Photoperiod time measurement for activity, torpor, molt and reproduction in mice

Resonance light:dark cycles (LD 6:18, 6:30, 6:42, or 6:54) were used to establish that a circadian rhythm of light sensitivity is involved in the thermoregulatory and reproductive responses to a short day photoperiod in the mouse, Peromyscus leucopus. A fifth group was maintained on the long day photoperiod of LD 16:8. After 19 weeks animals presented with LD 6:18 or 6:42 exhibited short day photoperiod responses: gonadal regression, incidence of spontaneous daily torpor and molt to the winter pelage. In contrast animals responded to LD 6:30 and 6:54 as long day photoperiods: maintenance of gonadal system, no incidence of spontaneous daily torpor, and summer pelage. In a second study a T-experiment was conducted to determine that more than one circadian system may regulate these multiple photoperiodic effects. Mice were exposed to 1 of 8 LD cycles for 15 weeks (1:22.00, 1:22.25, 1:22.50, 1:23.00, 1:23.50, 1:23.75, 9:15, or 16:8), Entrained wheel-running activity occurred under all LD regimes. Mice on LD 1:22.50, 1:23.00, and 1:23.50, however, exhibited activity patterns similar to mice on LD 9:15, and they exhibited gonadal regression. Mice on LD 1:22.00, 1:22.25, and 1:23.75 exhibited activity patterns similar to LD 16:8 animals, and most of these animals remained reproductively competent. There was also a close association between occurrence of reproductive regression and daily torpor. In contrast, molt to the winter pelt occurred under all non-24-hr LD cycles. This dysynchrony in response suggests that at least 2 circadian systems are involved in photoperiodic time measurement in P. leucopus.     

Comparison of pineal melatonin rhythms in young adult and old Djungarian hamsters (Phodopus sungorus) under long and short photoperiods

The pattern of the pineal melatonin rhythm was studied in 3-6- and 17-22-month-old female Djungarian hamsters under light-dark (LD) schedules, LD 16:8 and LD 8:16. Under both photoperiods, the amplitude of the melatonin rhythm was 2.5 times higher in young adult hamsters than in old ones. Two weeks after the change from LD 16:8 to LD 8:16, the period of elevated nocturnal melatonin levels lengthened by about 3 h in both age groups. It is suggested that old Djungarian hamsters, as well as young adults, might be able to recognize the length of a photoperiod and its change.     

Effect of a short photoperiod on circadian rhythms of body temperature and motor activity in old rats

Circadian rhythms of body temperature and motor activity were documented in young and old rats (four 8-week-old and five 22-month-old male Wistars, implanted with telemetric probes and housed in a chronobiological facility) under two different photoperiod conditions. The animals were maintained in a light:dark (LD) cycle of 12 h each (LD 12:12) for 4 weeks and then exposed to a LD 6:18 cycle for 7 weeks to assess the effect of age on the desynchronization of the temporal structure of the rhythms. In old rats under LD 12:12, the power of the 24-h component and the circadian amplitude of body temperature and motor activity were markedly lower than in the young and both rhythms were phase-advanced. After the shift to LD 6:18, the circadian rhythmicity was maintained for both variables and the same phase delay (+5+/-1 h) was observed in both age groups, as was a gradual expansion of the patterns of both functions with the longer night. The photoperiod reduction (6 weeks under LD 6:18) did not modify the power of the 24-h component of body temperature and motor activity in old rats. In young rats, however, the power and amplitude of the 24-h component of motor activity rhythm fell to the levels of those in old rats, while the power of the 24-h component of body temperature rhythm and the amplitude did not change. Our data show that the circadian rhythm of motor activity, but not of body temperature, responds age dependently to a photoperiod reduction.     

Direct and circadian control of sparrow behavior by light and dark

House sparrows, Passer domesticus, have perch-hopping activity (1) which was elicited by light (direct), and (2) which exhibited daily rhythms that were entrained by environmental light-dark cycles (circadian). When photoperiod was more than 14 hr, the sparrows' activity coincided with the light; when it was less than 14 hr, the birds were also active in the dark according to circadian predictions. Bimodality was dependent on photoperiod with the maximum incidence (75%) in LD16:8. Sparrows placed in LD1:11 (skeleton of 13:11) synchronized the onsets of their activity with the light beginning 8-18 hr after the time of the last L/D irrespective of when the birds experienced the first 1 hr light. Thirty-five percent of the sparrows advanced when they entrained to LD1:11 with the first pulse 8 hr after the last L/D; 76-87% of the sparrows delayed when they entrained to LD1:11 with the first pulse 2, 5 or 18 after the last L/D. Sparrows kept in exotic light-dark cycles (with periods of 10 min, 1.5 hr, 3.0 hr, 6.0 hr, 12 hr) were active in the light. Some birds displayed circadian rhythms superimposed on short period patterns. The period lengths of the circadian rhythms were shorter (22.8 hr) than in constant dark (24.2 hr). When sparrows subjected to LD1.5:1.5 or 36 hr of constant light were placed in constant dark, the phase of their activity onsets extrapolated to 15 hr after the last lights-off.     

