Role of area postrema in control of torpor in Siberian hamsters

Siberian hamsters undergo torpor during the short days of winter and in response to glucoprivation or food restriction. We tested whether the area postrema and the adjacent nucleus of the solitary tract (hereafter the AP), which monitor metabolic fuel availability, also control the onset of torpor. Siberian hamsters that had manifested torpor spontaneously or had entered torpor in response to 2-deoxy-D-glucose (2-DG) treatment were subjected to area postrema ablations (APx). Hamsters continued to display torpor postoperatively; most features of torpor were unaffected by APx. The AP is not necessary for expression of torpor elicited by short day lengths or metabolic challenge. In contrast, decreases in food intake manifested by hamsters treated with 2-DG were counteracted by APx. In Siberian hamsters, the AP appears to mediate effects of 2-DG on food intake but not torpor.     

Melatonin production accompanies arousal from daily torpor in Siberian hamsters

Arousal from deep hibernation is accompanied by a transient rise of melatonin (Mel) in circulation; there are no comparable analyses of Mel concentrations in species that undergo much shallower, shorter duration episodes of daily torpor. Serum Mel concentrations were determined during arousal from both natural daily torpor and torpor induced by 2-deoxy-D-glucose (2-DG) treatment (2,500 mg/kg, intraperitoneal [IP]); blood samples were drawn from the retro-orbital sinus of anesthetized Siberian hamsters. For animals kept in darkness during torpor, Mel concentrations were highest during early arousal when thermogenesis is maximal, and they decreased as body temperature increased during arousal and returned to baseline once euthermia was reestablished. In hamsters kept in the light during the torpor bout, Mel concentrations were elevated above basal values during arousal, but the response was significantly blunted in comparison with values recorded in darkness. Increased Mel concentrations were detected in hamsters only during arousal from torpor (either natural or 2-DG induced) and were not simply a result of the drug treatment; hamsters that remained euthermic or manifested mild hypothermia after drug treatment maintained basal Mel concentrations. We propose that increased Mel production may reflect enhanced sympathetic activation associated with intense thermogenesis during arousal from torpor rather than an adjustment of the circadian rhythm of Mel secretion.     

Juvenile Siberian hamsters display torpor and modified locomotor activity and body temperature rhythms in response to reduced food availability

Siberian hamsters as young as 16 and 28 d displayed torpor in response to treatment with 2,500 mg/kg 2-deoxy-D-glucose and reduced food availability, respectively. In addition, most food-restricted hamsters displayed increased locomotor activity and elevated body temperatures in the 3 h immediately preceding daily food delivery. This anticipatory activity disappeared within a few days of reimposition of ad lib. feeding. Torpor first appeared spontaneously at approximately 13 wk of age in hamsters fed ad lib. and maintained in short day lengths. The onset of this "spontaneous" torpor was unaffected by the hamsters' history of food restriction before age 2 mo. Siberian hamsters born late in the breeding season can conserve energy by undergoing torpor immediately after weaning when they contend with food shortages and concurrent energetic challenges imposed by growth requirements and low ambient temperatures.     

Feeding schedule controls circadian timing of daily torpor in SCN-ablated Siberian hamsters

Timing of daily torpor was assessed in suprachiasmatic nucleus-ablated (SCNx) and sham-ablated Siberian hamsters fed restricted amounts of food each day either in the light or dark phase of a 14:10 light-dark cycle. Eighty-five percent of sham-ablated and 45% of SCNx hamsters displayed a preferred hour for torpor onset. In each group, time of torpor onset was not random but occurred at a mean hour that differed significantly from chance. Time of food presentation almost completely accounted for the timing of torpor onset in SCNx animals and significantly affected timing of this behavior in intact hamsters. These results suggest that the circadian pacemaker in the SCN controls the time of torpor onset indirectly by affecting timing of food intake, rather than by, or in addition to, direct neural and humoral outputs to relevant target tissues.     

