Circadian rhythm of locomotor activity in the four-striped field mouse, Rhabdomys pumilio: a diurnal African rodent

Although humans are diurnal in behaviour, animal models used for the study of circadian rhythms are mainly restricted to nocturnal rodents. This study focussed on the circadian behaviour of a rodent from South Africa that has a preference for daylight, the four-striped field mouse, Rhabdomys pumilio. In order to characterise the behavioural pattern of daily activity, locomotor rhythms were studied under different light regimes using an automated data recording system. Under conditions of natural daylight, which include dawn and dusk transitions, R. pumilio exhibited activity restricted to the daytime period. Activity was concentrated around morning and evening with a decrease during mid-day. A similar diurnal preference pattern of behaviour was recorded under a light-dark cycle of artificial illumination. Under conditions of constant darkness, the four-striped field mouse exhibited a free-running circadian rhythm of locomotor activity with activity concentrated during the subjective day. Free-running rhythms varied greatly between individuals, from slightly less to slightly more than 24 h (range = 23.10 to 24.80 h). Under conditions of constant light, the mice were more active during subjective day, but the free-running rhythm in all individuals was consistently longer than 24 h (range = 24.30 to 24.79 h).     

Circadian rhythms of locomotor activity in the subterranean Mashona mole rat, Cryptomys darlingi

The Mashona mole rat, Cryptomys darlingi, is a social, subterranean African rodent that is rarely, if ever, exposed to light, and that exhibits a regressed visual system. This study investigated locomotor activity patterns of Mashona mole rats (n=12) under different light cycles. Activity was measured using either infrared captors (n=8) or running wheels (n=4). The mole rats entrained their activity to a standard (LD 12:12) photoperiod. They displayed either a nocturnal or diurnal activity preference with one bout of activity and one bout of rest. Therefore, as a species, the Mashona mole rat did not show a clear nocturnal or diurnal activity preference. When the LD (12:12) light cycle was inversed, the animals switched their activity, too. Under constant dark (DD), most mole rats (73%) showed a free-running circadian activity rhythm, but under constant light (LL), only some (36%) did. The free-run period of the rhythm (tau) ranged from 23.83 to 24.10 h. The remaining animals were arrhythmic. There was large interindividual and intraindividual variations in the rate and extent of entrainment, time of activity preference, and activity patterns. Possible reasons for the observed variations are discussed. It is concluded that the Mashona mole rat has an endogenous activity rhythm which approximates 24 h, that the mole rat can distinguish between light and dark, and that the endogenous clock utilises this photic information as a zeitgeber.     

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.     

Two strategies for coping with food shortage in desert golden spiny mice

Desert rodents face periods of food shortage and use different strategies for coping with it, including changes in activity level. Golden spiny mice (Acomys russatus) inhabit rock crevasses and do not dig burrows nor store food. When kept under 50% food restriction most, but not all, golden spiny mice defend their body mass by physiological means. We tested the hypothesis that these rodents use two different behavioral strategies, i.e., increasing activity level and searching for food or decreasing activity level and conserving energy to cope with food shortage. Twelve golden spiny mice were fed ad libitum for 14 days, followed by 40 days of 50% food restriction, and 14 days of refeeding. Body mass, food consumption and general activity were monitored. Seven mice significantly reduced activity level, concentrating their activity around feeding time, lowering energy expenditure and thus keeping their body mass constant ("resistant"), while five ("non-resistant") significantly increased activity level (possibly searching for food) and thus energy expenditure, thereby losing mass rapidly (more than 25% of body mass). The non-resistant golden spiny mice were active throughout many hours of the day, with high variability both between and among individuals. The use of two strategies to cope with food shortage as found in the golden spiny mice may be of evolutionary advantage, since it allows a more flexible reaction to food restriction at the population level.     

