Short day lengths attenuate the symptoms of infection in Siberian hamsters

Symptoms of infection, such as fever, anorexia and lethargy, are ubiquitous among vertebrates. Rather than nonspecific manifestations of illness, these responses are organized, adaptive strategies that are often critical to host survival. During times of energetic shortage such as winter, however, it may be detrimental for individuals to prolong energetically demanding symptoms such as fever. Individuals may adjust their immune responses prior to winter by using day length to anticipate energetically-demanding conditions. If the expression of sickness behaviours is constrained by energy availability, then cytokine production, fever, and anorexia should be attenuated in infected Siberian hamsters housed under simulated winter photoperiods. We housed hamsters in either long (14 L : 10 D) or short (10 L : 14 D) day lengths and assessed cytokines, anorexia and fever following injections of lipopolysaccharide (LPS). Short days attenuated the response to lipopolysaccharide, by decreasing the production of interleukin (IL)-6 and IL-1beta, and diminishing the duration of fever and anorexia. Short-day exposure in hamsters also decreased the ingestion of dietary iron, a nutrient vital to bacterial replication. Taken together, short day lengths attenuated the symptoms of infection, presumably to optimize energy expenditure and survival outcome.     

Testicular recrudescence in intermediate day lengths reflects loss of photoperiodic memory in Siberian hamsters

Siberian hamsters transferred from a long (16 h light/day [16 L]) to an intermediate (13.5 L) day length (DL) undergo testicular regression within 2 months followed approximately 2 months later by "spontaneous" testicular recrudescence. Recovery of gonadal function after prolonged exposure to intermediate DLs is thought to reflect development of neuroendocrine refractoriness to intermediate-duration melatonin signals. The authors tested the alternative hypothesis that testicular recrudescence in 13.5 L occurs when the "memory" for the 16-L photoperiod fades and hamsters can no longer compare the 13.5-L to the prior 16-L day length. Adult hamsters transferred from 16 L to 13.5 L that underwent testicular involution were either maintained continuously in 13.5 L for 41 weeks or given a supplementary 2-week treatment of 16 L before being returned to 13.5 L. The supplementary treatment was administered either after hamsters had been in 13.5 L for 10 weeks and had involuted testes, or after 24 weeks, when the gonads had undergone recrudescence. The authors found that 16 L treatment administered at week 10 delayed final gonadal recrudescence by approximately 12 weeks; similar 16-L treatment at week 24 induced a second gonadal regression when animals were returned to 13.5 L. The most parsimonious hypothesis to account for these findings is that gonadal recrudescence in intermediate DLs reflects fading of the "memory" for prior long DLs rather than induction of refractoriness to melatonin signals generated in intermediate DLs.     

Simulated natural day lengths synchronize seasonal rhythms of asynchronously born male Siberian hamsters

Photoperiodism research has relied on static day lengths and abrupt transitions between long and short days to characterize the signals that drive seasonal rhythms. To identify ecologically relevant critical day lengths and to test the extent to which naturally changing day lengths synchronize important developmental events, we monitored nine cohorts of male Siberian hamsters (Phodopus sungorus) born every 2 wk from 4 wk before to 12 wk after the summer solstice in a simulated natural photoperiod (SNP). SNP hamsters born from 4 wk before to 2 wk after the solstice underwent rapid somatic and gonadal growth; among those born 4-6 wk after the solstice, some delayed puberty by many weeks, whereas others manifested early puberty. Hamsters born eight or more weeks after the solstice failed to undergo early testicular development. The transition to delayed development occurred at long day lengths, which induce early puberty when presented as static photoperiods. The first animals to delay puberty may do so predominantly on the basis of postnatal decreases in day length, whereas in later cohorts, a comparison of postnatal day length to gestational day length may contribute to arrested development. Despite differences in timing of birth and timing of puberty, autumn gonadal regression and spring gonadal and somatic growth occurred at similar calendar dates in all cohorts. Incrementally changing photoperiods exert a strong organizing effect on seasonal rhythms by providing hamsters with a richer source of environmental timing cues than are available in simple static day lengths.     

