Nonphotic Zeitgebers Research Articles

Non-photic entrainment of human rest-activity cycle independent of circadian pacemaker

Entrainment of rest-activity cycles and plasma melatonin rhythms by a forced schedule was examined in humans who were held in temporal isolation with dim light conditions (<10 lx). The sleep schedule of subjects was phase-advanced by approximately 8 h from the habitual sleep time for 8 days, which was followed by a free-running session where the subjects self-determined the times of sleep and wake up for 6 days. As a result, the rest-activity cycle was advanced by 8.2 h on the first day of free-run after the forced schedule, whereas the circadian melatonin rhythm was not significantly shifted on the last day of the schedule. The findings indicate that the forced sleep schedule of 8 days entrain the rest-activity cycle but not the melatonin rhythm. Under free-running conditions, the rest-activity cycles resynchronized with the melatonin rhythm by either phase-advance or phase-delay shifts. The direction and extent of phase-shift depended on the phase relationship between the rest-activity cycle and plasma melatonin rhythm one cycle before the phase-shift. The findings indicate the existence of an oscillatory coupling between the rest-activity cycle and the plasma melatonin rhythm. It is concluded that non-photic zeitgebers can entrain the rest-activity cycle in humans, which is independent of the circadian pacemaker.

Period and phase adjustments of human circadian rhythms in the real world.

Entrainment of the circadian rhythm has 2 aspects, period and phase adjustments, which are established simultaneously in most nonhuman circadian systems. The human circadian system is unique in its functional structure in which 2 different subsystems are involved; one is the circadian pacemaker analogous to that located in the suprachiasmatic nucleus, and the other is the oscillatory system of unknown nature that drives the rest-activity cycle. The human circadian system shows the endogenous period very close to 24 h under entrainment and less sensitive to photic stimuli than under free running, which may explain stable entrainment in the real word where natural sun lights are unpredictable in terms of the intensity and time of appearance. On the other hand, nonphotic entrainment seems to play a significant role in phase adjustment of the human circadian system. Nonphotic zeitgebers initially directed to the rest-activity cycle may affect the circadian pacemaker through feedback and/or associated LD cycles.

Olfactory cues accelerate reentrainment following phase shifts and entrain free-running rhythms in female Octodon degus (Rodentia).

Social interactions between conspecifics is a type of nonphotic zeitgeber common to several species. In the diurnal rodent Octodon degus, social interactions enhance reentrainment after phase shifts and can act as a weak zeitgeber. Olfactory stimuli appear necessary for these effects since bulbectomy eliminates socially enhanced reentrainment. In Experiment 1, the authors examined whether stimulation of the main olfactory system was sufficient to enhance reentrainment after 6-h phase advances and delays in the adult female O. degus. When test animals received conspecific odor cues during reentrainment, they entrained 39% faster after phase advances (p < 0.05) and 33% faster after phase delays (p < 0.001) than when they did not receive odor cues. Thus, olfactory cues from distant female donors were sufficient to enhance rates of entrainment in female O. degus and provided results equivalent to earlier studies with donors and shifters housed in the cages together. In Experiment 2, the authors examined whether discrete 3-h and 1-h daily pulses of airborne odors from a group of 5 entrained female degus would be sufficient to produce entrainment of wheel-running activity in adult female conspecifics. During the period of exposure to 3-h pulses, 50% (4/8) of the subjects temporarily entrained to a 24-h cycle, while 12.5% (1/8) of the subjects fully entrained. Exposure to 1-h pulses allowed 37.5% (3/8) of the subjects to temporarily entrain and 12.5% (1/8) of the subjects to fully entrain. Duration of entrained episodes was positively correlated with psi, daily onset of activity with respect to the timing of odor exposure (Pearson r = 0.731; p < 0.05), such that animals with the entraining odor pulse beginning during subjective day (psi = 7.8 h, CT 7.8 +/- 1.4) had longer periods of entrainment (22.2 +/- 5.6 days) than animals with the entraining pulse occurring during subjective night (psi = -4.6 h; CT 19.4 +/- 0.9; 5.6 +/- 0.9 days; p < 0.001). In addition, for each animal, the combined duration of all episodes of 24-h entrainment correlated with increased period length (tau) of free-running rhythms (Pearson r = 0.733; p < 0.05). Thus, daily discrete pulses of odors with durations of either 1 or 3 h from female conspecifics were sufficient to produce both temporary and full entrainment to a 24-h cycle in the majority of female O. degus, and the likelihood of long periods of entrainment correlated with long taus and coordination of the odor pulse with mid subjective day.