Varying responses to the rat forced-swim test under diurnal and nocturnal conditions

The paradox that experiments in behavioural pharmacology employing nocturnal rodent species are carried out almost exclusively in the resting phase of the animals' circadian cycle has remained largely unexamined and unquestioned. This is despite the fact that all major physiological systems in the body are intrinsically aligned with its natural circadian rhythm. The forced-swim test (FST) is a rodent model that is used extensively as a screening test for antidepressant activity. The objectives of the present study were to examine the behaviour of rats in the FST under diurnal and nocturnal conditions and, in addition, to profile the response of neurochemical, neuroendocrine, and cellular indices of stress at time points up to 120 min following exposure to the FST. The time spent in escape-oriented activity was significantly less when animals were tested in the dark phase. The profile of serum corticosterone and adrenal ascorbic acid concentrations indicates that the animals were less stressed by the test situation during the active (i.e., dark) phase of their circadian cycle. Similarly, increases in blood enzymatic markers of stress-induced cellular damage were less marked following FST exposure in the nocturnal period. Characteristic stress-induced increases in 5-HT turnover in the frontal cortex and amygdala observed in the diurnal phase were reversed in the nocturnal period. In conclusion, circadian differences in behaviour in the FST may be related to parallel alterations in the ability of animals to adapt to exposure to stress.     

Role of the pineal gland in circadian organization of diurnal ground squirrels

Golden-mantled ground squirrels, Spermophilus lateralis, pinealectomized (pinx) or sham-pinx at 70 days of age, were maintained in a LD 10:14 photoperiod; phase angles of activity onset were 1.6 +/- 0.3 and 1.9 +/- 0.3 hr in advance of light onset, respectively, and did not differ significantly between the groups. Rates of phase shifting of the activity rhythm after a 6 hr phase advance in the LD cycle also were comparable for the two groups and stable re-entrainment was achieved in 11 days. The period of the free-running activity rhythm in constant light did not differ between the groups. As demonstrated previously in nocturnal rodents, the pineal gland exerts little if any influence on generation or entrainment of the ground squirrel diurnal circadian activity rhythm. The rodent pineal is neither a master circadian oscillator nor a significant component of the transduction process by which light entrains the circadian activity rhythm.     

Enhanced circadian photoresponsiveness after prolonged dark adaptation in seven species of diurnal and nocturnal rodents

Previous studies in mice and Syrian hamsters have described an enhancement of circadian photoresponsiveness after exposure to darkness for several weeks. The present study investigated the generality of the phenomenon in 3 diurnal and 4 nocturnal rodent species. In four of the species tested, phase delays of the running-wheel activity rhythm evoked by 1-h light pulses were several-fold larger after 3 to 4 weeks of exposure to darkness than after a single day. This drastic change in photoresponsiveness has important implications for the understanding of the process of photic entrainment. Differences between species that showed a significant effect of dark adaptation and species that showed no effect were not accounted for by temporal niche (diurnal versus nocturnal) or photic sensitivity (albino versus pigmented). Further research is needed to elucidate the mechanisms responsible for inter-species differences in the occurrence of enhanced photoresponsiveness after dark adaptation and to identify the neural substrates of this phenomenon in species that exhibit it.     

Differences in the suprachiasmatic nucleus and lower subparaventricular zone of diurnal and nocturnal rodents

Diurnal and nocturnal species are profoundly different in terms of the temporal organization of daily rhythms in physiology and behavior. The neural bases for these divergent patterns are at present unknown. Here we examine functional differences in the suprachiasmatic nucleus (SCN) and one of its primary targets in a diurnal rodent, the unstriped Nile grass rat (Arvicanthis niloticus) and in a nocturnal one, the laboratory rat (Rattus norvegicus). Grass rats and laboratory rats were housed in a 12:12 light:dark cycle, and killed at six time points. cFos-immunoreactive rhythms in the SCN of grass rats and laboratory rats were similar to those reported previously, with peaks early in the light phase and troughs in the dark phase. However, cFos-immunoreactivity in the lower subparaventricular zone (LSPV) of grass rats rose sharply 5 h into the dark phase, and remained high through the first hour after light onset, whereas in laboratory rats it peaked 1 h after light onset and was low at all other sampling times. Daily cFos rhythms in both the SCN and the LSPV persisted in grass rats, but not in laboratory rats, after extended periods in constant darkness. In grass rats, the endogenous cFos rhythm in the LSPV, but not the SCN, was present both in calbindin-positive and in calbindin-negative cells. Cells that expressed cFos at night in the region of the LSPV in grass rats were clearly outside of the boundaries of the SCN as delineated by Nissl stain and immunoreactivity for vasopressin and vasoactive intestinal peptide. The LSPV of the grass rat, a region that receives substantial input from the SCN, displays a daily rhythm in cFos expression that differs from that of laboratory rats with respect to its rising phase, the duration of the peak and its dependence on a light/dark cycle. These characteristics may reflect the existence of mechanisms in the LSPV that enable it to modulate efferent SCN signals differently in diurnal and nocturnal species.     