Monosodium glutamate-induced arcuate nucleus damage affects both natural torpor and 2DG-induced torpor-like hypothermia in Siberian hamsters

Siberian hamsters (Phodopus sungorus) have the ability to express daily torpor and decrease their body temperature to approximately 15 degrees C, providing a significant savings in energy expenditure. Daily torpor in hamsters is cued by winterlike photoperiods and occurs coincident with the annual nadirs in body fat reserves and chronic leptin concentrations. To better understand the neural mechanisms underlying torpor, Siberian hamster pups were postnatally treated with saline or MSG to ablate arcuate nucleus neurons that likely possess leptin receptors. Body temperature was studied telemetrically in cold-acclimated (10 degrees C) male and female hamsters moved to a winterlike photoperiod (10:14-h light-dark cycle) (experiments 1 and 2) or that remained in a summerlike photoperiod (14:10-h light-dark cycle) (experiment 3). In experiment 1, even though other photoperiodic responses persisted, MSG-induced arcuate nucleus ablations prevented the photoperiod-dependent torpor observed in saline-treated Siberian hamsters. MSG-treated hamsters tended to possess greater fat reserves. To determine whether reductions in body fat would increase frequency of photoperiod-induced torpor after MSG treatment, hamsters underwent 2 wk of food restriction (70% of ad libitum) in experiment 2. Although food restriction did increase the frequency of torpor in both MSG- and saline-treated hamsters, it failed to normalize the proportion of MSG-treated hamsters undergoing photoperiod-dependent torpor. In experiment 3, postnatal MSG treatments reduced the proportion of hamsters entering 2DG-induced torpor-like hypothermia by approximately 50% compared with saline-treated hamsters (38 vs. 72%). In those MSG-treated hamsters that did become hypothermic, their minimum temperature during hypothermia was significantly greater than comparable saline-treated hamsters. We conclude that 1) arcuate nucleus mechanisms mediate photoperiod-induced torpor, 2) food-restriction-induced torpor may also be reduced by MSG treatments, and 3) arcuate nucleus neurons make an important, albeit partial, contribution to 2DG-induced torpor-like hypothermia.     

Short-day increases in aggression are inversely related to circulating testosterone concentrations in male Siberian hamsters (Phodopus sungorus)

Many nontropical rodent species display seasonal changes in both physiology and behavior that occur primarily in response to changes in photoperiod. Short-day reductions in reproduction are due, in part, to reductions in gonadal steroid hormones. In addition, gonadal steroids, primarily testosterone (T), have been implicated in aggression in many mammalian species. Some species, however, display increased aggression in short days despite basal circulating concentrations of T. The goal of the present studies was to test the effects of photoperiod on aggression in male Siberian hamsters (Phodopus sungorus) and to determine the role of T in mediating photoperiodic changes in aggression. In Experiment 1, hamsters were housed in long and short days for either 10 or 20 weeks and aggression was determined using a resident-intruder model. Hamsters housed in short days for 10 weeks underwent gonadal regression and displayed increased aggression compared to long-day-housed animals. Prolonged maintenance in short days (i.e., 20 weeks), however, led to gonadal recrudescence and reduced aggression. In Experiment 2, hamsters were housed in long and short days for 10 weeks. Half of the short-day-housed animals were implanted with capsules containing T whereas the remaining animals received empty capsules. In addition, half of the long-day-housed animals were castrated whereas the remaining animals received sham surgeries. Short-day control hamsters displayed increased aggression compared to either castrated or intact long-day-housed animals. Short-day-housed T treated hamsters, however, did not differ in aggression from long-day-housed animals. Collectively, these results confirm previous findings of increased aggression in short-day-housed hamsters and suggest that short-day-induced increases in aggression are inversely related to gonadal steroid hormones.     

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.     

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.     

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.     

