Pineal-dependent and -independent effects of photoperiod on immune function in Siberian hamsters (Phodopus sungorus)

Siberian hamsters (Phodopus sungorus) exhibit reproductive and immunological responses to photoperiod. Short (<10-h light/day) days induce gonadal atrophy, increase leukocyte concentrations, and attenuate thermoregulatory and behavioral responses to infection. Whereas hamster reproductive responses to photoperiod are dependent on pineal melatonin secretion, the role of the pineal in short-day induced changes in immune function is not fully understood. To examine this, adult hamsters were pinealectomized (PINx) or sham-PINx, and transferred to short days (9-h light/day; SD) or kept in their natal long-day (15-h light/day; LD) photoperiod. Intact and PINx hamsters housed in LD maintained large testes over the next 12 weeks; sham-PINx hamsters exhibited gonadal regression in SD, and PINx abolished this effect. Among pineal-intact hamsters, blood samples revealed increases in leukocyte, lymphocyte, CD62L+ lymphocyte, and T cell counts in SD relative to LD; PINx did not affect leukocyte numbers in LD hamsters, but abolished the SD increase in these measures. Hamsters were then treated with bacterial lipopolysaccharide (LPS), which induced thermoregulatory (fever), behavioral (anorexia, reductions in nest building), and somatic (weight loss) sickness responses in all groups. Among pineal-intact hamsters, febrile and behavioral responses to LPS were attenuated in SD relative to LD. PINx did not affect sickness responses to LPS in LD hamsters, but abolished the ameliorating effects of SD on behavioral responses to LPS. Surprisingly, PINx failed to abolish the effect of SD on fever. In common with the reproductive system, PINx induces the LD phenotype in most aspects of the immune system. The pineal gland is required for photoperiodic regulation of circulating leukocytes and neural-immune interactions that mediate select aspects of sickness behaviors.     

Gonadal hormone-dependent and -independent regulation of immune function by photoperiod in Siberian hamsters

Siberian hamsters (Phodopus sungorus) exhibit changes in reproductive and immune function in response to seasonal variations in day length. Exposure to short days induces gonadal regression and inhibits testosterone secretion. In parallel, short days enhance immune function: increasing leukocyte numbers and attenuating cytokine and behavioral responses to infection. We examined whether photoperiodic changes in leukocyte phenotypes and sickness behaviors are dependent on concurrent photoperiodic changes in gonadal function. Male hamsters were gonadectomized or sham-gonadectomized and either exposed to short days (9 h light/day; SD) or kept in their natal long-day (15 h light/day; LD) photoperiod for 10-13 wk. Blood samples were obtained for leukocyte enumeration, and hamsters were challenged with bacterial LPS, which induced behavioral (anorexia, reductions in nest building) and somatic (weight loss) sickness responses. Among gonad-intact hamsters, exposure to SD increased total and CD62L+ lymphocytes and CD3+ T lymphocytes in blood and significantly attenuated LPS-induced sickness responses. Independent of photoperiod, castration alone increased total and CD62L+ lymphocyte and CD3+ T lymphocyte numbers and attenuated somatic and anorexic sickness responses. Among castrated hamsters, SD exposure increased lymphocyte numbers and suppressed sickness behaviors. In castrated hamsters, the magnitude of most immunological effects of SD were diminished relative to those evident in gonad-intact hamsters. The SD phenotype in several measures of immunity can be instated via elimination of gonadal hormones alone; however, photoperiodic effects on immune function persist even in castrated hamsters. Thus, photoperiod affects the immune system and neural-immune interactions underlying sickness behaviors via gonadal hormone-dependent and -independent mechanisms.     

Photoperiod controls the induction,retention, and retrieval of antigen-specific immunological memory