Diurnal rhythms of blood pressure, heart rate, and locomotor activity in adult and old male Wistar rats

The diurnal rhythms of systolic blood pressure (SBP), diastolic BP (DBP), heart rate (HR), and spontaneous locomotor activity (SLA) were determined in adult (6-month-old) and old (24-month-old) male Wistar rats by using radiotelemetry. The rhythm parameters (mesor, amplitude, acrophase, and percent rhythm) were analyzed by Fast-Fourier Transform and Cosinor methods. We found that the 12-h mean values of SBP, DBP, HR, and SLA were significantly (p<0.001) higher in the dark phase than in the light phase in both adult and old rats. The nocturnal 12-h mean value of HR was significantly (p<0.01) lower in old than in adult rats. In addition, the differences between diurnal and nocturnal 12-h mean values of SBP and HR were reduced in old rats. There was no significant difference in the 12-h mean values of SBP, DBP, and SLA between old and adult rats. Otherwise, the diurnal HR rhythm amplitude was significantly (p<0.01) reduced in old rats (32+/-2 vs. 46+/-2 bpm). A nearly 1-h delay in SBP and DBP acrophases (03h55 +/- 00h19 vs. 02h57 +/- 00h14 and 03h17 +/- 00h13 vs. 01h53 +/- 00h22, respectively) was found in old rats comparing to adult rats. No significant change in SLA diurnal rhythm was observed in old rats. In conclusion, these results show a decrease in the nocturnal 12-h mean value of HR and an alteration in cardiovascular diurnal rhythms by a 1-h delay of SBP and DBP acrophases and a reduction of HR rhythm amplitude in old Wistar rats.     

Interaction between the adrenal and the pineal gland in chronic experimental inflammation induced by BCG in mice

OBJECTIVE: To investigate the adrenal gland influence on diurnal rhythm of chronic inflammation induced by BCG in mice and its interaction with the pineal gland. METHODS: C57Bl/6 mice were injected with BCG in the footpad and maintained in a 12/12 h light-dark cycle. All the experimental manipulations were done after 20-45 days. Paw swelling was measured every 4 h for 48 or 72 h and decomposed by Fourier transformation. Vascular permeability was evaluated by Evans Blue overflow, in mice killed at midday or midnight. 6-Sulphatoxymelatonin urine concentration was determined by radioimmunoassay in samples taken during the dark or light phase. RESULTS: Adrenalectomy or metyrapone treatment abolished the paw swelling diurnal rhythm, the nocturnal reduction in vascular permeability, and the nocturnal increase in 6-sulphatoximelatonin in the urine. Nocturnal administration of melatonin to adrenalectomized mice restored the paw swelling diurnal variation and the reduction of vascular permeability of the inflamed paw. CONCLUSION: Adrenal cortical hormones are important for the maintenance of the diurnal rhythm of chronic inflammation (paw swelling and vascular permeability), probably by promoting a nocturnal surge of melatonin, which is the hormone that modulates the diurnal variation of chronic inflammation.     