Short-day increases in aggression are independent of circulating gonadal steroids in female Siberian hamsters (Phodopus sungorus)

Among the suite of adaptations displayed by seasonally-breeding rodents, individuals of most species display reproductive regression and concomitant decreases in gonadal steroids during the winter. In addition, some species display increased aggression in short "winter-like" days compared with long "summer-like" day lengths. For example, male Syrian and Siberian hamsters held in short days express heightened levels of aggression that are independent of gonadal steroids. Virtually nothing is known, however, regarding seasonal aggression in female Siberian hamsters (Phodopus sungorus). Studies were undertaken to determine female levels of aggression in long and short days as well as the role of gonadal steroids in mediating this behavior. In Experiment 1, females were housed in long or short days for 10 weeks and resident-intruder aggression was assessed. Prior to testing, estrous cycle stages were determined by vaginal cytology and females were tested during both Diestrus I and Proestrus. In Experiment 2, hormone levels were experimentally manipulated; long-day females were ovariectomized (OVx) or given sham surgeries whereas short-day females were implanted with capsules containing 17beta-estradiol (E(2)) or Progesterone (P). In Experiment 3, both long- and short-day females were ovariectomized and implanted with either an exogenous E(2) or blank capsule, or given a sham surgery. Short-day hamsters displayed increased aggression relative to long-day females. Aggression was not affected by estrous stage. There was no difference in aggression between long-day OVx and sham animals. Furthermore, neither exogenous E(2) nor P had any significant effect on aggression. These results support previous findings of increased non-breeding aggression and suggest that short-day aggression is not likely mediated by circulating levels of gonadal steroids. These results also suggest that the endocrine regulation of seasonal aggression may be similar between the sexes.     

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.     

Role of short photoperiod and cold exposure in regulating daily torpor in Djungarian hamsters

1. Male and female Djungarian hamsters (Phodopus sungorus) were gonadectomized or sham-operated after 12 weeks of exposure to short photoperiods (10L:14D). Half of the animals were single housed and transferred to a cold environment (7 degrees C) at week 13 of short days and half were transferred to cold at week 21. The time courses of short photoperiod induced seasonal changes in body weight, pelage color stage, and daily torpor were monitored periodically until the experiment was terminated after 34 weeks of short days. 2. The total duration of short photoperiod exposure was of primary importance compared to the duration of cold exposure in regulating seasonal changes in the frequency of daily torpor, body weight and pelage color exhibited by male and female Djungarian hamsters; that is, the change from long to short days was much more effective as a seasonal time cue than was the onset of cold exposure. 3. Gonadectomy did not prevent the occurrence of seasonal torpor in hamsters of either sex, indicating that these cycles are regulated by a time measuring mechanism (seasonal clock) that is largely independent of the gonadal cycle. However, castration did influence certain aspects of the body weight and torpor cycles exhibited by male hamsters. 4. Some castrated animals showed a delay in terminating the torpor season lending further support to the hypothesis that the spontaneous recrudescence of the testes which occurs toward the end of the torpor season may play a role in the termination of torpor in males.(ABSTRACT TRUNCATED AT 250 WORDS)     

Daily torpor is associated with telomere length change over winter in Djungarian hamsters

Ageing can progress at different rates according to an individual's physiological state. Natural hypothermia, including torpor and hibernation, is a common adaptation of small mammals to survive intermittent or seasonal declines in environmental conditions. In addition to allowing energy savings, hypothermia and torpor have been associated with retarded ageing and increased longevity. We tested the hypothesis that torpor use slows ageing by measuring changes in the relative telomere length (RTL) of Djungarian hamsters, Phodopus sungorus, a highly seasonal rodent using spontaneous daily torpor, over 180 days of exposure to a short-day photoperiod and warm (approx. 20°C) or cold (approx. 9°C) air temperatures. Multi-model inference showed that change in RTL within individuals was best explained by positive effects of frequency of torpor use, particularly at low body temperatures, as well as the change in body mass and initial RTL. Telomere dynamics have been linked to future survival and proposed as an index of rates of biological ageing. Our results therefore support the hypothesis that daily torpor is associated with physiological changes that increase somatic maintenance and slow the processes of ageing.     