Sparrow circadian rhythm responses to rotated light-dark schedules

House sparrows, Passer domesticus, were individually subjected to light-dark regimens while their perching activity was continuously monitored. The sparrows resynchronized in 5 days when LD8:16 (8 hr of light alternating with 16 hr of dark) was advanced by 8 hr; however, the sparrows were 1.7 hr from resynchronization after 5 days when the schedule was delayed 8 hr. Sparrows subjected to two simultaneously presented light-dark schedules (rotated LD8:16 provided by one light source imposed together with LD12:12 provided by a second light source) did not ignore either cycle; instead the sparrows responded as to a sequence of photoperiods; they resynchronized the onsets of their activity with the first time of lights-on of the collective photoperiod provided by the two light sources.     

Resetting of the rat circadian clock after a shift in the light/dark cycle depends on the photoperiod.

Adjustment of the circadian clock to shifts in the light/dark (LD) cycle was assessed from the rat pineal N-acetyltransferase (NAT) rhythm which is controlled by a pacemaker in the suprachiasmatic nucleus of the hypothalamus. Re-entrainment to an 8-h delay in the LD cycle took more than 3 days in rats maintained under a regime with 18 h of light and 6 h of darkness per day (LD 18:6) whereas it was completed within 3 days in those maintained under LD 12:12. Re-entrainment to an advance in the LD cycle proceeded through a transient diminution or almost disappearance of the NAT rhythm amplitude following a 5-h, 3-h and even a mere 2-h advance shift under LD 18:6, whereas no such diminution occurred under LD 12:12 even after a 5-h advance shift. Altogether, the data indicate that resetting of the circadian clock after shifts in the LD cycle depends on the photoperiod.     

Circadian rhythms in house sparrows: lighting ad lib

House sparrows, Passer domesticus, have circadian rhythms of locomotor activity that can be entrained by light-dark cycles. Perch-hopping activity was studied in house sparrows that were given control of their own lighting. In one series of experiments, sparrows permitted to select their own lighting most commonly chose circadian freerunning cycles. The period of the selected freerunning cycles was 23.2 hr (0.9 hr shorter than the period length the sparrows exhibited in constant dark). The average self-imposed "photoperiods" in the selected freerunning cycles ranged from 8.2-10.0 hr. In a second series of experiments, sparrows were exposed to LDLD1:6:1:16. This cycle can be interpreted ambiguously as the skeleton of a short photoperiod, LD8:16, or of a long photoperiod, LD18:6. All the birds (13 birds; 23 trials) interpreted the skeleton cycle as a short photoperiod because they entrained to it as they would to LD8:16.     

Effect of reproductive state on circadian periodicity in the rat

The circadian activity rhythms of adult female rats maintained under a light-dark cycle of 14 hr light, 10 hr dark (LD 14:10) or constant dim illumination (dim LL) were recorded during their 4 or 5 day estrous activity cycles and when they were pseudopregnant. In LD 14:10 both the phase angle difference (ψ), which defines the temporal relationship between the onsets of activity and darkness, and the period (τ) of locomotor activity differed significantly among the days of the 4 and 5 day estrous cycle. Activity-time (α) varied reliably only over the days of the 5 day estrous cycle. The period of the free-running activity rhythm in dim LL also differed significantly among the days of the estrous cycle. In both LD and dim LL the most positive ψ, shortest τ and longest α were observed on the day of estrus. Pseudopregnancy diminished the amplitude and altered the daily pattern of the estrous activity rhythm. We conclude that the periodicity of circadian activity systematically varies as a function of the stage of the estrous cycle and in a manner that cannot be solely explained by corresponding alterations in endogenous estrogen.     