Circadian rhythms of locomotor activity in the Lesotho mole-rat, Cryptomys hottentotus subspecies from Sani Pass, South Africa

The Lesotho mole-rat is a social subterranean rodent that occurs at altitude in the Drakensberg mountain range. As a consequence of living permanently underground these animals rarely if ever are exposed to light. The visual system of African mole-rats is particularly regressed whereas the circadian system is proportionately conserved. This study investigated the locomotor activity patterns of 12 Lesotho mole-rats maintained under a range of different lighting regimes. The majority (91.7%) of mole-rats entrained their activity patterns to a LD photoperiod of 12L/12D. The mole-rats displayed a monophasic nocturnal activity preference. Under constant dark (DD) most of the mole-rats (83.3%) showed a free running circadian activity pattern with a tau of 23.8 h to 24.4 h (mean+/-S.E.M.: 24.07 h+/-0.07 h; n=10). The phase of the activity rhythms each mole-rat exerted during the previous LD-cycle did not change when the animals started free-running after being placed in constant conditions. The duration of re-entrainment to a second bout of LD 12:12 amounted to 9.4+/-2.03 days (mean+/-S.E.M., n=10). Eleven mole-rats (91.7%) adjusted their locomotor activity rhythms to an inversed light regime DL 12:12 and displayed significant nocturnal activity preference. The animals required 9.73+/-2.01 days (mean+/-S.E.M., n=11) to adjust to the DL-photoperiod. The Lesotho mole-rat thus possesses a functional circadian clock that responds to a photic zeitgeber.     

Response curve, free-running period, and activity time in circadian locomotor rhythm of rats

Phase response curves (PRC) for the spontaneous locomotor rhythm were constructed by applying short light pulses to rats in constant darkness (DD). The offset of locomotor activity as well as the onset was taken as a phase reference (offset PRC vs. onset PRC). The amount of phase shift yielded by light pulses was evaluated on the next day of pulse treatment (immediate PRC) and also after completion of a new steady state (steady state PRC). Significant differences in shape were observed between the onset and offset PRCs as well as between the immediate and steady state PRCs. In the immediate onset PRC, an area under the phase advance part (A) was absent, while it was present in the immediate offset PRC. In contrast, the steady state PRCs for activity onset and offset were essentially the same. The shape of steady state PRC depended on the free-running period in DD (tau). In the PRCs of long tau rhythms, the range covered by the phase delay area (D) was lengthened without changing its amplitude, resulting in a larger D/A ratio. A strong positive correlation was detected between tau and activity time (alpha). The steady state PRC shapes also depended on alpha; the D/A ratio was larger in a long alpha rhythm than in a short alpha. These results are in good agreement with the hypothesis that the circadian locomotor rhythm of nocturnal rodents is regulated by two coupled oscillators.     

Circadian rhythms of activity and drinking in mice lacking angiotensin II 1A receptors.

Angiotensin II (ANG II) type 1 receptors are found in the mouse suprachiasmatic nucleus (SCN), the site of the circadian pacemaker, but their significance for circadian timekeeping is unknown. We examined circadian rhythms of wheel running and drinking in angiotensin AT(1a) receptor knockout (KO) mice. Mean daily running and drinking activity were elevated in KO mice under a light-dark (LD) cycle and in constant dark (DD). These increases were confined to the usual active (dark) period, thus, the 'amplitude' of running and drinking rhythms was higher in KO mice. The phase of entrainment to LD (measured by the onset of the daily active period) did not differ between groups, either in LD or on the first day of DD ('unmasked' phase). KO mice showed a modestly shorter free-running period (tau) in DD. The direction and magnitude of phase shifts to light pulses at two circadian times (CTs) in DD did not differ between groups. Core functions of the circadian system appear intact following AT(1a) receptor KO. The modestly shorter tau and increased rhythm amplitude in KO mice may be secondary to an effect of the mutation on the level of running and drinking activity.     

Locomotor, feeding and melatonin daily rhythms in sharpsnout seabream (Diplodus puntazzo)