Aggressive encounters differentially affect serum dehydroepiandrosterone and testosterone concentrations in male Siberian hamsters (Phodopus sungorus)

The gonadal hormone testosterone (T) regulates aggression across a wide range of vertebrate species. Recent evidence suggests that the adrenal prohormone dehydroepiandrosterone (DHEA) may also play an important role in regulating aggression. DHEA can be converted into active sex steroids, such as T and estradiol (E₂), within the brain. Previous studies show that circulating DHEA levels display diurnal rhythms and that melatonin increases adrenal DHEA secretion in vitro. Here we examined serum DHEA and T levels in long-day housed Siberian hamsters (Phodopus sungorus), a nocturnal species in which melatonin treatment increases aggression. In Experiment 1, serum DHEA and T levels were measured in adult male hamsters during the day (1200 h, noon) and night (2400 h, midnight). In Experiment 2, aggression was elicited using 5-min resident–intruder trials during the day (1800 h) and night (2000 h) (lights-off at 2000 h). Serum DHEA and T levels were measured 24 h before and immediately after aggressive encounters. In Experiment 1, there was no significant difference in serum DHEA or T levels between noon and midnight, although DHEA levels showed a trend to be lower at midnight. In Experiment 2, territorial aggression was greater during the night than the day. Moreover, at night, aggressive interactions rapidly decreased serum DHEA levels but increased serum T levels. In contrast, aggressive interactions during the day did not affect serum DHEA or T levels. These data suggest that nocturnal aggressive encounters rapidly increase conversion of DHEA to T and that melatonin may play a permissive role in this process.     

Exogenous T3 mimics long day lengths in Siberian hamsters

Siberian hamsters (Phodopus sungorus) exhibit seasonal cycles of reproduction driven by changes in day length. Day length is encoded endogenously by the duration of nocturnal melatonin (Mel) secretion from the pineal gland. Short-duration Mel signals stimulate reproduction and long-duration signals inhibit reproduction. The mechanism by which Mel signals are decoded at the level of neural target tissues remains uncharacterized. In Siberian hamsters, exposure to short day lengths or injections of Mel in long days results in a decrease in hypothalamic expression of type 2 iodothyronine deiodinase (Dio2) mRNA. Dio2 catalyzes the conversion of the thyroid hormone thyroxine to triiodothyronine (T3). Thus exposure to short and long day lengths should decrease and increase hypothalamic T3 concentrations, respectively. We tested the hypothesis that exogenous T3 administered to short-day hamsters would mimic exposure to long day lengths with respect to gonadal stimulation. Hamsters gestated and raised in short day lengths that exhibited photoinhibition of the testes were given daily subutaneous injections of T3 or saline vehicle for 4 wk beginning at week 12 of life. The results indicate that exogenous T3 induced gonadal growth in short-day hamsters and delayed spontaneous gonadal development by an interval equal to the number of weeks during which T3 was administered. T3 injections delayed gonadal regression if given coincident with the transfer of hamsters from long to short day lengths. These results suggest that T3 mimics long day exposure in Siberian hamsters and may serve as an intermediate step between the Mel rhythm and the reproductive response.     

Timing of torpor bouts during hibernation in European hamsters (Cricetus cricetus L.)