Changes in day length affect several measures of immunity in seasonally breeding mammals. In Siberian hamsters (Phodopus sungorus), short day lengths suppress specific secondary antibody responses to the keyhole limpet hemocyanin (KLH) antigen and enhance cutaneous delayed-type hypersensitivity (DTH) responses to dinitrofluorobenzene (DNFB). These experiments tested whether day length affects secondary antibody and DTH responses by altering immune function solely during the interval after the initial exposure to each antigen, solely during the interval after the second exposure, or during both stages of the respective immune responses. Adult male Siberian hamsters were exposed to either a long (16 h light/day; LD) or a short (8 h light/day; SD) photoperiod for 7.5 wk before receiving an initial exposure to each antigen (KLH injection, cutaneous DNFB treatment; separate groups of animals for each antigen). A subset of LD hamsters was transferred to the SD photo-period, and a subset of SD hamsters was transferred to the LD photoperiod. Other hamsters remained in LD or SD. Eight weeks later, all hamsters were challenged with a second subcutaneous injection of KLH or a second application of DNFB to the ear, and immune responses were measured. Exposure to SD during the primary antibody response did not affect secondary IgG responses, but SD exposure during the secondary response significantly suppressed IgG production independent of day length during the initial KLH treatment. In contrast, exposure to SD during the DNFB challenge enhanced the ensuing DTH response, but this enhancement depended on the photoperiod prevailing during the initial exposure. Exposure to SD during the sensitization stage did not enhance DTH in hamsters subsequently exposed to LD. The data suggest that short photoperiods have enduring effects on immune responsiveness and on the establishment and retention of immunological memory.     

Peripubertal immune challenges attenuate reproductive development in male Siberian hamsters (Phodopus sungorus)

Differential allocation of energy to reproduction versus host defense is assumed to drive the seasonal antiphase relation between peak reproductive function and immunocompetence; however, evidence supporting this assumption is only correlational. These experiments tested whether photoperiod affects immune responses to antigens in peripubertal Siberian hamsters, whether such activation of the immune system exacts energetic and reproductive costs, and whether such costs vary seasonally. Male Siberian hamsters were raised from birth in long (LD) or short days (SD), which respectively initiate or inhibit the onset of puberty. To elicit a specific immune response, hamsters were injected with a novel antigen (keyhole limpet hemocyanin [KLH]) as juveniles. Reproductive development was attenuated and body temperature was elevated in LD hamsters relative to saline-injected control animals. In contrast, KLH treatments affected neither thermoregulation nor reproductive development in photoinhibited SD hamsters. In experiment 2, juvenile male hamsters were challenged with bacterial lipopolysaccharide (LPS) in order to elicit an innate immune response. Febrile and anorexic responses to LPS were greater in reproductively stimulated LD hamsters relative to reproductively inhibited SD hamsters. LPS treatments attenuated somatic and testicular development in LD hamsters, but did not significantly affect circulating testosterone concentrations. In contrast, LPS treatments were without effect on somatic and reproductive development in SD hamsters. These experiments indicate that photoperiod affects antigen-specific antibody production, febrile responses to LPS, and sickness behaviors in juvenile Siberian hamsters, and that peripubertal activation of the immune system exacts energetic and metabolic costs that can diminish the magnitude of somatic and reproductive maturation in LD. The data also underscore the importance of seasonally dependent life history factors in assessing physiological tradeoffs.     

Different photoperiods affect proliferation of lymphocytes but not expression of cellular,humoral, or innate immunity in hamsters

In seasonal mammals, photoperiod change is associated with a suite of alterations in physiology. It has recently been proposed that the immune response is one of the systems regulated by changes in photoperiod, although this hypothesis has not been rigorously challenged by assays of functional immune responses. The aim of this study was to test the hypothesis that photoperiod modulates immune responsiveness in Syrian (Mesocricetus auratus) and Siberian (Phodopus sungorus) hamsters. Consistent with previously reported data, short-day-housed (SD) animals exhibited a significant increase in lymph node cell (LNC) numbers and increased cellular proliferation in response to the polyclonal mitogen concanavalin A compared to long-day-housed (LD) animals. In contrast, LNC numbers from intact or gonadectomized SD animals that had been sensitized with the antigen dinitrofluorobenzene (DNFB) exhibited a reduced ex vivo proliferative response and reduced production of interleukin-6 (IL-6) compared to LD animals. In vivo studies of the contact hypersensitivity response of animals that had previously been sensitized, and subsequently challenged, with DNFB were similar in SD and LD animals, as was the proliferative activity of LNC recovered from these animals. There were also no photoperiodic differences in the antidinitrophenyl antibody response of animals sensitized with DNFB, or the anti-sheep red blood cell (srbc) response of animals immunized with srbc. Furthermore, no differences could be detected in the activity of natural killer cells from spleens of LD and SD Siberian hamsters, or in lipopolysaccharide-induced IL-6 production by LD and SD Syrian hamsters in vivo. Thus, although photoperiod is able to influence factors regulating the gross number and non-antigen-specific proliferation of lymphocytes in seasonally breeding mammals, day length does not directly influence activation of an effective immune response. The authors conclude, therefore, that expression of the immune response is not directly modified or compromised by photoperiod in these seasonally breeding hamster species.     