Short day lengths alter stress and depressive-like responses, and hippocampal morphology in Siberian hamsters

Many psychological disorders comprise a seasonal component. For instance, seasonal affective disorder (SAD) is characterized by depression during autumn and winter. Because hippocampal atrophy may underlie the symptoms of depression and depressive-like behaviors, one goal of this study was to determine whether short days also induce structural changes in the hippocampus using photoperiod responsive rodents — Siberian hamsters. Exposure to short days increases depressive-like responses (increased immobility in the forced swim test) in hamsters. Male hamsters were housed in either short (LD 8:16) or long days (LD 16:8) for 10 weeks and tested in the forced swim test. Brains were removed and processed for Golgi impregnation. HPA axis function may account for photoperiod-related changes in depressive-like responses. Thus, stress reactivity was assessed in another cohort of photoperiod-manipulated animals. Short days reduced soma size and dendritic complexity in the CA1 region. Photoperiod did not induce gross changes in stress reactivity, but an acute stressor disrupted the typical nocturnal peak in cortisol concentrations. These data reveal that immobility induced by exposure to short days is correlated with reduced CA1 cell complexity (and perhaps connectivity). This study is the first to investigate hippocampal changes in the context of short-day induced immobility and may be relevant for understanding psychological disorders with a seasonal component.     

Short day lengths alter stress and depressive-like responses,and hippocampal morphology in Siberian hamsters

Many psychological disorders comprise a seasonal component. For instance, seasonal affective disorder (SAD) is characterized by depression during autumn and winter. Because hippocampal atrophy may underlie the symptoms of depression and depressive-like behaviors, one goal of this study was to determine whether short days also induce structural changes in the hippocampus using photoperiod responsive rodents — Siberian hamsters. Exposure to short days increases depressive-like responses (increased immobility in the forced swim test) in hamsters. Male hamsters were housed in either short (LD 8:16) or long days (LD 16:8) for 10 weeks and tested in the forced swim test. Brains were removed and processed for Golgi impregnation. HPA axis function may account for photoperiod-related changes in depressive-like responses. Thus, stress reactivity was assessed in another cohort of photoperiod-manipulated animals. Short days reduced soma size and dendritic complexity in the CA1 region. Photoperiod did not induce gross changes in stress reactivity, but an acute stressor disrupted the typical nocturnal peak in cortisol concentrations. These data reveal that immobility induced by exposure to short days is correlated with reduced CA1 cell complexity (and perhaps connectivity). This study is the first to investigate hippocampal changes in the context of short-day induced immobility and may be relevant for understanding psychological disorders with a seasonal component.     

Suppression of kisspeptin expression and gonadotropic axis sensitivity following exposure to inhibitory day lengths in female Siberian hamsters

To avoid breeding during unsuitable environmental or physiological circumstances, the reproductive axis adjusts its output in response to fluctuating internal and external conditions. The ability of the reproductive system to alter its activity appropriately in response to these cues has been well established. However, the means by which reproductively relevant cues are interpreted, integrated and relayed to the reproductive axis remain less well specified. The neuropeptide kisspeptin has been shown to be a potent positive stimulator of the hypothalamo-pituitary-gonadal (HPG) axis, suggesting a possible neural locus for the interpretation/integration of these cues. Because a failure to inhibit reproduction during winter would be maladaptive for short-lived female rodents, female Siberian hamsters (Phodopus sungorus) housed in long and short days were examined. In long "summer" photoperiods, kisspeptin is highly expressed in the anteroventral periventricular nucleus (AVPV), with low expression in the arcuate nucleus (Arc). A striking reversal in this pattern is observed in animals held in short, "winter" photoperiods, with negligible kisspeptin expression in the AVPV and marked staining in the Arc. Although all studies to date suggest that both populations act to stimulate the reproductive axis, these contrasting expression patterns of AVPV and Arc kisspeptin point to disparate roles for these two cell populations. Additionally, we found that the stimulatory actions of exogenous kisspeptin are blocked by acyline, a gonadotropin-releasing hormone (GnRH) receptor antagonist, suggesting an action of kisspeptin on the GnRH system rather than pituitary gonadotropes. Finally, females held in short day lengths exhibit a reduced response to exogenous kisspeptin treatment relative to long-day animals. Together, these findings indicate a role for kisspeptin in the AVPV and Arc as an upstream integration center for reproductively relevant stimuli and point to a dual mechanism of reproductive inhibition in which kisspeptin expression is reduced concomitant with reduced sensitivity of the HPG axis to this peptide.     