Body temperature (T _b) of seven European hamsters maintained at constant ambient temperature (T _a = 8 °C) and constant photoperiod (LD 8:16) was recorded throughout the hibernating season using intraperitoneal temperature-sensitive HF transmitters. The animals spent about 30% of the hibernation season in hypothermia and 70% in inter-bout normothermy. Three types of hypothermia, namely deep hibernation bouts (DHBs), short hibernation bouts (SHBs), and short and shallow hibernation bouts (SSHBs), were distinguished by differences in bout duration and minimal body temperature (T _m). A gradual development of SSHBs from the diel minimum of T _b during normothermy could be seen in individual hamsters, suggesting a stepwise decrease of the homeostatic setpoint of T _b regulation during the early hibernation season. Entry into hibernation followed a 24-h rhythm occurring at preferred times of the day in all three types of hypothermia. DHBs and SHBs were initiated approximately 4 h before SSHBs, indicating a general difference in the physiological initiation of SSHBs on the one hand and DHBs and SHBs on the other. Arousals from SHBs and SSHBs also followed a 24-h rhythm, whereas spontaneous arousals from DHBs were widely scattered across day and night. Statistical analyses of bout length and the interval between arousals revealed evidence for a free-running circadian rhythm underlying the timing of arousals. The results clearly demonstrate that entries into hypothermia are linked to the light/dark-cycle. However, the role of the circadian system in the timing of arousals from DHBs remains unclear. Accepted: 11 December 1996     

Photoperiodic regulation of the orexigenic effects of ghrelin in Siberian hamsters

Animals living in temperate climates with predictable seasonal changes in food availability may use seasonal information to engage different metabolic strategies. Siberian hamsters decrease costs of thermoregulation during winter by reducing food intake and body mass in response to decreasing or short-day lengths (SD). These experiments examined whether SD reduction in food intake in hamsters is driven, at least in part, by altered behavioral responses to ghrelin, a gut-derived orexigenic peptide which induces food intake via NPY-dependent mechanisms. Relative to hamsters housed in long-day (LD) photoperiods, SD hamsters consumed less food in response to i.p. treatment with ghrelin across a range of doses from 0.03 to 3 mg/kg. To determine whether changes in photoperiod alter behavioral responses to ghrelin-induced activation of NPY neurons, c-Fos and NPY expression were quantified in the arcuate nucleus (ARC) via double-label fluorescent immunocytochemistry following i.p. treatment with 0.3 mg/kg ghrelin or saline. Ghrelin induced c-Fos immunoreactivity (-ir) in a greater proportion of NPY-ir neurons of LD relative to SD hamsters. In addition, following ghrelin treatment, a greater proportion of ARC c-Fos-ir neurons were identifiable as NPY-ir in LD relative to SD hamsters. Changes in day length markedly alter the behavioral response to ghrelin. The data also identify photoperiod-induced changes in the ability of ghrelin to activate ARC NPY neurons as a possible mechanism by which changes in day length alter food intake.     

Maternal transfer of photoperiodic information in Siberian hamsters. V. Effects of melatonin implants are dependent on photoperiod.

Photoperiodic information is transferred from female Siberian hamsters to their fetuses during gestation. Although maternal melatonin is known to be essential for the transfer of prenatal photoperiodic information, its specific role is not well defined. The duration of the daily melatonin signal, expressed as an elevation of serum melatonin levels in the maternal circulation, has been hypothesized to convey day length information to the fetus. If this hypothesis is valid, it predicts that identical maternal melatonin signals should affect the fetuses identically, regardless of the prenatal photoperiod. To test this hypothesis, adult females received melatonin in beeswax or beeswax alone. They were paired with males and housed in photoperiods of 12L:12D or 16L:8D. On the day of parturition, mother and young were transferred to constant light (LL). Young males were killed on Day 28 of life, and weights of testes were determined. Prenatal treatment with beeswax alone did not affect the nature of the signal transferred from mother to fetus; young gestated in 12L:12D and reared in LL developed small testes, while those gestated in 16L:8D had large testes. On the other hand, the effect of the prenatal melatonin treatment on postnatal testicular development in LL was inversely dependent on the prenatal photoperiod: testicular growth was stimulated in young gestated in 12L:12D, but inhibited in young gestated in 16L:8D. To verify that the melatonin pellets produced equivalent serum melatonin levels in adult females in 12L:12D and 16L:8D, unmated adult females were killed 6-10 wk after receiving melatonin pellets. Serum levels were elevated in both groups throughout the day and night.(ABSTRACT TRUNCATED AT 250 WORDS)