Pubertal growth of the medial amygdala delayed by short photoperiods in the Siberian hamster, Phodopus sungorus

We investigated whether puberty influences the morphology of the medial nucleus of the amygdala (MeA) by comparing Siberian hamsters (Phodopus sungorus) that had been raised from birth in either long day (LD; 16:8 h light:dark) or short day (SD; 8:16) photoperiods. Hamsters were sacrificed at 42-49 days of age, at which point all LD hamsters were reproductively mature, as evidenced by adult-like testes weights (mean: 657 mg). In contrast, the testes weights of the SD hamsters were low (mean: 31 mg), indicating that the SD photoperiod had delayed puberty. The regional volume and mean soma size of the four MeA subnuclei was estimated bilaterally by stereological procedures. In the posterior dorsal and ventral MeA subnuclei, regional volume was 22-25% larger, and mean soma size 18% larger, in LD males than SD males. Unbiased cell counts in the posterior dorsal MeA showed that LD and SD hamsters have equivalent neuron numbers. In the anterior MeA subnuclei, regional volumes and soma sizes from LD and SD hamsters were equivalent. Additionally, the regional volume of the posteroventral subnucleus was larger in the right hemisphere than the left, but this laterality did not respond to photoperiod manipulation. These results suggest that the extant neurons within the posterior MeA, a steroid-sensitive nucleus implicated in socio-sexual behavior, grow in response to the elevated levels of circulating androgen accompanying puberty, and that photoperiodic regulation of puberty affects morphological maturation of this nucleus.     

Maternal transfer of photoperiodic information in Siberian hamsters. III. Melatonin injections program postnatal reproductive development expressed in constant light

In Siberian hamsters, transference of photoperiodic information from dam to fetus influences pubertal testicular development of the young when reared either in constant light (LL) or postnatal photoperiods of intermediate length (i.e. 14L:10D). The effects of short photoperiods during gestation can be mimicked by administering melatonin to pregnant females. This experiment examined whether there exists a daily pattern of sensitivity to melatonin when it is administered to pineal-intact pregnant females housed on a long photoperiod. Groups of pregnant and lactating females received melatonin at each hour of the day. The young were not treated with exogenous melatonin. At the approximate time of maturation of their endogenous pineal melatonin rhythm (Day 15), the young were placed in LL to suppress pineal melatonin secretion. Young males were killed at 28 days of age. Afternoon (1200 h-2000 h) and late night (0400 h) injections of melatonin into females caused their male young to develop as though gestation occurred on a short photoperiod. Melatonin injections at other times were ineffective. The daily pattern of effectiveness of exogenous melatonin administration to pregnant females resembles that observed in adult males of this and other hamster species and is consistent with the hypothesis that a daily rhythm in sensitivity to melatonin is involved in the transduction of photoperiodic signals.     

Hypothalamic Ventricular Ependymal Thyroid Hormone Deiodinases Are an Important Element of Circannual Timing in the Siberian Hamster (Phodopus sungorus)

Exposure to short days (SD) induces profound changes in the physiology and behaviour of Siberian hamsters, including gonadal regression and up to 30% loss in body weight. In a continuous SD environment after approximately 20 weeks, Siberian hamsters spontaneously revert to a long day (LD) phenotype, a phenomenon referred to as the photorefractory response. Previously we have identified a number of genes that are regulated by short photoperiod in the neuropil and ventricular ependymal (VE) cells of the hypothalamus, although their importance and contribution to photoperiod induced physiology is unclear. In this refractory model we hypothesised that the return to LD physiology involves reversal of SD expression levels of key hypothalamic genes to their LD values and thereby implicate genes required for LD physiology. Male Siberian hamsters were kept in either LD or SD for up to 39 weeks during which time SD hamster body weight decreased before increasing, after more than 20 weeks, back to LD values. Brain tissue was collected between 14 and 39 weeks for in situ hybridization to determine hypothalamic gene expression. In VE cells lining the third ventricle, expression of nestin, vimentin, Crbp1 and Gpr50 were down-regulated at 18 weeks in SD photoperiod, but expression was not restored to the LD level in photorefractory hamsters. Dio2, Mct8 and Tsh-r expression were altered by SD photoperiod and were fully restored, or even exceeded values found in LD hamsters in the refractory state. In hypothalamic nuclei, expression of Srif and Mc3r mRNAs was altered at 18 weeks in SD, but were similar to LD expression values in photorefractory hamsters. We conclude that in refractory hamsters not all VE cell functions are required to establish LD physiology. However, thyroid hormone signalling from ependymal cells and reversal of neuronal gene expression appear to be essential for the SD refractory response.     

