that seen previously in male grass rats. Rhythms beyond the SCN were varied and different from those seen in most nocturnal species, suggesting that signals originating in the SCN are modified by its direct and/or indirect targets in different ways in nocturnal and diurnal species.     

Circadian rhythms in the rat: Constant darkness,entrainment to T cycles and to skeleton photoperiods

Free running activity and drinking rhythms of male Sprague-Dawley rats were observed in constant darkness (DD) for up to 44 days. The average period of the rhythms ($\text{τ}{}_{\mathrm{<mtext>dd</mtext>}}$) was 24.2 hr (±0.12 hr) and the activity time was near one half of the circadian cycle. In the second experiment, rats were entrained to T cycles (T=period) with 2 hr of light per cycle. At T=23 and T=26 about one half of the rats entrained indicating that these periods are near the limits of entrainment. T=23 induced a lasting aftereffect on $\text{τ}{}_{\mathrm{<mtext>dd</mtext>}}$ while T=26 affected $\text{τ}{}_{\mathrm{<mtext>dd</mtext>}}$ only briefly. In contrast to some other nocturnal rodents, activity time was not compressed as T neared the limits of entrainment. In the third experiment, rats and hamsters were entrained to 24 hr skeleton photoperiods (two 1 hr light pulses/cycle). Rats phase jumped to the longer subjective night when the interval between the light pulses was reduced to 6 or 5 hr, while most hamsters phase jumped at 3.5 hr. Furthermore, all rats phase jumped by means of delaying transients while most hamsters showed advancing transients. Finally, while skeleton photoperiods compressed activity time in hamsters to 6 hr or less, activity time remained fairly constant in rats. These results demonstrate considerable differences in the organization of the circadian system among commonly studied nocturnal rodents.     

Circadian rhythms in the short-tailed shrew, Blarina brevicauda

Circadian rhythms of wheel running and feeding were measured in the short-tailed shrew. Shrews were strongly nocturnal, and their activity rhythms entrained to both long-day (LD 16:8) and short-day (LD 6:18) photocycles. Under conditions of continuous light (LL) or darkness (DD), the activity rhythms free-ran with average periodicities of 25.1 hours and 24.1 hours, respectively. In LL the level of activity was depressed, and in some cases wheel running was completely inhibited. No significant sex differences were observed in the period or amplitude of the monitored circadian rhythms. All shrews fed throughout the day and night; however, unlike in previous reports, ultradian periods of feeding behavior were not found. The results are related to Aschoff's four observations for the effect of light on activity rhythms in nocturnal rodents.     

Circadian feeding and drinking rhythms in the rat under complete and skeleton photoperiods

Feeding and drinking rhythms were studied in rats maintained under 24-hr light-dark (LD) cycles with various photoperiods, under two-pulse (2P) and one-pulse (1P) skeleton photoperiods, and under constant dark (DD). Rhythmic waveforms were similar under complete LD cycles and corresponding skeleton photoperiods, indicating that these rhythms mainly reflect the entrainment of underlying circadian pacemakers. Little or no role was found for masking effects of light on circadian feeding and drinking waveforms. Entrainment was found to depend mainly on the timing of the dawn light signal, whether it was a 15-min light pulse or a dark-to-light transition initiating a complete photoperiod. Furthermore, the use of 1P schedules revealed that a dawn signal was sufficient for entrainment. These results closely match those obtained for motor activity measures in other nocturnal rodent species, and generally conform to the predictions of Pittendrigh's nonparametric theory of entrainment. Furthermore, the close correspondence of the two rhythms during entrainment, phase-jumps, and free-running (DD) conditions indicates that they are controlled by common circadian pacemakers.     

Circadian pacemakers in lizards: phase-response curves and effects of pinealectomy

Phase-response curves (PRCs) for 6-h fluorescent light pulses are described for both intact (sham-pinealectomized) and pinealectomized iguanid lizards (Sceloporus occidentalis). Although strongly diurnal in habit the PRC for intact lizards is more typical of those seen in nocturnal rodents. Other "nocturnal" characteristics of this lizard include the fact that the average free-running period (tau) is less than 24 h and the average tau in continuous light is longer than that observed in continuous darkness. The PRC for pinealectomized lizards is greatly distorted relative to that obtained from intact lizards. This "distortion" is discussed in terms of the role of the pineal as a coupling device or as a pacemaker within a multioscillator circadian system. In some individuals pinealectomy was also associated with 1) increased instability in free-running activity rhythms or arrhythmicity and 2) nocturnal entrainment to LD 12:12.     

Comparison of synchronization of primate circadian rhythms by light and food.