Temperature dependence of gonadal regression in Syrian hamsters exposed to short day lengths

We sought to determine whether ambient temperature (T(a)) affects gonadal function by altering the rate at which circadian rhythms entrain to short day lengths. Syrian hamsters were housed in cages where they received 14 h of light per day ("long days," 14L) at 22 degrees C. Hamsters were then transferred to cages to receive 10 h of light per day ("short days," 10L) and kept at 5, 22, or 28 degrees C or were maintained in 14L at 22 degrees C. Body mass and estimated testis volume as well as duration of nocturnal locomotor activity (alpha), previously established as a reliable indicator of the duration of nocturnal melatonin secretion, were determined over the course of 24 wk. Testicular regression in short days was accelerated by 4 wk at 5 degrees C and delayed by 3 wk at 28 degrees C relative to 22 degrees C. The interval between alpha-expansion and initiation of testicular regression was markedly affected by T(a) with delays of 0, 3, and 6 wk at 5, 22, and 28 degrees C, respectively. All hamsters held at 5 and 22 degrees C underwent testicular regression, but 25% of those maintained at 28 degrees C failed to do so. We suggest that T(a) modulates testicular regression primarily by affecting responsiveness of neuroendocrine target tissues to long melatonin signals.     

Differential effects of multiple short day lengths on body weights of gonadectomized siberian hamsters

Siberian hamsters (Phodopus sungorus) maintained under simulated natural photoperiods exhibit marked reductions in body weight as day lengths decrease in summer and fall. This experiment assessed whether the component of the seasonal body weight rhythm that is independent of gonadal hormones exhibits a graded dependence on decreasing day lengths or whether the entire program of weight loss is triggered by the crossing of a single critical day length in late summer. Male hamsters born into a photoperiod with 13 h light and 11 h dark (i.e., 13L : 11D) were castrated and transferred to simulated natural photoperiod for early April at 40 degrees N latitude. At the summer solstice (15L : 9D) some hamsters remained on that photoperiod whereas others experienced gradual decreases in day length. Three additional groups were moved to static photoperiods when day lengths had subsequently declined to 13L : 11D, 11L : 13D, or 9L : 15D, respectively. Day lengths decreasing to 13L : 11D were sufficient to suppress body weight but were less inhibitory than further decreases in day length. Hamsters identified as photononresponsive on the basis of daily activity rhythms increased body weight monotonically. These results establish that steroid-independent modulation of body weight depends on photoperiod in a graded fashion.     

Short day lengths delay development of the SNB neuromuscular system in the Siberian hamster,Phodopus sungorus

The Siberian hamster, Phodopus sungorus, breeds seasonally. In the laboratory, the seasonal breeding can be controlled by photoperiod, which affects the durations of nightly melatonin secretions. Winterlike short day lengths induce gonadal regression in adult animals, and pups born and maintained in short days undergo gonadal development much later than animals born into long days. The spinal nucleus of the bulbocavernosus (SNB) and its target muscles, the bulbocavernosus (BC) and levator ani (LA), comprise a sexually dimorphic, androgen-sensitive neuromuscular system involved in male reproduction. The SNB neuromuscular system was studied in male Siberian hamsters maintained from conception in short-day (8:16 h light/dark cycle) versus long-day (16:8 h light/dark cycle) conditions. At 40–47 days of age, development of three components of the SNB neuromuscular system were all significantly delayed in hamsters raised in the short photoperiod: BC/LA muscle weight, the size of SNB motoneuronal somata, and the area of the neuromuscular junctions at the BC/LA muscles of short-day hamsters were each significantly reduced relative to those of long-day counterparts. Thus, development of the SNB reproductive system is delayed under short day lengths in this species. © 1998 John Wiley & Sons, Inc. J Neurobiol 35: 355–360, 1998     

Housing condition alters immunological and reproductive responses to day length in Siberian hamsters (Phodopus sungorus)

During winter, increased thermoregulatory demands coincide with limited food availability necessitating physiological tradeoffs among expensive physiological processes resulting in seasonal breeding among small mammals. In the laboratory, short winter-like day lengths induce regression of the reproductive tract, but also enhance many aspects of immune function. It remains unspecified the extent to which bolstered immune responses in short days represent enhanced immune function per se compared to long days or represents energetic disinhibition mediated by the regression of the reproductive tract. Cohabitation of male Siberian hamsters with intact female conspecifics can block short-day reproductive regression. We sought to determine whether female cohabitation could also block the enhanced immune function associated with short days. Adult male Siberian hamsters were housed in long or short day lengths in one of three housing conditions: (1) single-housed, (2) housed with a same sex littermate, or (3) housed with an ovariectomized female. Delayed-type hypersensitivity (DTH) responses were assessed after 8 weeks of photoperiod treatment. Housing with an ovariectomized female was not sufficient to block short-day reproductive regression, but prevented short-day enhancement of DTH responses. Housing with a male littermate did not alter reproductive or immune responses in either photoperiod. These data suggest that short day enhancement of immune function is independent of photoperiod-mediated changes in the reproductive system.     