Interval timer control of puberty in photoinhibited Siberian hamsters

Puberty, which is markedly delayed in male Siberian hamsters (Phodopus sungorus) born into short day lengths, is controlled by an interval timer regulated by the duration of nocturnal melatonin secretion. Properties of the interval timer were assessed by perturbing normal patterns of melatonin secretion in males gestated and maintained thereafter in 1 of 2 short day lengths, 10 h light/day (10 L) or 12L. Melatonin secretion of short-day hamsters was suppressed by constant light treatment or modified by daily injection of propranolol to mimic nocturnal melatonin durations typical of long-day hamsters. Constant light treatment during weeks 3 to 5 induced early incomplete gonadal growth in 12L but not 10 L hamsters but did not affect late onset of gonadal development indicative of puberty in either photoperiod. Propranolol treatment during postnatal weeks 3 to 5 induced transient growth of the testes and ultimately delayed the timing of puberty by 3 weeks. Similar treatments between weeks 5 and 7 or on alternate weeks for 24 weeks did not affect the interval timer. The first 2 weeks after weaning may constitute a critical period during which the interval timer is highly responsive to photoperiod. Alternatively, the hamsters' photoperiodic history rather than age or developmental stage may be the critical variable. The interpolation of long-day melatonin signals at the time of weaning does not appear to reset the interval timer to its zero position but may reduce timer responsiveness to long-day melatonin signals several weeks later.     

Kisspeptin mediates the photoperiodic control of reproduction in hamsters

The KiSS-1 gene encodes kisspeptin, the endogenous ligand of the G-protein-coupled receptor GPR54. Recent data indicate that the KiSS-1/GPR54 system is critical for the regulation of reproduction and is required for puberty onset. In seasonal breeders, reproduction is tightly controlled by photoperiod (i.e., day length). The Syrian hamster is a seasonal model in which reproductive activity is promoted by long summer days (LD) and inhibited by short winter days (SD). Using in situ hybridization and immunohistochemistry, we show that KiSS-1 is expressed in the arcuate nucleus of LD hamsters. Importantly, the KiSS-1 mRNA level was lower in SD animals but not in SD-refractory animals, which spontaneously reactivated their sexual activity after several months in SD. These changes of expression are not secondary to the photoperiodic variations of gonadal steroids. In contrast, melatonin appears to be necessary for these seasonal changes because pineal-gland ablation prevented the SD-induced downregulation of KiSS-1 expression. Remarkably, a chronic administration of kisspeptin-10 restored the testicular activity of SD hamsters despite persisting photoinhibitory conditions. Overall, these findings are consistent with a role of KiSS-1/GPR54 in the seasonal control of reproduction. We propose that photoperiod, via melatonin, modulates KiSS-1 signaling to drive the reproductive axis.     

Early photoperiod history and short-day responsiveness in Siberian hamsters

Siberian hamsters exhibit seasonal, photoperiod influenced cycles of reproductive activity, body size, pelage characteristics, and thermoregulatory behavior. Laboratory populations generally exhibit inter-individual variability in expression of photoperiod responsiveness, with a subset of individuals that fail to show the species typical responses to short photoperiod. This variability is partly explained by a genetic component, as it has been possible to increase the number of short-day nonresponders by artificial selection. Responsiveness to short photoperiod is also substantially influenced by photoperiod history in this species; hamsters that have been raised under long (16L) or very long (18L) day lengths are less likely to exhibit winter-type responses to short days as compared to hamsters raised under an intermediate (14L) day length. In the present experiment, we examined effects of age and early photoperiod history in a strain of Siberian hamsters that had been selected for short-day nonresponsiveness. Hamsters transferred into short photoperiod on the day of birth were uniform in exhibiting winter-type responses. However, hamsters raised until 25 days of age in either continuous illumination or in 16L exhibited variation in responsiveness when subsequently moved into short photoperiod. We conclude that virtually all hamsters of the short-day nonresponsive strain are born responsive to short days. Subsequent development of resistance to potential short day effects is dependent on age and/or photoperiod history.     

