Bruce D. Goldman

The Pineal Gland and Mammalian Photoperiodism

The mammalian pineal gland appears to be a major endocrine component in the regulation of photoperiodic responses. The circadian pattern of secretion of the pineal hormone, melatonin, is regulated by the nervous system. Changes in photoperiod, acting via the nervous system, alter the temporal pattern of melatonin secretion. The changes in secretion pattern convey information about daylength from neural components of the circadian system to the reproductive system, and probably to other physiological systems.

Circadian Regulation of Pineal Melatonin and Reproduction in the Djungarian Hamster

Gonadal state, pineal melatonin rhythms, and locomotor activity rhythms were examined in juvenile male Djungarian hamsters exposed to non-24-hr light cycles (T-cycles) or to full photoperiods. At the end of 1 month, hamsters exposed to a 1-hr pulse of light every 24.33 hr (T 24.33) exhibited small testes, whereas those receiving the same amount of light every 24.78 hr (T 24.78) displayed stimulated gonads, ten-fold larger in size. Accompanying the nonstimulatory effect of the T 24.33 cycle were nocturnal peaks in both pineal melatonin content and serum melatonin concentration which were longer by approximately 4 hr than those observed on the photostimulatory T 24.78 cycle. Exposure to an intermediate-length T-cycle (T 24.53) resulted in a mixed gonadal response and in pineal and serum melatonin peaks of intermediate duration. Wheel-running activity was entrained to the T-cycles such that light was present only near the beginning of the subjective night, its phase (relative to activity onset) differing only slightly among T-cycle groups. Hence the durational differences observed in the melatonin peaks were apparently not due to the acute suppressive or phase-advancing effects of morning light on melatonin biosynthesis, but were rather the result of differences in the endogenous control of pineal activity by the circadian pacemaker system. While no strong correlation was detected between gonadal state and the phase of locomotor activity onset relative to the light pulse, a significant correlation was observed between gonadal state and the duration of daily locomotor activity (alpha). These data were compared to similar measures obtained from hamsters exposed to long-versus short-day full photoperiods (LD 16:8 vs. LD 10:14). In summary, the results of this study indicate involvement of the circadian pacemaker system of Djungarian hamsters in the control of pineal melatonin synthesis and secretion, and in photoperiodic time measurement. Furthermore, these data strengthen the hypothesis that it is the duration of nocturnal pineal melatonin secretion that is the critical feature of this neuroendocrine glands photoperiodic signal.

Photoperiodism and Seasonality in Hamsters: Role of the Pineal Gland

During the past two decades, a large body of evidence has been accumulated to indicate a central role for the pineal gland in the regulation of photoperiodic responses in mammals (Goldman and Darrow 1983). Most of this evidence has come from studies of the effects of pinealectomy on the reproductive system in photoperiodic mammals. The Syrian hamster has been the most intensively studied of these species, and frequently has been presented as a “model” for the role of the pineal in regulating reproductive activity. This species is a long-day breeder and exhibits gonadal regression following several weeks of exposure to short days—i.e., daylengths of less than 12.5-h illumination/24-h cycle (Elliott 1976). Removal of the pineal completely prevents this response to short-day exposure; pinealectomized Syrian hamsters remain reproductively active under all photoperiodic conditions (Reiter 1969, Reiter 1974). The photoperiod dependency of the response to pinealectomy in this species has been emphasized. In long days, pinealectomized and intact Syrian hamsters show identical levels of reproductive activity; the effect of pinealectomy becomes apparent only during exposure to short days (Reiter 1974). The closely related Turkish hamster is also a long-day breeder and requires daylengths of nearly 16 h to stimulate reproductive activity (Hong et al. 1986). Pinealectomy also has a photoperiod-dependent effect on reproductive activity in this species, but the nature of the response to pinealectomy is almost the reverse of that seen in Syrian hamsters. In Turkish hamsters, pinealectomy actually triggers testicular regression in long-day-housed animals; short-day-exposed Turkish hamsters exhibit gonadal regression regardless of whether or not they have been pinealectomized (Carter et al. 1982).

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

Summary1.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 °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 (Figs. 1–3); 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 (Figs. 1–2) 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. The seasonal body weight gain was diminished in castrate as compared to testis-intact hamsters (Fig. 3).5.The frequency of daily torpor was lower in females as compared to males (Figs. 1–2) and was not significantly changed by ovariectomy. The latter result suggests that the annual gonadal cycle has less influence on the torpor season in females than in males.