Strain differences of the mouse''s free-running circadian rhythm in continuous darkness

The circadian rhythms for 80 days of continuous darkness (DD) were examined after they were released from a LD 12:12 photoperiod. Two inbred strains of mice, DDK and C57BL/10Sn, were selected on the basis of the results of the preliminary study. The rhythms of DDK strain were unstable, while those of C57BL/10Sn were stable over 80 days of DD. In DDK strain, two patterns of rhythm were observed during the experimental period. One was characterized by larger amount of activity, clear onsets of activity, and distinct difference between activity and rest time. The other exhibited the opposite characteristics that included smaller amount of activity, blurred onsets and ends of activity, and expanded activity time. Moreover, the circadian period of the rhythm which showed clear onsets of activity was undoubtedly shorter than the other one within the same individual. In the rhythms of C57BL/10Sn, on the other hand, the features of clear onsets, larger amount of activity, distinct difference between activity and rest time were observed throughout the experimental period. These results suggest that one basic factor which affects the circadian rhythm is genetic.     

Control of behavioral circadian rhythms for nesting and wheel running in mice

In Experiment 1 a circadian rhythm for nest-building behavior is demonstrated in 10 males from a genetically heterogeneous stock of Mus musculus. In Experiment 2, this circadian rhythm in nesting and that for wheel running activity were monitored simultaneously in an additional sample of five males from the same stock. Under a 16:8 LD photoperiod, mice displayed a 24-hr periodicity for both behaviors but a phase difference in peak behavioral intensities of approximately two and one-half hours. After ten days of exposure to constant light both rhythms persisted, but with no detectable difference in phase. The altered phase relationship under constant light suggests a difference in control of the circadian periodicities of these two behaviors. In Experiment 3, 5 additional males were subjected to a 10-hr shift in photoperiod to further examine control of these rhythms as well as those in food and water consumption. All four circadian rhythms re-entrained within four days. Thus, their entrainment mechanisms are functionally similar in spite of the differences in control suggested in Experiment 2.     

Circadian entrainment of the squirrel monkey by extreme photoperiods: Interactions between the phasic and tonic effects of light

To examine the role that the phasic and tonic aspects of the light-dark (LD) cycle play in entraining the circadian timing system of primates, squirrel monkeys (Saimiri sciureus) were exposed to 24 hr LD cycles in which the light duration (photoperiod) was varied from 1 sec to 23 hr. The monkeys were maintained in isolation and the circadian rhythm of drinking was monitored. The photoperiod was first gradually shortened until constant darkness was reached. Even in extremely short photoperiods of only one second of light per day, the drinking rhythm remained synchronized to the 24 hr period of the LD cycle. In the second set of experiments, the photoperiod was gradually lengthened until constant light was achieved. The drinking rhythm of all monkeys was synchronized by 21 hr photoperiods (LD 21:3), but free-ran in 23 hr photoperiods (LD 23:1) which provided a 1 hr dark pulse each day. The tonic effects of light may contribute to the difference between the ability to entrain to short versus long photoperiods. In constant darkness the free-running period was close to 24 hr, thus reducing the phase-resetting necessary to achieve entrainment to a 24 hr period by short light pulses. However, in constant light or in the long photoperiods which did not entrain (LD 23:1) the free-running period of the drinking rhythm was greater than 25 hr, thus requiring a much larger daily phase shift to achieve entrainment to a 24 hr period.     

Annual rhythm and hormonal control of predatory behavior in female ferrets

The predatory behavior of female ferrets shows seasonal fluctuations which appear to be affected by estradiol. Under natural lighting conditions in the laboratory the annual rhythm of the behavior was observed during anestrus, estrus, pregnancy, pseudopregnancy and lactating period. Females in heat failed to show predatory behavior whereas females in anestrus killed their prey. Exposure of anestrous ferrets to a prolonged illumination (LD 16:8) during winter induced an estrus which inhibited predatory behavior. When estrus was terminated with human chorionic gonadotropin (HCG), predatory behavior did not further regress as it did in control runs. Thus, during the period of estrus, when estrogen levels are presumably high, predatory behavior was inhibited. To prove a possible interdependency of estrogen and predatory behavior, estradiol-17 beta-valerat was chronically administered. This treatment induced the estrous cycle one day after the first injection. Inhibition of predatory behavior occurred following a delay of 28 days. Thus, fluctuations of estradiol levels are a factor which may affect fluctuations of predatory behavior in female ferrets.     