Vasopressin deficiency provides evidence for separate circadian oscillators of activity and temperature

Vasopressin-containing Long–Evans and vasopressin-deficient Brattleboro rats were maintained in individual cages while telemetered activity (AC) and body temperature (BT) data were collected. Rats were initially exposed to a 12 h/12-h light/dark cycle (photic zeitgeber) and were allowed ad-libitum access to food and water. Daily feeding, care, and handling (nonphotic zeitgebers) occurred at the beginning of the second hour of the dark cycle. After a 14-day habituation period, rats were subjected to continuous light (LL) or dark (DD) and nonphotic cues were presented irregularly. During the habituation period, both strains exhibited clear 24-h circadian rhythms of AC and BT. In LL or DD, photic cues were removed and nonphotic cues were presented irregularly. There was a shift in the rhythm for Long–Evans animals to 26 h for both AC and BT in LL and 24.6 h in DD. Feeding, care, and handling were seen as minor artifact. In Brattleboro rats, although there were robust 26-h and 24.6-h circadian rhythms of AC in the LL and DD, respectively, BT data were inconsistent and showed sporadic fluctuations. In the BT rhythm of Brattleboro animals, strong peaks were associated with feeding, care, and handling times and trough periods were characterized by a dramatic drop in temperature. This experiment demonstrates that AC and BT are controlled by separate oscillators. In addition, the importance of vasopressinergic fibers in the control of circadian rhythms of BT is evidenced by the loss of circadian rhythms in animals lacking these functional fibers when exposed to free-running paradigms where there is no entrainment of photic or nonphotic oscillators.

Exogenous Melatonin Reduces the Resynchronization Time after Phase Shifts of a Nonphotic Zeitgeber in the House Sparrow (Passer domesticus)

Continuous melatonin administration via silastic implants accelerates the resynchronization of the circadian locomotor activity rhythm in house sparrows (Passer domesticus) after exposure to phase shifts of a weak light-dark cycle. Constant melatonin might induce this effect either by increasing the sensitivity of the visual system to a light zeitgeber or by reducing the degree of self-sustainment of the circadian pacemaker. To distinguish between these two possible mechanisms, two groups of house sparrows, one carrying melatonin implants and the other empty implants, were kept in constant dim light and subjected to advance and delay shifts of a 12-h feeding phase. The resynchronization times of their circadian feeding rhythm following the phase shifts were significantly shorter when the birds carried melatonin implants than when they carried empty implants. In a second experiment, melatonin-implanted and control birds were released into food ad libitum conditions 2 days after either a delay or an advance phase shift. The number of hours by which the activity rhythms had been shifted on the second day in food ad libitum conditions was assessed. Melatonin-implanted house sparrows had significantly larger phase shifts in their circadian feeding rhythm than control birds. This is in accordance with the first experiment since a larger phase shift at a given time reflects accelerated resynchronization. Additionally, the second experiment also excludes any possible masking effects of the nonphotic zeitgeber. In conclusion, constant melatonin accelerates resynchronization even after phase shifts of a nonphotic zeitgeber, indicating that constant high levels of melatonin can reduce the degree of self-sustainment of the circadian pacemaker independent of any effects on the photoreceptive system.

Suprachiasmatic nucleus and intergeniculate leaflet in the diurnal rodent Octodon degus: retinal projections and immunocytochemical characterization