Effect of Melatonin Infusion Duration and Frequency on Gonad, Lipid, and Body Mass in Pinealectomized Male Siberian Hamsters1

The goal of this study was to discriminate between two hypotheses regarding how the circadian rhythm of pineal melatonin (MEL) production transmits photoperiodic informa tion : (1) A circadian rhythm of sensitivity to MEL regulates the hormones effect; (2) the duration of the MEL signal, rather than its circadian timing, is the critical parameter of the MEL rhythm. The experiment examined the response of pinealectomized (PINX) male Sibe rian hamsters to 10-hr (short-day-type) versus 6-hr (long-day-type) duration MEL infusions (10 ng/infusion) in cycles with period lengths (T) of 18, 24, 36, and 48 hr. After cannula implantation, animals were moved from LD 16:8 to LD 10:14 (lights-on from 0500 to 1500 hr, EST), where the timed infusions began. Additional T 24 cycles included as controls employed 18-hr MEL, 18-hr saline (SAL), and 10-hr SAL infusions. Body weight and food intake were measured weekly. After 6 weeks, animals were killed; blood samples were taken for radio immunoassay (RIA) of serum follicle-stimulating hormone (FSH) and prolactin (PRL); and terminal body, epididymal white adipose tissue (EPIWAT), and paired testis weights were recorded. Six-hour MEL infusions failed to induce short-day-type effects, regardless of the period (T) of the infusion cycle. In contrast, compared to SAL and 6-hr MEL infusions, 10-hr MEL resulted in decreases in body, EPIWAT, and testis weights in T 24, but not in T 36 or T 48. In T 18, testis, body, and EPIWAT mass were decreased, but not to the same extent as in T 24. Similarly, daily 18-hr MEL infusions (T 24) were less effective as a short-day stimulus than were 10-hr MEL infusions. The effectiveness of 10-hr, but not 6-hr, MEL infusions in T 18 and T 24 is consistent with the duration hypothesis and argues against the circadian hypothesis. Neither hypothesis could have predicted that all infusion cycles of T ≥ 36 hr, regardless of the infusion durations, would fail to elicit short-day-type responses. This out come suggests a need for relatively frequent (T < 36 hr) MEL stimulation in addition to the requirement for adequate duration of each MEL infusion.

Influence of photoperiod and gonadal steroids on hibernation in the European hamster

SummaryTorpor was monitored daily in adult male and female European hamsters (Cricetus cricetus) induced to hibernate by exposure to a cold environment (6 °C). The effect of photoperiodic manipulations or administration of exogenous gonadal steroids was examined in gonadectomized or intact hamsters.1.Gonadal regression occurred in all short day, but only in some long day, cold-exposed hamsters. Entry into hibernation was not observed until reproductive regression had occurred. Thus, gonadal atrophy appears to be a necessary precondition for hibernation.2.Castrated hamsters in the short day cold condition showed a significantly greater incidence of torpor than those in the long day cold condition. Hence, photoperiod affected torpor independently of its effect on the gonadal cycle.3.Testosterone, when administered via silastic capsules at near physiological levels, completely inhibited torpor in gonadectomized male and female hamsters hibernating in the short day cold condition.4.In ovariectomized females, torpor was unaffected by progesterone treatment, but partially inhibited by estradiol. A greater inhibition of torpor was observed when estradiol-primed females were administered both estradiol and progesterone simultaneously. Thus, the effect of both hormones may be functionally comparable to that of the single testicular hormone.5.Estradiol inhibited torpor to a greater extent in intact and ovariectomized female hamsters hibernating in long days than those in short days, suggesting an effect of photoperiod on responsiveness to estradiol.nThese results indicate an inverse relationship between the gonadal and hibernation cycles, and a probable role for gonadal steroids to influence the timing of the hibernation season. However, non-gonadal factors must also be involved in controlling hibernation, since photoperiod affected the incidence of torpor in gonadectomized animals and because hamsters were able to terminate hibernation in the absence of gonadal hormones.

Male hamster investigatory and copulatory responses to vaginal discharge: Relationship to the endocrine status of females

The ability of vaginal discharge from ovariectomized (OVEX) or hypophysectomized (HYPOX) female hamsters to elicit intense genital investigation and to facilitate overt copulatory behavior in males was compared with that of estrous vaginal discharge. The discharges were collected by vaginal lavage with water. In order to avoid exposure of experimental males to female stimuli other than vaginal discharge, the behavioral tests employed anesthetized males (female surrogates) whose hindquarters were scented with the collected vaginal material or with control solvent (water). Both the OVEX and HYPOX discharges elicited intense genital investigation and significantly increased the incidence of intromission attempts toward the scented surrogates. However, both types of discharge had significantly less behavioral activity than estrous vaginal discharge. In a subsequent experiment, a water dilution series of estrous vaginal discharge was tested for the ability to promote genital investigation and copulatory behavior toward scented surrogates. The amount of discharge typically extruded by one estrous female in response to tactile genital stimulation can be diluted one hundred-fold without appreciable reductions in its behavioral activity. These results demonstrate that the behavioral activity of hamster vaginal discharge is related to the endocrine status of females, and suggest that previous failures to demonstrate clear dependence on ovarian function might have been due to ceiling effects in laboratory tests.

Circadian organization of locomotor activity in the Turkish hamster (Mesocricetus brandti)

The circadian organization of locomotor activity was examined in Turkish hamsters while exposed to a light-dark (LD) cycle, constant illumination (LL), and following blinding and gonadectomy. Under LD 16:8 the activity rhythm of all hamsters became well entrained with activity beginning approximately 30 min after dark onset. In contrast, when activity rhythms free-ran as the result of exposure to LL or blinding, a variety of spontaneous perturbations in the period and/or phase of the activity rhythm were observed.