Dual control of seasonal time keeping in male and female juvenile European hamsters.

In contrast to photoperiodic rodent species, adult circannual European hamsters (Cricetus cricetus) do not rely on melatonin as transducer of the photoperiodic message. Instead, seasonal entrainment involves a special circadian organisation which characterizes a photoperiod-sensitive phase. When days shorten a precise activity pattern ("summer pattern") switches to a weak or arrhythmic "winter pattern". At the very same day gonadal regression is initiated and the circannual clock is reset. In contrast to this difference in photoperiodic time measurement, the broad time span in which offspring are born and the birth-season dependent timing of puberty is similar to photoperiodic rodents. We investigated how juvenile European hamsters measure photoperiod to situate themselves at the proper position in the annual cycle. Activity and 6-sulphatoxymelatonin (aMT6s) excretion were recorded in pups of five litters born at different seasons. Pups of all litters showed an activity pattern identical with the adults' summer pattern until postnatal day 78, suggesting that the pathway known to reset the circannual clock in adults is functional. The synchronous start of reproduction in yearlings supports this. However, since puberty and gonadal regression occurred before the switch in the activity pattern, the timing of reproduction in the birth year must be controlled by other means. As in photoperiodic species melatonin might be involved, since the aMT6s excretion showed daily and seasonal rhythms from early life on.

Photoperiod can entrain circannual rhythms in pinealectomized European hamsters.

In mammals, the pineal hormone melatonin is thought to be essential to process environmental photoperiodic information. In this study, we demonstrate in a circannual species, the European hamster Cricetus cricetus, the existence of a melatonin-independent second pathway. In 4 physiological parameters (reproduction, body weight, activity pattern, body temperature), a large majority of pinealectomized European hamsters were entrained to an accelerated photoperiodic regime. It compressed the natural variations in the photoperiod to a 6-month cycle, which allowed us to record up to 6 complete physiological cycles during the life span of the individuals. We show further that whether a pinealectomized animal is able to entrain to changes in the photoperiod is influenced by the season of pinealectomy. The results do not disprove that melatonin is capable of entraining a circannual rhythm, but they show clearly that melatonin is not necessary, demonstrating another melatonin-independent pathway for circannual entrainment by the photoperiod. In view of these new insights, a revision of the original literature revealed that probably the melatonin-independent pathway plays an important role in most circannual mammals but only a minor role in photoperiodic species. Thus, the present work provides also the first evidence for different synchronization mechanisms in photoperiodic and circannual species.

Interspecific contact affects phase response and activity in Desert hamsters.

Circadian rhythms enhance survival and reproductive fitness of animals by promoting optimal timing of behavior and physiology with reference to geophysical changes in environment. Although light is considered the dominant stimulus for entraining circadian rhythms, social stimuli can also act as zeitgebers. The aim of this study was to analyze how Desert hamsters (Phodopus roborovskii) coordinate their behavior in time with that of animals of another competing species (Mongolian gerbils, Meriones unguiculatus). First, the behavior of hamsters was analyzed during a step-wise avoidance test. Two effects were observed: a) spatial separation if it was possible or b) shortening of the activity period due to contact without chance for avoidance. The latter finding was now further analyzed using a phase response curve (PRC). Here, phase shifts of Desert hamsters caused by single social interactions with Mongolian gerbils were quantified. Phase advances during the rest period were found at CT3 and CT9, a similar tendency was observed at CT6. A second phase advance was determined at CT18, coinciding with the end of the activity period. Then, it was tested whether additional activity during the stimulus was a trigger for the phase response. Although an increase in activity occurred especially when stimuli were applied during the rest period, there was no general relation between additional activity measured and the phase response shown. Overall, relevance of interspecific contact as nonphotic zeitgeber was indicated by phase shifts in a phase response curve. The shape of it can be explained by two behavioral adaptations; stress and contact avoidance.

5-HT3 receptor-mediated photic-like responses of the circadian clock in the rat.

Serotonin (5-HT) and 5-HT agonists have various resetting effects on the master clock, located in the suprachiasmatic nucleus (SCN), depending on the species. In rats, they induce photic-like effects on both locomotor activity rhythms and gene expression in the SCN. The 5-HT receptor(s) mediating these effects at circadian time 22 are localized in the SCN, most likely at a presynaptic level, on the retinohypothalamic terminals (RHT) known to convey photic information by releasing glutamate. Indeed, RHT degeneration blocks photic-like effects of a non-specific 5-HT agonist, quipazine. However, the 5-HT receptor subtype(s) involved is still unknown, although 5-HT(3) receptor activation is known to induce glutamate release. We thus analyzed the effects of selective 5-HT(3) agonist and antagonist, as well as a specific NMDA receptor antagonist, on different parameters of the clock. This study shows that the 5-HT(3) receptor mediates the resetting effects of quipazine on locomotor activity rhythms. The 5-HT(3) receptor is only partially implicated in quipazine-induced expression of c-FOS, while NMDA receptor inhibition blocks quipazine photic-like effects on both parameters. Taken together, photic-like responses produced by 5-HT stimulation in rats are likely mediated by (presynaptic?) 5-HT(3) receptor activation followed by NMDA receptor activation.

Asymmetric control of short day response in European hamsters.