Reception of photoperiodic information by fetal Siberian hamsters: role of the mother's pineal gland

The rate of reproductive development in juvenile male Siberian hamsters is strongly influenced by daylength (photoperiod). Recent studies indicate that reception of photoperiodic cues begins during fetal life. The present experiments yielded a further demonstration that developing male Siberian hamsters receive information about the photoperiod to which their mother is exposed during pregnancy. The possibility that photoperiodic information is transmitted from mother to young after birth was investigated by cross-fostering young gestated on 12L and 16L to mothers from the other photoperiod. Litters were cross-fostered on the day of birth and then were transferred, along with their foster mothers, to 14L. We found no influence of the mother after birth, indicating that transmission of photoperiodic information from mother to young must occur during gestation. To determine if the pineal gland of the mother is required for this response, adult females were pinealectomized or sham-operated and paired with intact males in 12L, 14L, or 16L. After parturition parents and offspring were exposed to 14L. The influence of prenatal photoperiod on postnatal testicular development in 14L was blocked by pinealectomy of the mother. Postnatal testicular development was retarded in offspring that experienced a photoperiod transfer from either 15L to 14L or 8L to 12L at birth. In contrast, the inhibitory effect of a transfer from 16L to 14L at birth was abolished when juvenile males were exposed to a single long photoperiod (16.3 h light) at age 17-21 days and then were returned to 14L.     

Lipolytic and antilipolytic responses of the Siberian hamster (Phodopus sungorus sungorus) white adipocytes after weight loss induced by short photoperiod exposure

Short day photoperiod promotes thermogenesis and extensive weight loss in Siberian hamsters (Phodopus sungorus sungorus). To determine whether a change in hormone-sensitive lipolysis occurs after short-photoperiod exposure, some lipolytic responses were measured on white adipocytes isolated from animals exposed in warm conditions to short or Long daylight photoperiod. The body mass of male Siberian hamsters exposed during 11 weeks to short days (SD; light: dark, 6:18 hr) reached only 50% of those kept in long days (LD; 16: 8 hr). In SD-hamsters, adipose depot mass also represented approximately 50% of the LD group. A lower DNA content was observed in intra-abdominal fat pads of SD-hamsters. Lipolytic responses to noradrenaline, adrenaline, isoproterenol and ACTH were unchanged. However, sensitivity to the beta-3 adrenergic agonist, BRL 37344, was moderately increased. The major component of the adrenergic control of lipolysis was mediated by beta-3 adrenoceptors in both LD- and SD-Siberian hamsters. The limited antilipolytic effect of alpha-2 adrenergic agonists, PYY or insulin was rather surprising in Siberian hamsters since these inhibitory systems are efficient in hibernants and other photoperiod-sensitive rodents. Our results show that, after short photoperiod exposure, white adipose tissue mass and DNA content are reduced, especially in the epididymal fat pad, with only minor changes in the adipocyte sensitivity to lipolytic hormones.     

Maternal transfer of photoperiodic information in Siberian hamsters. II. The nature of the maternal signal, time of signal transfer, and the effect of the maternal signal on peripubertal reproductive development in the absence of photoperiodic input

Peripubertal reproductive development of Siberian hamsters is controlled by maternally derived photoperiodic information and the ambient photoperiod present after weaning. Previous experiments suggested that the maternally derived information is transferred during gestation, not during lactation. Development was examined in several photoperiods following manipulation of gestational and lactational photoperiods; development was influenced by the gestational, but not lactational, photoperiod. Second, effects of the gestational photoperiod were observed in young reared in constant light (LL) from Day 15. Depriving the young of ambient photoperiodic information after Day 15 allows a more direct assessment of the signal received from their dams. Finally, melatonin injections to long-day dams, at certain times of day, caused transmission of a short-day signal to young, as evidenced by their development in LL and light-dark cycles. Thus, a maternally derived signal that is dependent on melatonin influences reproductive development of the young during gestation; the maternally directed pattern of development can subsequently be modified by the youngs' own response to ambient photoperiods after weaning.     