The neural connections and neurotransmitter content of the suprachiasmatic nucleus and intergeniculate leaflet have been characterized thoroughly in only a few mammalian species, primarily nocturnal rodents. Few data are available about the neural circadian timing system in diurnal mammals, particularly those for which the formal characteristics of circadian rhythms have been investigated. This paper describes the circadian timing system in the diurnal rodent Octodon degus, a species that manifests robust circadian responses to photic and non-photic (social) zeitgebers. Specifically, this report details: (i) the distribution of six neurotransmitters commonly found in the suprachiasmatic nucleus and intergeniculate leaflet; (ii) the retinohypothalamic tract; (iii) the geniculohypothalamic tract; and (iv) retinogeniculate projections in O. degus. Using immunocytochemistry, neuropeptide Y-immunoreactive, serotonin-immunoreactive and [Met]enkephalin-immunoreactive fibers and terminals were detected in and around the suprachiasmatic nucleus; vasopressin-immunoreactive cell bodies were found in the dorsomedial and ventral suprachiasmatic nucleus; vasoactive intestinal polypeptide-immunoreactive cell bodies were located in the ventral suprachiasmatic nucleus; [Met]enkephalin-immunoreactive cells were located sparsely throughout the suprachiasmatic nucleus; and substance P-immunoreactive fibers and terminals were detected in the rostral suprachiasmatic nucleus and surrounding the nucleus throughout its rostrocaudal dimension. Neuropeptide Y-immunoreactive and [Met]enkephalin-immunoreactive cells were identified in the intergeniculate leaflet and ventral lateral geniculate nucleus, as were neuropeptide Y-immunoreactive, [Met]enkephalin-immunoreactive, serotonin-immunoreactive and substance P-immunoreactive fibers and terminals. The retinohypothalamic tract innervated both suprachiasmatic nuclei equally; in contrast, retinal innervation to the lateral geniculate nucleus, including the intergeniculate leaflet, was almost exclusively contralateral. Bilateral electrolytic lesions that destroyed the intergeniculate leaflet depleted the suprachiasmatic nucleus of virtually all neuropeptide Y- and [Met]enkephalin-stained fibers and terminals, whereas unilateral lesions reduced fiber and terminal staining by approximately half. Thus, [Met]enkephalin-immunoreactive and neuropeptide Y-immunoreactive cells project equally and bilaterally from the intergeniculate leaflet to the suprachiasmatic nucleus via the geniculohypothalamic tract in degus. This is the first report examining the neural circadian system in a diurnal rodent for which formal circadian properties have been described. The data indicate that the neural organization of the circadian timing system in degus resembles that of the most commonly studied nocturnal rodents, golden hamsters and rats. Armed with such data, one can ascertain differences in the functional organization of the circadian system between diurnal and nocturnal mammals.

Nonphotic Entrainment of Activity and Temperature Rhythms in Anophthalmic Mice

Although it is more common to study the effects of light on circadian systems, nonphotic stimuli can also influence and entrain circadian clocks. Because anophthalmic mice (ZRDCT-AN) have a genetic mutation that prevents the development of the eyes, they do not respond to light or entrain to light–dark cycles. Thus, entrainment of anophthalmic mice requires a nonphotic zeitgeber (entraining stimulus). In the current study we attempted to entrain sighted and anophthalmic mice of the same strain, using restricted access to an unlocked running wheel as the zeitgeber. First, free-running rhythms were established. The running wheels were then locked, and unlocked only from 0930–1130 h each day. Finally, a postentrainment free run was measured. In one group of animals, body temperature and general activity were measured using a Minimitter telemetry system. In another, general activity was measured by a sensitive force plate beneath the cage. Running-wheel activity was recorded in both groups. The force plate proved satisfactory for observing the behavior of the circadian system during wheel locking, and preferable to the temperature transmitters for long-term studies because the battery life of the mouse temperature transmitters was limited. Both sighted and anophthalmic mice were able to entrain to restricted wheel access, although not all animals responded. Mice that did not entrain showed either no effect of wheel locking or exhibited masking.

Removal of the olfactory bulbs delays photic reentrainment of circadian activity rhythms and modifies the reproductive axis in male Octodon degus

The diurnal rodent, Octodon degus, exhibits robust sex differences in several circadian measures, including circadian period ( τ) and reentrainment rates to photic and nonphotic (social) zeitgebers. The neural substrates underlying such physiological differences remain unknown. In female degus, olfactory bulbectomies (BX) inhibit socially-facilitated reentrainment, but do not alter photic reentrainment, entrained measures, or τ in constant darkness (DD). This experiment investigated the effects of BX in male degus on (i) photic reentrainment rates of circadian rhythms following a 6-h phase advance of the light–dark (LD) cycle; (ii) photic entrainment; (iii) τ of free-running activity rhythms in DD; and (iv) body weight, paired testis weight, and the reproductive hormones, testosterone, androstenedione and follicle stimulating hormone (FSH). BX significantly delayed photic reentrainment rates. They did not, however, modify τ, the phase of activity onset or offset, amplitude or duration ( α) of the activity rhythm, mean daily locomotor activity levels, or body weight. FSH, testosterone and androstenedione were unaffected by BX, whereas paired testis weights were significantly greater in BX degus compared with shams. Thus, the olfactory bulbs influence photic reentrainment of circadian rhythms and modestly affect the reproductive axis in male degus. Our results suggest that the olfactory bulbs may be a neural source of observed sex differences in photic reentrainment in degus, and highlight interspecies variation in the olfactory bulbs' effects on entrained and free-running circadian rhythms and on reproduction.