The European hamster (Cricetus cricetus) is a circannual species in which the synchronization of the circannual cycle to the natural year occurs during 2 annual phases of sensitivity. Around the summer solstice, the animals are sensitive to a shortening of photoperiod. During this sensitive phase, pronounced changes in circadian output parameters are observed, indicating a different functional state of the circadian system. This special state is assumed to be necessary to develop the extreme sensitivity to short day length in European hamsters during this phase. In natural conditions, the animals are able to recognize the shortening of photoperiod already in mid-July, when the photoperiod is reduced only by 30 min. To investigate the short-day response in sensitive European hamsters on the basis of the 2-coupled oscillator model of Pittendrigh and Daan (1976), daily activity and the reproductive state of European hamsters were recorded after an asymmetrical reduction of photoperiod from long (LD 16:08) to short (LD 08:16) photoperiods. The activity pattern of the animals showed an immediate response to the short photoperiod at the day of transfer when the night was extended only into the evening, but there was a significant delay in the response time when the night was extended into the morning. Thus, the evening oscillator E is more important in inducing the photoperiodic response than the morning oscillator M. Moreover, the broad intragroup variation in the latter conditions strongly suggests that the changes in the activity pattern were endogenously induced and that the animals were not able to recognize a lengthening of the night into the morning. Gonadal regression started in both groups 3 weeks after the change in the activity pattern, indicating that this process is initiated when the circadian system has received the short-day signal either through changes in photoperiod or through the circannual clock.

Seasonal variations in circadian rhythms coincide with a phase of sensitivity to short photoperiods in the European hamster.

European hamsters (Cricetus cricetus) show pronounced seasonal changes in their physiology and behavior. The present study provides a detailed analysis of the temporal relationship between seasonal cycles of reproduction and body mass and seasonal changes of two circadian parameters, i.e., locomotor activity and 6-sulphatoxymelatonin (aMT6s) excretion, in individual animals kept under natural light conditions. Our results demonstrate a characteristic pattern of locomotor activity and aMT6s excretion observed around the summer solstice, i.e., from mid-May to mid-July. During this time, locomotor activity was characterized by a high level of activity and an early activity onset, while the nightly elevation of melatonin was reduced to baseline levels. These seasonal changes in aMT6s excretion and locomotor activity were only loosely related to changes in the reproductive status of the animals, but correlated well with a period of the annual cycle during which the animals were sensitive to short days. They may therefore reflect a specific state of the circadian pacemaker system within the SCN and can thus be a valuable tool to further characterize molecular and physiological mechanisms of photoperiodic time measurements in European hamsters.

The circadian RNA-binding protein CHLAMY 1 represents a novel type heteromer of RNA recognition motif and lysine homology domain-containing subunits.

The RNA-binding protein CHLAMY 1 from Chlamydomonas reinhardtii binds specifically to UG> or =7 repeat sequences situated in the 3' untranslated regions of several mRNAs. Its binding activity is controlled by the circadian clock. The biochemical purification and characterization of CHLAMY 1 revealed a novel type of RNA-binding protein. It includes two different subunits (named C1 and C3), whose interaction appears necessary for RNA binding. One of them (C3) belongs to the proteins of the CELF (CUG-BP-ETR-3-like factors) family and thus bears three RNA recognition motif domains. The other is composed of three lysine homology domains and a protein-protein interaction domain (WW). The subunits C1 and C3 have theoretical molecular masses of 45 and 52 kDa, respectively, and are present in nearly equal amounts during the circadian cycle. At the beginning of the subjective night, both can be found in protein complexes of 100 to 160 kDa. However, during subjective day when binding activity of CHLAMY 1 is low, the C1 subunit in addition is present in a high-molecular-mass protein complex of more than 680 kDa. These data indicate posttranslational control of the circadian binding activity of CHLAMY 1. Notably, the C3 subunit shows significant homology to the rat CUG-binding protein 2. Anti-C3 antibodies can recognize the rat homologue, which can also be found in a protein complex in this vertebrate.

European hamsters (Cricetus cricetus) show a transient phase of insensitivity to long photoperiods after gonadal regression.

Annual rhythms of body weight and reproduction in the European hamster (Cricetus cricetus) are the result of an interaction between seasonal changes in day length (photoperiod) and seasonal changes in the responsiveness of animals to these photoperiods. The present study demonstrates that under natural conditions European hamsters are not able to perceive long photoperiods (i.e., a 16L:8D cycle) before mid-November. This is an important difference to other hamster species, in which regrowth of the gonads can be stimulated by exposure to long photoperiods at any stage of gonadal regression. The experiments also demonstrate the existence of an annual phase of sensitivity to long photoperiods that starts around mid-November and extends until March/April. During this phase of sensitivity, exposure to a long photoperiod (16L:8D) induced gonadal regrowth within 3 wk. Additional experiments with an accelerated photoperiodic lighting regimen indicated that a photoperiod of approximately 13 h is necessary to stimulate gonadal regrowth. Under natural light conditions in Stuttgart (48.46 degrees N), a photoperiod of 13 h is reached by the beginning of April, which fits well with the finding that the majority of animals kept under a natural light:dark cycle had well-developed gonads by the end of April. Nevertheless, these animals showed a rather variable timing of gonadal regrowth, ranging from early January to late April. This is most likely the result of two processes: first, an endogenous mechanism (photorefractoriness) that induces gonadal recrudescence without any photoperiodic information while the animals are still in their hibernation burrows, and second, a direct stimulatory effect of long photoperiods.