Inhibition of hibernation by exercise is not affected by intergeniculate leaflets lesion in hamsters

The circadian clock of mammals, located in the suprachiasmatic nuclei (SCN) of the hypothalamus, has been demonstrated to integrate day length change from long (LP) to short photoperiod (SP). This photoperiodic change induces in Syrian hamsters a testicular regression through melatonin action, a phenomenon that is inhibited when hamsters have free access to a wheel. The intergeniculate leaflets (IGL), which modulate the integration of photoperiod by the SCN, are a key structure in the circadian system, conveying nonphotic information such as those induced by novelty-induced wheel running activity. We tested in hamsters transferred from LP to a cold SP the effects of wheel running activity on a photoperiod-dependent behavior, hibernation. Lesions of the IGL were done to test the role of this structure in the inhibition induced by exercise of photoperiod integration by the clock. We show that wheel running activity actually inhibits hibernation not only in sham-operated animals, but also in hamsters with a bilateral IGL lesion (IGLX). In contrast, IGL-X hamsters without a wheel integrate slower to the SP but hibernate earlier compared with sham-operated animals. Moreover, some hibernation characteristics are affected by IGL lesion. Throughout the experiment at 7 degrees C, IGL-X hamsters were in hypothermia during 18% of the experiment vs. 32% for sham-operated hamsters. Taken together, these data show that the IGL play a modulatory role in the integration of photoperiodic cues and modulate hibernation, but they are not implicated in the inhibition of hibernation induced by wheel running activity.     

Pineal-independent regulation of photo-nonresponsiveness in the Siberian hamster (Phodopus sungorus)

The pineal hormone melatonin influences circadian rhythms and also mediates reproductive responses to photoperiod. The authors tested whether pinealectomy influences circadian oscillators responsible for induction of nonresponsiveness to short day lengths by preventing normal short-day patterns of circadian entrainment. Adult male Siberian hamsters were pinealectomized or sham operated, maintained in either 18 h light per day (18L) or 15L for 10 weeks, and then tested for responsiveness to 10L. Because pinealectomized hamsters do not show gonadal regression in short day lengths, responsiveness was assessed by measuring phase angle of entrainment and the length of the nightly activity period following transfer to 10L. The incidence of nonresponsiveness was significantly higher in 18L hamsters than in 15L hamsters but was unaffected by pineal status. Fully 88% of 18L hamsters failed to entrain to 10L in the normal short-day manner; the duration of nightly activity remained compressed, and the phase angle of entrainment was large and negative relative to lights off. The 15L hamsters entrained normally to 10L. Exposure to constant light after 10L treatment was equally effective in inducing arrhythmicity in pinealectomized and intact hamsters. Changes in the period of morning and evening circadian oscillators subsequent to 18L treatment did not predict circadian responsiveness to short photoperiod. Long-day induction of photo-nonresponsiveness, which prevents winter responses to short day lengths, occurs independently of pineal melatonin feedback on the circadian system.     

Short days and exogenous melatonin increase aggression of male Syrian hamsters (Mesocricetus auratus)

Many nontropical rodent species rely on photoperiod as a primary cue to coordinate seasonally appropriate changes in physiology and behavior. Among these changes, some species of rodents demonstrate increased aggression in short, "winter-like" compared with long "summer-like" day lengths. The precise neuroendocrine mechanisms mediating changes in aggression, however, remain largely unknown. The goal of the present study was to examine the effects of photoperiod and exogenous melatonin on resident-intruder aggression in male Syrian hamsters (Mesocricetus auratus). In Experiment 1, male Syrian hamsters were housed in long (LD 14:10) or short (LD 10:14) days for 10 weeks. In Experiment 2, hamsters were housed in long days and half of the animals were given daily subcutaneous melatonin injections (15 microg/day in 0.1 ml saline) 2 h before lights out for 10 consecutive days to simulate a short-day pattern of melatonin secretion, while the remaining animals received injections of the vehicle alone. Animals in both experiments were then tested using a resident-intruder model of aggression and the number of attacks, duration of attacks, and latency to initial attack were recorded. In Experiment 1, short-day hamsters underwent gonadal regression and displayed increased aggression compared with long-day animals. In Experiment 2, melatonin treatment also increased aggression compared with control hamsters without affecting circulating testosterone. Collectively, the results of the present study demonstrate that exposure to short days or short day-like patterns of melatonin increase aggression in male Syrian hamsters. In addition, these results suggest that photoperiodic changes in aggression provide an important, ecologically relevant model with which to study the neuroendocrine mechanisms underlying aggression in rodents.     