Photoperiod and body weight in female Syrian hamsters: skeleton photoperiods, response magnitude, and development of photorefractoriness

Two experiments examined the effects of various photoperiods on body weight and reproductive function in Syrian hamsters (Mesocricetus auratus). In Experiment 1 female hamsters were exposed to symmetrical skeleton photoperiods in which dawn and dusk were mimicked by 1-hr light pulses. A skeleton long (LD 16:8) photoperiod had no effect on body weight or estrous cyclicity (compared with animals in a complete LD 16:8 photoperiod), but exposure to a skeleton short (LD 10:14) photoperiod increased body weight and interrupted estrous cycles. Thus, body weight appears to respond to the relative timing of the two light pulses (a circadian mechanism) rather than to the absolute amount of light or darkness (an hourglass mechanism), just as does reproduction. In Experiment 2 female hamsters were exposed to a long photoperiod (LD 16:8) or to one of two short photoperiods (LD 10:14 and LD 8:16). Both short photoperiods increased body weight and interrupted estrous cycles, but the LD 8:16 photoperiod was substantially more effective at increasing body weight than was the LD 10:14. Thus, hamster body weight appears to be capable of a graded response to photoperiod, with shorter days producing a greater obesity. With prolonged exposure to the two short photoperiods (greater than 30 weeks), body weights spontaneously returned to the same level as the long-day controls, and estrous cycles resumed. When these hamsters were treated with the pineal gland hormone, melatonin, only those housed in long days exhibited the characteristic body weight gains, growth of brown and white adipose tissues, and decreases in uterine weight. Therefore, with prolonged exposure to short days, energy balance develops a photorefractoriness and an insensitivity to melatonin treatment, just as with reproductive function.     

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.     

Robust circadian rhythm in heart rate and its variability: influence of exogenous melatonin and photoperiod

Heart rate (HR) and heart rate variability (HRV) undergo marked fluctuations over the 24-h day. Although controversial, this 24-h rhythm is thought to be driven by the sleep-wake/rest-activity cycle as well as by endogenous circadian rhythmicity. We quantified the endogenous circadian rhythm of HR and HRV and investigated whether this rhythm can be shifted by repeated melatonin administration while exposed to an altered photoperiod. Eight healthy males (age 24.4 +/- 4.4 years) participated in a double-blind cross-over design study. In both conditions, volunteers were scheduled to 16 h-8 h rest : wake and dark : light cycles for nine consecutive days preceded and followed by 29-h constant routines (CR) for assessment of endogenous circadian rhythmicity. Melatonin (1.5 mg) or placebo was administered at the beginning of the extended sleep opportunities. For all polysomnographically verified wakefulness periods of the CR, we calculated the high- (HF) and low- (LF) frequency bands of the power spectrum of the R-R interval, the standard deviation of the normal-to-normal (NN) intervals (SDNN) and the square root of the mean-squared difference of successive NN intervals (rMSSD). HR and HRV variables revealed robust endogenous circadian rhythms with fitted maxima, respectively, in the afternoon (16:36 hours) and in the early morning (between 05:00 and 06:59 hours). Melatonin treatment phase-advanced HR, HF, SDNN and rMSSD, and these shifts were significantly greater than after placebo treatment. We conclude that endogenous circadian rhythmicity influences autonomic control of HR and that the timing of these endogenous rhythms can be altered by extended sleep/rest episodes and associated changes in photoperiod as well as by melatonin treatment.     

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.     

Bird eyes distinguish summer from winter: Retinal response to acute photoperiod change in the night-migratory redheaded bunting

Eyes are the part of the circadian timekeeping system but not involved in the photoperiod regulated seasonal physiology in songbirds. Here, two experiments tested whether eyes detect and respond to seasonal change in the photoperiod environment, by examining gene and protein expressions in the retinas of redheaded buntings exposed to a single long day (LD, 16L:8D), with controls on short days (SD, 8L:16D). In the first experiment, mRNA expression of genes implicated in the light perception (opsins, rhodopsin, neuropsin, melanopsin, peropsin) and photoperiod induction (eya3, tsh-β, dio2, dio3) was measured at hours 15 and 19 (hour 0 = light on) on the first long day. There was a significant increase in the eya3, tsh-β and dio2 mRNA expression, albeit with a temporal difference, and decrease in the neuropsin mRNA expression in buntings on the first long day. There was no change in the dio3, rhodopsin, melanopsin and peropsin mRNA expressions on exposure to long days. The second experiment immunohistochemically examined the eya3, tsh-β and rhodopsin peptide expressions. eya3 was expressed in both light conditions, but with a significant higher levels in the retinal photoreceptor layer (PRL) under LD, as compared to SD. Similarly, tsh-β was expressed in the PRL of LD retinas only. Rhodopsin levels were not significantly different between SD and LD conditions, however. These results for the first time show photoperiod-dependent molecular switches in the bunting retina, similar to the well documented thyroid hormone response genes based molecular cascades in the avian hypothalamus.     