Sharpsnout seabream is a marine teleost of increasing interest for Mediterranean aquaculture, but there is still a lack of information regarding its circadian organization. In this study, we have investigated sharpsnout seabream locomotor activity, feeding and plasma melatonin daily rhythms under a 12:12-h LD cycle, as well as the persistence of locomotor activity circadian rhythmicity under constant light (LL) conditions. When submitted to an LD cycle, most sharpsnout seabream displayed a diurnal locomotor pattern, with an average 74% of activity recorded during daytime. However, along the experiment 40% of fish spontaneously changed their locomotor rhythm phasing and became nocturnal. Feeding behaviour, nevertheless, remained strictly diurnal in all cases, with 97% of food demands being made during the light period. Free-running locomotor rhythms were recorded in one third of the fish kept under LL. Daily plasma melatonin levels displayed a rhythmic profile, with low daytime values (111 pg/ml) and high nighttime concentrations (791 pg/ml). Taken together, these results evidence a high degree of plasticity for sharpsnout seabream activity patterns, as well as phasing independence of locomotor and feeding rhythms. Finally, the existence of a well-defined daily rhythm of plasma melatonin was found.     

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.     

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.     

Secretion of DJ-1 into the serum of patients with Parkinson's disease

In the diurnal rodent Arvicanthis niloticus (grass rats) the pattern of expression of the clock genes and their proteins in the suprachiasmatic nucleus (SCN) is very similar to that seen in nocturnal rodents. Rhythms in clock gene expression have been also documented in several forebrain regions outside the SCN in nocturnal Ratus norvegicus (lab rats). To investigate the neural basis for differences in the circadian systems of diurnal and nocturnal mammals, we examined PER1 expression in the oval nucleus of the bed nucleus of the stria terminalis (BNST-OV), and in the basolateral (BLA) and the central (CEA) amygdala of male grass rats kept in a 12:12 light/dark cycle. In the BNST-OV, peak levels of PER1 expression were seen early in the light phase of the cycle, 12h out of phase with what has been reported for nocturnal lab rats. In the BLA the pattern of PER1 expression featured sustained high levels during the day and low levels at night. PER1 expression in the CEA was also at its highest early in the light phase, but the effect of sampling time was not statistically significant (p<0.06). The results are consistent with the hypothesis that differences between nocturnal and diurnal species are due to differences in neural systems downstream from the SCN.     

Effects of methamphetamine upon circadian rhythms in multiple unit activity inside and outside the suprachiasmatic nucleus in the golden hamster (Mesocricetus auratus)

To investigate the circadian system of the golden hamster, multiple unit activity (MUA) was recorded inside and outside the suprachiasmatic nucleus (SCN). MUA inside the SCN showed a daily rhythm with a daytime peak during a 24 h light-dark cycle (LD, 12:12), whereas MUA outside the SCN revealed a nighttime peak. The phase reversal of MUA between inside and outside the SCN in the golden hamster was similar to the rat which is also a nocturnal rodent. MUA rhythms to the lighting cycle started to freerun after methamphetamine administration. This result indicates that methamphetamine may affect directly the neural circadian oscillator to induce behavioral change.     

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.     

Diurnal variation in circulating leptin is dependent on gender, food intake and circulating insulin in mice

Leptin is an adipocyte hormone involved in the regulation of energy homeostasis. Its circulating levels show a diurnal rhythm with a nocturnal peak. We examined the influences of gender, feeding state, and plasma insulin and glucose on the diurnal rhythm in normal mice. Plasma was sampled at 4-h interval for 24 h in female (n=80) and male (n=80) mice, which were freely fed or fasted. In both genders, plasma leptin displayed a diurnal rhythm with a nadir at 8 or 10 AM and a nocturnal peak at 10 PM to 2 AM. The nocturnal increase in leptin was higher in females (+160+/-18%) than in males (61+/- 16%; P<0.001), completely abolished by fasting, and correlated significantly to the diurnal variation in plasma insulin both in females (r=0.44, P=0.003) and males (r=0.46, P<0.001). Baseline plasma leptin in non-fasted animals were not different between the genders, whereas during fasting, the reduction in leptin was more pronounced in males than in females, resulting in a higher plasma leptin after fasting in females. Plasma insulin was higher in males under non-fasted conditions (P=0.003), but not significantly different between genders in fasted animals. In conclusion, plasma leptin displays a nocturnal increase in mice, which is more pronounced in female mice than in male mice, is completely abolished by fasting and correlates to the diurnal variation in circulating insulin. It is suggested that the nocturnal rise in leptin shows gender dependency and is caused by the increase in plasma insulin caused by food intake.