Twice Daily Melatonin Peaks in Siberian but not Syrian Hamsters under 24 h Light:Dark:Light:Dark Cycles

The daily pattern of blood-borne melatonin varies seasonally under the control of a multi-oscillator circadian pacemaker. Here we examine patterns of melatonin secretion and locomotor activity in Siberian and Syrian hamsters entrained to bimodal LDLD8:4:8:4 and LD20:4 lighting schedules that facilitate novel temporal arrangements of component circadian oscillators. Under LDLD, both species robustly bifurcated wheel-running activity in distinct day scotophase (DS) and night scotophase (NS) bouts. Siberian hamsters displayed significant melatonin increases during each scotophase in LDLD, and in the single daily scotophase of LD20:4. The bimodal melatonin secretion pattern persisted in acutely extended 16 h scotophases. Syrian hamsters, in contrast, showed no significant increases in plasma melatonin during either scotophase of LDLD8:4:8:4 or in LD20:4. In this species, detectable levels were observed only when the DS of LDLD was acutely extended to yield 16 h of darkness. Established species differences in the phase lag of nocturnal melatonin secretion relative to activity onset may underlie the above contrast: In non-bifurcated entrainment to 24 h LD cycles, Siberian hamsters show increased melatonin secretion within ～2 h after activity onset, whereas in Syrian hamsters, detectable melatonin secretion phase lags activity onset and the L/D transition by at least 4?h. The present results provide new evidence indicating multi-oscillator regulation of the waveform of melatonin secretion, specifically, the circadian control of the onset, offset and duration of nocturnal secretion.     

A melatonin-independent seasonal timer induces neuroendocrine refractoriness to short day lengths.

The duration of nocturnal pineal melatonin secretion transduces effects of day length (DL) on the neuroendocrine axis of photoperiodic rodents. Long DLs support reproduction, and short DLs induce testicular regression, followed several months later by spontaneous recrudescence; gonadal regrowth is thought to reflect development of tissue refractoriness to melatonin. In most photoperiodic species, pinealectomy does not diminish reproductive competence in long DLs. Turkish hamsters (Mesocricetus brandti) deviate from this norm: elimination of melatonin secretion in long-day males by pinealectomy or constant light treatment induces testicular regression and subsequently recrudescence; the time course of these gonadal transitions is similar to that observed in males transferred from long to short DLs. In the present study, long-day Turkish hamsters that underwent testicular regression and recrudescence in constant light subsequently were completely unresponsive to the antigonadal effects of short DLs. Other hamsters that manifested testicular regression and recrudescence in short DLs were unresponsive to the antigonadal effects of pinealectomy or constant light. Long-term suppression of melatonin secretion induces a physiological state in Turkish hamsters similar or identical to the neuroendocrine refractoriness produced by short-day melatonin signals (i.e., neural refractoriness to melatonin develops in the absence of circulating melatonin secretion). A melatonin-independent interval timer, which would remain operative in the absence of melatonin during hibernation, may determine the onset of testicular recrudescence in the spring. In this respect, Turkish hamsters differ from most other photoperiodic rodents.     

Genetic and environmental influences on short-day responsiveness in Siberian hamsters (Phodopus sungorus)

Siberian hamsters are photoperiodic rodents that typically exhibit several physiological changes when exposed to a short-day photoperiod. However, development of the winter phenotype in short days is largely conditional on prior photoperiod history: Hamsters that have been reared in an exceptionally long day length (18 L) do not usually exhibit the winter phenotype after transfer to short days, whereas animals reared under "moderately" long days (16 L) are more variable in responsiveness to subsequent short-day exposure, with 20% to 30% generally failing to exhibit winter-type responses. Hamsters reared exclusively in an "intermediate" day length (14 L) are almost uniformly responsive to short photoperiod. In the present study, the authors examine the influence of photoperiod history on short-day responsiveness in a breeding line of hamsters that has been subjected to artificial selection for resistance to the effects of short days. The results demonstrate that photoperiod history is an important determinant of short-day responsiveness in both random-bred (UNS) hamsters and animals artificially selected and bred for nonresponsiveness to short photoperiod (PNR). The PNR hamsters have a reduced requirement for long-day exposure to evoke a state of unresponsiveness to short days. The results are discussed in relation to possible significance for the origin of population and species differences in photoperiod responsiveness.