Several circadian rhythms in squirrel monkeys (Saimiri sciureus) entrained by two different agents were studied to compare their mode of coupling with the environmental zeitgebers. Synchronization was accomplished either by light-dark cycles consisting of 12 h of 600 lx followed by 12 h of less than 1 lx (LD 12:12), or by eat-fast cycles in which the animals could eat for 3 h and then had to fast for the remaining 21 h each day (EF 3:21). The rhythms of drinking, colonic temperature, and urinary potassium and water excretion were measured in chair-acclimatized monkeys. The drinking and urinary rhythms were more reproducible (smaller mean variance) and more stable (smaller standard deviation of the timing of a phase reference point) in EF than in LD cycles, whereas the temperature rhythm was more tightly controlled by LD cycles than by EF cycles. In constant light an 8-h phase delay in the EF cycle caused the drinking and urinary rhythms to resynchronize to the EF cycle within one day, while the temperature rhythm required about 6 days to resynchronize. In contrast, previously published data for a similar phase delay in the LD cycle with food available ad libitum show that the drinking and temperature rhythms resynchronized more rapidly than the urinary rhythms. These results indicate that separate mechanisms are involved in transducing temporal cues from LD and EF cycles in the circadian timekeeping system of these nonhuman primates.     

Circadian rhythms of small carnivores and the effect of restricted feeding on daily activity

Restricted daily feeding can entrain an endogenous circadian clock of rodents. Carnivores have not been tested even though, unlike rodents, the availability of their foods can naturally vary with the light-dark cycle. In addition, very little is known of the characteristics of carnivore circadian rhythms in constant illumination. The locomotor activities of weasels and minks were measured on running wheels and tilt floors in LD 12:12 and constant illumination. The animals were then subjected to daily restricted feeding to determine their ability to anticipate the arrival of food. Weasels and minks anticipated food delivery but endogenous control was not unequivocally demonstrated. Anticipatory activity was suppressed during days of food excess but exhibited during days of deprivation when these conditions were presented on alternating days. The characteristics of mink activity rhythms in constant light and dark are consistent with Aschoff's rule for nocturnal animals. Free-running rhythms were not measurable for most weasels due to arhythmicity or lack of data.     

Circadian rhythm dissociation in an environment with conflicting temporal information.

The relative contributions of light-dark (LD) cycles and feeding (EF) cycles in providing temporal information to the circadian time-keeping system were examined in chair-acclimatized squirrel monkeys (Saimiri sciureus). The circadian rhythms of drinking, colonic temperature, urine volume, and urinary potassium excretion were measured with the LD and EF cycles providing either conflicting phases or periods. In conflicting phase experiments, animals were exposed to 24-h LD cycles consisting of 12 h of 600 lx followed by 12 h of less than 1 ls and concurrent 24-h EF cycles in which the animals ate for 3 h and then fasted for 21 h. One group had food available at the beginning and a second group at the end of the light period. In conflicting period experiments, monkeys were exposed to 23-h LD cycles (LD 11.5:11.5) and 24-h EF cycles (EF 3:21). Analysis of the rhythms showed that both phase and period information were conveyed to the drinking and urinary rhythms by the EF cycle, and to the temperature rhythm by the LD cycle.     

Potentiation of the resetting effects of light on circadian rhythms of hamsters using serotonin and neuropeptide Y receptor antagonists

Circadian rhythms are entrained by light/dark cycles. In hamsters, the effects of light on circadian rhythms can be modulated by serotonergic input to the suprachiasmatic nucleus from the raphe nuclei and by neuropeptide Y containing afferents to the suprachiasmatic nucleus from the intergeniculate leaflet in the thalamus. In this study we measured effects of compounds acting on serotonergic 1A and neuropeptide Y Y5 receptors to determine if combined serotonergic-neuropeptide Y inhibition could synergistically potentiate effects of light on rhythms. We used mixed serotonergic agonist/antagonists BMY 7378 or NAN-190 as well as a neuropeptide Y Y5 antagonist CP-760,542. Both BMY 7378 and NAN-190 are thought to block serotonin release via acting as agonists at the 5-hydroxytryptamine 1A (5-HT1A) autoreceptors on cells in the raphe, and also block response of target cells by acting as antagonists at post-synaptic 5-HT1A receptors, for example, in the suprachiasmatic nuclei or the intergeniculate leaflet. Replicating prior work, we found that pretreatment with either drug alone increased the phase shift to light at circadian time 19. The combined effect of BMY 7378 and CP-760,542 given prior to light at circadian time 19 was to further potentiate the subsequent phase shift in wheel-running rhythms (the phase shift was 317% of controls; light alone: 1.35 h phase shift vs. BMY 7378, CP-760,542, and light: 4.27 h phase shift). Combined treatment with NAN-190 and CP-760,542 produced a light-induced phase shift 576% of controls (phase shift to light alone: 1.23 h vs. NAN-190, CP-760,542, and light: 7.1 h phase shift). These results suggest that the resetting effects of light on circadian rhythms can be greatly potentiated in hamsters by using pharmacological treatments that block both serotonergic and neuropeptide Y afferents to the suprachiasmatic nuclei.     