Short day lengths affect perinatal development of the male reproductive system in the Siberian hamster, Phodopus sungorus.

The Siberian hamster, Phodopus sungorus, breeds seasonally. In the laboratory, seasonal breeding can be controlled by photoperiod, which affects the duration of nightly melatonin secretion. Winterlike, short day lengths induce gonadal regression in adult animals, and pups born and maintained in short days undergo pubertal gonadal development later than animals born into long days. However, to date there have been no reports of gestational photoperiod affecting fetal development of reproductive systems. The spinal nucleus of the bulbocavernosus (SNB) and its target muscles, the bulbocavernosus (BC) and levator ani (LA), compose a sexually dimorphic, androgen-sensitive neuromuscular system involved in male reproduction. The SNB neuromuscular system was studied in male Siberian hamsters maintained from conception in short-day (8 h light, 16 h dark; 8L:16D) versus long-day (16L:8D) conditions. On the day of birth, and at postnatal (PN) days 2 and 18, the BC/LA muscles of hamsters gestated and raised in the short photoperiod were significantly reduced relative to those of their long-day counterparts. Testes weights were not significantly different between groups until day 18. Thus, photoperiod exposure during gestation and after birth affects perinatal development of the SNB system in this species, and these effects can be seen as early as the day of birth. Because photoperiod did not significantly affect testes weights until PN18, these results suggest that either perinatal photoperiod affects fetal androgen production without affecting testes weight or it influences BC/LA development independently from androgen.     

Winter day lengths counteract stimulatory effects of apomorphine and yohimbine on sexual behavior of male Syrian hamsters

Yohimbine and apomorphine selectively act on noradrenergic and dopaminergic neural substrates to augment male sexual behavior (MSB) in several rodent species. The present study assessed whether these drugs can overcome the suppressive effects of short winter-like day lengths on MSB. Yohimbine treatments that markedly increase copulatory behavior of male hamsters in long days were completely ineffective in facilitating MSB when injected after gonadal regression induced by 16 wks of short day lengths and after complete gonadal recrudescence after 32 wks of short days; apomorphine was similarly ineffective. The brain circuit that mediates MSB either may be less responsive to yohimbine and apomorphine in short than long days, or these drugs may not produce equivalent neurotransmitter changes in the two day lengths. After 32 wks of short-day treatment, all males had undergone testicular recrudescence and successfully ejaculated on initial tests with sexually receptive females after a hiatus of at least 4 mo during which they were denied mating opportunities. This suggests that overwintering males in the field are in a state of reproductive readiness at the outset of spring conditions favorable for survival of offspring.     

Exogenous insulin enhances humoural immune responses in short-day,but not long-day,Siberian hamsters (Phodopus sungorus)

Many animals experience marked seasonal fluctuations in environmental conditions. In response, animals display adaptive alterations in physiology and behaviour, including seasonal changes in immune function. During winter, animals must reallocate finite energy stores from relatively costly, less exigent systems (e.g. reproduction and immunity) to systems critical for immediate survival (e.g. thermoregulation). Seasonal changes in immunity are probably mediated by neuroendocrine factors signalling current energetic state. One potential hormonal candidate is insulin, a metabolic hormone released in response to elevated blood glucose levels. The aim of the present study was to explore the potential role of insulin in signalling energy status to the immune system in a seasonally breeding animal, the Siberian hamster (Phodopus sungorus). Specifically, exogenous insulin was administered to male hamsters housed in either long ‘summer-like’ or short ‘winter-like’ days. Animals were then challenged with an innocuous antigen and immune responses were measured. Insulin treatment significantly enhanced humoural immune responses in short, but not long days. In addition, insulin treatment increased food intake and decreased blood glucose levels across photoperiodic treatments. Collectively, these data support the hypothesis that insulin acts as an endocrine signal integrating seasonal energetic changes and immune responses in seasonally breeding rodents.     

Decrease of food intake by MC4-R agonist MTII in Siberian hamsters in long and short photoperiods

We investigated the role of the hypothalamic melanocortin system in the regulation of food intake in the Siberian hamster, which shows a profound seasonal decrease in food intake and body weight in short photoperiod (SP). In male hamsters maintained in long photoperiod (LP), intracerebroventricular injection of melanotan II (MTII) just before lights off significantly decreased food intake relative to vehicle treatment over the 6-h observation period. Similar effects were observed in age-matched hamsters after exposure to a short daylength for 9 wk, when body weight had significantly decreased. There was no clear difference in either the magnitude of response or the dose required for half-maximal inhibition of food intake in hamsters in SP compared with those in LP. MTII significantly increased grooming in both LP and SP. Our results indicate that the melanocortin system is a potent short-term regulator of food intake. However, the lack of differential response or sensitivity to MTII treatment in the obese (LP) vs. lean (SP) states does not support the hypothesis that changes in this melanocortin pathway underlie the long-term decrease in food intake that occurs in this seasonal model.     