The interaction of photoperiod and testosterone on the development of copulatory behavior in castrated male hamsters

Castrated adult male golden hamsters were maintained on either a stimulatory (LD 14:10) or a nonstimulatory (LD 6:18) light cycle for 10 weeks, and then were implanted subcutaneously with empty or testosterone-filled Silastic capsules of various lengths. Animals were tested for copulatory behavior prior to capsule implantation and 10, 20 and 40 days after implantation. Androgen-treated LD 14:10 hamsters showed a higher incidence of ejaculation on the final trial than did similarly treated LD 6:18 animals. When serum androgen levels were maintained at physiological levels (about 3 ng/ml, from a 20 mm capsule), significantly greater numbers of LD 14:10 hamsters intromitted and ejaculated compared to LD 6:18 animals. Examination of the development of copulation over trials revealed an interaction of photoperiod and androgen: LD 14:10 animals showed significant improvement over trials if stimulated with 8,20 or 100 mm long testosterone capsules, while LD 6:18 animals showed increased copulation over trials only if they were implanted with 100 mm capsules. These results indicate that exposure to short days for 10 weeks renders copulatory behavior of the castrate male hamster less responsive to the stimulatory effects of testosterone. This alteration in sensitivity to androgen may be one way in which the photoperiod acts to decrease copulation in seasonally breeding animals.     

Effects of photoperiod and 6-methoxy-2-benzoxazolinone on male-induced estrus in prairie voles

Prairie voles (Microtus ochrogaster) are characterized as facultative breeders with higher rates of reproductive activities observed during spring and summer than autumn and winter. The environmental factors regulating seasonal breeding in this species remain unspecified. Short day lengths inhibit reproductive organ development in male prairie voles in the laboratory, but these males remain fertile and capable of siring offspring; female prairie voles have been reported to be reproductively unresponsive to day length in the laboratory. The organization of estrus in this species is unusual in that females never display the cyclic changes associated with estrus; rather, female prairie voles require chemosensory stimuli associated with fertile males in order to be induced into estrus. The plant compound, 6-methoxy-2-benzoxazolinone (6-MBOA), is present in vegetatively growing grasses and sedges and acts to trigger reproduction in other rodent species exposed to short days. It was suspected that 6-MBOA present in the laboratory diet may have overridden the effects of photoperiod on female prairie voles in previous laboratory studies. In the present study, the effects of 6-MBOA and photoperiod on estrus induction were examined. Beginning at Week 0, female prairie voles were housed in long (LD 16:8) or short (LD 8:16) photoperiods for 9 weeks, then implanted subcutaneously either with an empty Silastic capsule or one packed with 6-MBOA. A special diet, devoid of 6-MBOA, was available ad lib from Week 5 to the end of the study.(ABSTRACT TRUNCATED AT 250 WORDS)     

Short photoperiod stimulates brown adipose tissue growth and thermogenesis but not norepinephrine turnover in Syrian hamsters

This experiment examined the effect of short photoperiod on food intake, body weight, carcass composition, and brown adipose tissue (BAT) activity in female Syrian hamsters (Mesocricetus auratus). BAT function was assessed by measuring sympathetic nervous system (SNS) activity in BAT (estimated by the rate of norepinephrine (NE) turnover), BAT mitochondrial content (estimated by cytochrome c oxidase activity), and BAT mitochondrial proton conductance (estimated by guanosine-5'-diphosphate (GDP) binding to isolated BAT mitochondria). Food intake and body weight were both increased in short photoperiod-housed hamsters (8-hr light, 16-hr dark; LD 8:16) when compared to those of the long photoperiod-housed controls (LD 16:8). The weight gain was entirely due to an increase in carcass lipid. Interscapular BAT (IBAT) pads from short photoperiod-housed hamsters were 53% heavier and contained comparably more protein and DNA. Short photoperiod produced a 118% increase in BAT cytochrome c oxidase activity and a 41% increase in specific mitochondrial GDP binding. Whether expressed per mg wet tissue or per pad, neither the endogenous concentration of NE nor its rate of turnover were changed by short photoperiod exposure. These results demonstrate a dissociation of BAT thermogenesis from SNS activity in BAT from short photoperiod-housed Syrian hamsters.