Circadian activity rhythms in the spiny mouse, Acomys cahirinus

Circadian locomotor rhythms were examined in adult common spiny mice, Acomys cahirinus. Spiny mice demonstrated nocturnal activity, with onset of activity coinciding promptly with onset of darkness. Re-entrainment to 6-h delays of the light-dark cycle was accomplished faster than to 6-h advances. Access to running wheels yielded significant changes in period and duration of daily activity. Novelty-induced wheel running had no effect on phase of activity rhythms. Circadian responses to light at various times of the circadian cycle were temporally similar to those observed in other nocturnal rodent species. No gender differences were observed in any of the parameters measured.     

Entrainment of the circadian activity rhythm to the light cycle: Effective light intensity for a Zeitgeber in the retinal degenerate C3H mouse and the normal C57BL mouse

Effective light intensities for entrainment of activity rhythms were obtained in the retinal degenerated C3Hf/He mice and the normal C57BL/6J mice. The circadian activity rhythms of the mice were examined under LD 12:12 cycles with one of five different levels of light (L phase) and complete darkness (D phase). The thresholds of a Zeitgeber, defined as the light intensity effective for 50% entrainment, were estimated between 1 lux and 5 lux in the C3H and lower than 0.01 lux in the C57BL mice. These results suggest that at least two different kinds of photoreceptor including rods and cones participate in the photic entrainment of the circadian activity rhythms.     

A novel quantitative trait locus on mouse chromosome 18, "era1," modifies the entrainment of circadian rhythms

STUDY OBJECTIVE: The mammalian circadian clock in the suprachiasmatic nuclei (SCN) of the hypothalamus conveys 24-h rhythmicity to sleep-wake cycles, locomotor activity, and other behavioral and physiological processes. The timing of rhythms relative to the light/dark (LD12:12) cycle is influenced in part by the endogenous circadian period and the time of day specific sensitivity of the clock to light. We now describe a novel circadian rhythm phenotype, and a locus influencing that phenotype, in a segregating population of mice. METHODS: By crossbreeding 2 genetically distinct nocturnal strains of mice (Cast/Ei and C57BL/6J) and backcrossing the resulting progeny to Cast/Ei, we have produced a novel circadian phenotype, called early runner mice. RESULTS: Early runner mice entrain to a light/dark cycle at an advanced phase, up to 9 hours before dark onset. This phenotype is not significantly correlated with circadian period in constant darkness and is not associated with disruption of molecular circadian rhythms in the SCN, as assessed by analysis of period gene expression. We have identified a genomic region that regulates this phenotype-a major quantitative trait locus on chromosome 18 (near D18Mit184) that we have named era1 for Early Runner Activity locus one. Phase delays caused by light exposure early in the subjective night were of smaller magnitude in backcross offspring that were homozygous Cast/Ei at D18Mit184 than in those that were heterozygous at this locus. CONCLUSION: Genetic variability in the circadian response to light may, in part, explain the variance in phase angle of entrainment in this segregating mouse population.     

Human circadian rhythms and exercise

Many biological functions change cyclically over a 24-h period, such cycles being referred to as circadian rhythms. The major rhythms of relevance to examine performance are those of body temperature and the sleep-wake cycle. Many components of exercise performance are closely related to the body temperature curve which peaks in the early evening. Exercise with predominantly neuromotor and cognitive components depend also on the underlying sleep-wake cycle. Some performance measures are subject to ultradian cycles and show a transient decline in the early afternoon. Optimal time of day for exercise is determined not just by endogenous rhythms but also by the nature and intensity of exercise, the population concerned, environmental conditions, and individual phase types. Environmental factors impinging on circadian rhythms include light, heat, air ionization, activity and eating patterns, and social activities. Endogenous rhythms are desynchronized when perturbed by nocturnal shift work or time-zone transitions. Coping with desynchronosis involves behavioral, dietary, or pharmacological treatments. Sleep loss interacts with circadian rhythmicity but affects cognitive function more so than gross motor actions. The existence of self-sustaining rhythms should be recognized by athletic practitioners, sports scientists concerned with experimental work and fitness testing, sports injury specialists, and sports organizers concerned with the travel plans of athletes.