Anticipation and entrainment to feeding time in intact and SCN-ablated C57BL/6j mice

To characterize properties and mechanisms of non-photic entrainment of circadian rhythms, the effects of scheduled feeding were assessed in intact and suprachiasmatic nuclei (SCN) ablated C57BL/6j mice. During ad libitum food access, mice with no or partial SCN damage exhibited free-running activity and drinking rhythms, whereas mice with complete ablations were arrhythmic. When food was restricted to 4 h/day for 5–9 weeks, intact and partial SCN-ablated mice exhibited anticipatory activity to mealtime, concurrent with free-running rhythms. In some cases, free-running rhythms became entrained to feeding time; this was more prevalent in intact than partial ablated mice and was related to free-running period. Free-running phase or period were modified in other cases, revealing a phase–response profile consistent with other non-photic zeitgebers. Five of 12 mice with complete or near complete SCN ablations showed anticipatory activity. Mice that failed to anticipate were less active generally and sustained larger lesions. Sites of damage unique to non-anticipators were not evident. The results indicate that the SCN is not necessary for anticipatory rhythms in mice, but that cell populations distributed across several hypothalamic areas may be important for at least some behavioral markers of this circadian function.

Exercise and Human Circadian Rhythms: What we Know and What we Need to Know

A synopsis of the effects of exercise on the circadian system in nocturnal rodents is followed by a review of the few studies investigating the influence of exercise on the human circadian system. It is premature to make specific recommendations about using exercise to promote synchronization in people because of the lack of information on the best times of exercise, the amounts required, and interactions between nonphotic and photic zeitgebers. (Chronobiology International, 14(2), 221–229, 1997)

Nonphotic phase-shifting and the motivation to run: cold exposure reexamined.

Circadian rhythms in rodents can be phase shifted by appropriately timed activity. This may be dependent on motivational context; running induced by a novel wheel is effective, whereas running induced by cold has been inferred to be ineffective. This issue was reexamined using a different cold exposure procedure. On the first day of constant dark, 6 h before usual dark onset, Syrian hamsters were exposed to cold (+/- 4 degrees C) in their home cages, or were confined to novel wheels for 3 h. Activity rhythms were significantly phase advanced by 92 +/- 10 min following cold exposure and 86 +/- 17 min following novel wheel running, compared to 13 +/- 18 min in a control condition. Most hamsters exhibited eating, drinking, and modest levels of wheel running (1367 +/- 292 counts/6 h) during and for 3 h after cold exposure. Phase shifts following cold were not affected by food and water deprivation but were significantly attenuated by locking the wheel for 6 h beginning at cold onset (24 +/- 12 min). These data indicate that cold-induced running, even at modest levels, is an effective nonphotic Zeitgeber and do not provide support for a hypothesis that motivational contexts determine the phase-shifting value of physical activity.

Entrainment and phase shifting of circadian rhythms in mice by forced treadmill running

Daily schedules of spontaneous, drug-, or novelty-induced running can entrain circadian rhythms in rodents. Forced running, by contrast, has been reported to have weak or no effects, although a thorough comparative study in a single species is lacking. To fill this gap, drinking or activity rhythms were monitored in C57 mice subjected to daily, 3-h bouts of forced treadmill running or to 3-h daily access to home cage running wheels. Entrainment to treadmill running was observed in 17/27 mice, and to restricted wheel access in 11/20 mice. Entrainment was affected by availability of a home cage wheel (e.g., 14/16 mice with no wheel entrained to treadmill running). Phase angle of entrainment was related to prior circadian period (τ), and τ following entrainment exhibited aftereffects. No mice entrained to a 3-h daily schedule of water access, suggesting that entrainment to scheduled running was not related to water or associated food intake. Phase shifts in response to single 3-h bouts of treadmill running or wheel access were small and not reliably induced. The entrainment paradigm is thus recommended for further study of behavioral effects on the mouse circadian system; forced running, in particular, offers several methodological advantages. The results do not support prior suggestions that forced and voluntary activity differ in value as nonphotic zeitgebers.

Locomotor activity and non-photic influences on circadian clocks.