Homeostatic regulation of sleep in arrhythmic Siberian hamsters

Sleep is regulated by independent yet interacting circadian and homeostatic processes. The present study used a novel approach to study sleep homeostasis in the absence of circadian influences by exposing Siberian hamsters to a simple phase delay of the photocycle to make them arrhythmic. Because these hamsters lacked any circadian organization, their sleep homeostasis could be studied in the absence of circadian interactions. Control animals retained circadian rhythmicity after the phase shift and re-entrained to the phase-shifted photocycle. These animals displayed robust daily sleep-wake rhythms with consolidated sleep during the light phase beginning about 1 h after light onset. This marked sleep-wake pattern was circadian in that it persisted in constant darkness. The distribution of sleep in the arrhythmic hamsters over 24 h was similar to that in the light phase of rhythmic animals. Therefore, daily sleep amounts were higher in arrhythmic animals compared with rhythmic ones. During 2- and 6-h sleep deprivations (SD), it was more difficult to keep arrhythmic hamsters awake than it was for rhythmic hamsters. Because the arrhythmic animals obtained more non-rapid eye movement sleep (NREMS) during the SD, they showed a diminished compensatory response in NREMS EEG slow-wave activity during recovery sleep. When amounts of sleep during the SD were taken into account, there were no differences in sleep homeostasis between experimental and control hamsters. Thus loss of circadian control did not alter the homeostatic response to SD. This supports the view that circadian and homeostatic influences on sleep regulation are independent processes.     

Sustained reproductive responses in Djungarian hamsters (Phodopus sungorus) exposed to a single long day

Male and female Djungarian hamsters maintained from birth in a short photoperiod (8 h light per day; 8L:16D) showed substantial testicular and uterine growth in response to a single long photoperiod or a 15-min light pulse that interrupted the 16-h dark period at 18 days of age. These light regimens resulted in heavier testes and uteri at 30 and 35 days of age when compared with those of control animals. Similar results were obtained in hamsters maintained from birth to Day 18 in a long photoperiod (16L:8D), given a single longer day (20L:4D) or constant light on Day 18 and then transferred to a short photoperiod (8L:16D) on Day 19. At 35 days of age animals that received extended light treatment on Day 18 had significantly more developed reproductive structures than did control hamsters. The marked effects of brief light treatment in producing long-term changes in the reproductive axis provide a convenient mammalian model system in which to study neuroendocrine events that underlie photoperiodism.     

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.     

Photoperiod-peptide interactions in the energy intake of Siberian hamsters

Siberian hamsters (Phodopus sungorous sungorous) decrease their food intake when exposed to short (“winter-like”) photoperiods. The cause of this naturally-occurring hypophagia is unknown, but it may be due to a heightened sensitivity to the factors that normally terminate food intake in long photoperiods, such as the putative satiety peptides. The purpose of the present investigation was to test whether there would be an enhanced sensitivity to the inhibitory effects of some of these peptides on food intake in short relative to long days. Ad lib-fed, adult female Siberian hamsters were housed in a long photoperiod (LD 14:10) and injected with bombesin, glucagon, cholecystokinin octapeptide (CCK-8) and calcitonin (CT). Food intake was monitored 1, 2, 4, 6, and 24 hr post-injection. Bombesin and glucagon had no effect on food intake in long day-housed hamsters. CCK-8 and CT inhibited food intake; however, CCK-8 did so without any apparent behavioral disruption, while CT produced a marked and prolonged depression of behavior. After 10 weeks of exposure to a short photoperiod (LD 8:16) the hamsters were tested again. The previously ineffective dose of bombesin greatly inhibited food intake following short photoperiod exposure. In addition, an increased inhibition of food intake by CCK-8 was also found. In contrast, glucagon did not decrease food intake and CT still produced its non-specific, behaviorally disruptive effects. To our knowledge, this is the first demonstration that the effectiveness of a putative satiety peptide can be dependent upon a change in the photoperiod. This heightened responsiveness of short photoperiod-exposed Siberian hamsters to the inhibitory effects of bombesin and cholecystokinin may account for the reduction in food intake that accompanies short day exposure in this species.     

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.