Some of the main themes in this review are as follows. 1. The notion that non-photic zeitgebers are weak needs re-examining. Phase-shifts to some non-photic manipulations can be as large as those to light pulses. 2. As well as being able to phase-shift and entrain free-running rhythms, non-photic events have a number of other effects: these include after-effects of entrainment, period changes, and promotion of splitting. 3. The critical variable for non-photic shifting is unknown. Locomotor activity is more likely to be an index of some other necessary state rather than being causal itself. This index may be better when tendencies to move are channelled into easily measured behaviours like wheel-running. 4. Given ignorance about the critical variable, quantification of activity may be the best presently available measure of zeitgeber intensity. Therefore, the behaviour during non-photic manipulations must be examined as carefully as the shifts themselves. When no phase-shifting follows manipulations such as IGL lesions or serotonin depletion, if the animals are inactive, then little can be inferred. 5. Lack of information on the critical variable(s) for non-photic shifting makes it problematic to compare data from studies using different non-photic manipulations. However, the presence of locomotor activity (or its correlate) does appear to be necessary for triazolam to produce shifts. 6. Novelty-induced wheel-running in hamsters depends on the NPY projection from the IGL to SCN. It remains to be determined how important NPY is in other species or in clock-resetting by other manipulations, but methods are now available to study this. 7. Interactions between photic and non-photic zeitgebers remain virtually unexplored, but it is evident that photic and non-photic stimuli can attenuate the phase-shifting effects of each other. Interactions are not purely additive or predictable from PRCs. 8. The circadian system does more than synchronize free-running rhythms to the solar day. Its non-photic functions and their interactions with photic inputs probably account for some of the anatomical complexity of circadian circuitry.

Twelve-hour phase shifts of hamster circadian rhythms elicited by voluntary wheel running.

Running in a novel wheel can serve as a nonphotic zeitgeber to entrain or phase shift circadian rhythms in hamsters. In this study, hamsters were entrained to a light:dark schedule of 14:10 h but had no access to running wheels. At four different phase points of the light cycle, hamsters were transferred to constant darkness and provided with running wheels. All hamsters began running shortly after transfer and were allowed to continue running at their own volition. Approximately 20% of the hamsters transferred at zeitgeber time (ZT) 23 (ZT 12 = lights out) ran more than 4 h after transfer and showed phase advances of the circadian activity rhythm by as much as 15 h, while hamsters that ran less than 4 h on average did not phase shift. A similar result was observed for hamsters transferred at ZT 2. Hamsters transferred at ZT 5 and 8 also did not phase shift if they ran less than 4 h, although the relation between longer runs and phase shifts became less evident. A sustained run in excess of 4 h appeared to be associated with large phase advances. These results show that under certain conditions, a single sustained bout of wheel-running activity is capable of phase shifting the circadian pacemaker by more than 12 h.

Non-photic circadian entrainment in the Syrian hamster is not associated with phosphorylation of the transcriptional regulator CREB within the suprachiasmatic nucleus, but is associated with adrenocortical activation.

The mechanisms which mediate non-photic entrainment of the circadian clock are not known. The free-running circadian rhythm of the wheel-running activity of Syrian hamsters was phase advanced by subcutaneous injection of saline and the associated handling at circadian time (CT) 10 (2 h before activity onset, CT 12). Over several experiments, approximately 80% of the animals were sensitive to this non-photic cue and were, therefore, designated as 'shifters'. Injection at CT 6 had no phase-shifting effect in any animals. A series of six injections presented to shifters at CT 10 over 14 circadian cycles produced a cumulative phase advance to the activity rhythm which free ran from the phase established by the final injection, demonstrating that the non-photic stimulus caused true entrainment of the circadian clock, rather than simply masking its expression. Entrainment by light is associated with the rapid phosphorylation of the transcription regulatory factor, cyclic adenosine monophosphate response element binding protein (CREB), in the suprachiasmatic nuclei (SCN), the principal circadian clock. The induction of immunoreactivity to the phosphorylated form of CREB (P-CREB-ir) was used to determine whether phosphorylation is also activated by a non-photic phase-shifting cue. No significant P-CREB-ir was found in shifters maintained under constant dim red light and sampled at either CT 10.05 or 14.05, i.e., times when animals are sensitive to non-photic stimuli and light pulses, respectively. Exposure of animals to light for 5 min at CT 14 caused a dramatic increase in P-CREB-ir within the SCN at CT 14.05. However, despite being sensitive to the phase-shifting effects of handling and injection at CT 10, none of the shifters sampled 5 min after injection of saline at CT 10 exhibited P-CREB-ir within the SCN. These data demonstrate that non-photic cues do not activate a cellular pathway (phosphorylation of CREB) known to be activated within the SCN by light. To assess the importance of arousal in non-photic entrainment, the effect of injection of saline upon activation of the adrenocortical axis, a peripheral index of arousal, was investigated. As anticipated, there was a marked circadian variation in serum cortisol concentrations. In animals identified as shifters, the levels were low during mid-subjective day (CT 6) and rose in advance of activity onset (CT 10). Injection and handling at CT 6 did not have a did not have a significant effect upon serum cortisol levels. In contrast, injection of shifters at CT 10 was associated with a pronounced rise in serum cortisol levels.(ABSTRACT TRUNCATED AT 400 WORDS)

Daily variations in concentration of vasoactive intestinal peptide immunoreactivity in hypothalamic nuclei of rats rendered diurnal by restricted-schedule feeding

We previously described that in the suprachiasmatic (SCN), peri-(PeVN) and paraventricular (PaVN) nuclei of normal rats, vasoactive intestinal peptide (VIP)-like immunoreactivity (VIP-LI) accumulates during the night period and decreases during the day. In order to determine whether these variations are linked to the light-dark cycle or are a consequence of sleep-wake rhythm expression, we dissociated these two parameters by restricting feeding to diurnal hours. In these conditions which inverse the paradoxical sleep rhythm, the VIP-LI pattern is perturbed and its minimum advanced by 4 h in the SCN. In the PeVN, the daily pattern is maintained but the minimum is also advanced by 4 h. Finally, the rhythm is abolished in the PaVN. These circadian fluctuations indicate that the hypothalamic VIP-LI rhythm is not linked to the paradoxical sleep rhythm but could be sensitive to photic and non-photic Zeitgeber.

Photoperiodism in House Sparrows: Testing for Induction with Nonphotic Zeitgebers

In birds, as in other animals, the mechanism for photoperiodic time measurement is based on circadian rhythmicity. In models of this mechanism, the entrainment of circadian rhythms is a key feature. One can therefore ask whether any synchronizing agent (zeitgeber) that can entrain circadian rhythms could also induce photoperiodic responses. We addressed this question using known nonphotic circadian zeitgebers (playbacks of conspecific vocalizations, and nonspecific acoustic disturbance) in house sparrows. We subjected photosensitive male sparrows to stimulatory photoperiods (2L: 10D:2L: 10D and 12.5L: 11.5D) and to similar "phonoperiods" in which part or all of the light of the photoperiods was replaced by a combination of conspecific vocalization playbacks and nonspecific acoustic disturbance. Direct observation with an infrared visionscope revealed that almost all birds remained alert during the sound presentation. Their circadian rhythms were also entrained to the sound. However, whereas sparrows exposed to stimulatory photoperiods experienced testicular growth (from 6 mg to 311 mg), sparrows exposed to the corresponding phonoperiods did not. These results suggest that nonphotic zeitgebers cannot mimic the photoperiodic effect of light. Conceivably, however, photoperiodic-like effects might still be obtained with stronger nonphotic zeitgebers, as yet undiscovered in birds, or with nonphotic zeitgebers whose action would reveal itself only when the zeitgebers occurred at circadian phases other than those at which light is effective.

Reply To–Healy D. and Waterhouse J.M.: the Circadian System and Affective Disorders: Clocks or Rhythms? Chronobiologic Disorders, Social Cues and the Light-Dark Cycle

In their monograph (1), Healy and Waterhouse quite thoughtfully distinguish between the altered shapes of circadian rhythms and their entrainment (synchronization). Although there is a great deal of evidence that various influences can alter the shape of circadian rhythms (“masking”), the literature on multiple time cues (zeitgebers) entraining different pacemakers is less convincing. In humans, evidence for nonphotic (social and activity-rest cycle) zeitgebers is restricted to human studies of anchor sleep (2), to data from Wever (3) and Czeisler (4) and to animal studies by Mrosovksy (5) and Turek (6). Until proven otherwise, it seems most likely that social cues primarily affect the sleep-wake cycle (activity-rest cycle), which– being loosely coupled to the endogenous circadian pacemaker–can be dissociated from it and the overt rhythms that are driven by it.

Testicular Responses of House Sparrows and White-Crowned Sparrows to Short Daily Photoperiods with Low Intensities of Light

Testicular Responses of House Sparrows and White-Crowned Sparrows to Short Daily Photoperiods with Low Intensities of Light