Photoperiodic Influences on Testicular Regression in the Golden Hamster: Termination of Scotorefractoriness
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1 BIOLOGY OF REPRODUTION 17, (1978) Photoperiodic Influences on Testicular Regression in the Golden Hamster: Termination of Scotorefractoriness ERI L. BITTMAN Department of Psychology, University of aliforni Berkeley, alifornia 9472 ABSTRAT Hamsters whose testes have regressed and recrudesced during the animals exposure to short photoperiods are insensitive to short days (scotorefractoriness). To restore sensitivity to short days, hamsters must first experience many weeks of long days (Reiter, 1972). The precise photoperiodic requirements for the termination of scotorefractoriness were investigated. Animals with spontaneously recrudesced testes were subjected to different durations and patterns of long day exposure to test the hypothesis that a restricted long day-sensitive period exists. Twenty weeks of photostimulation uniformly allowed regression to occur upon return of the animals to short days; hamsters exposed to 1 weeks of photostimulation were generally rendered sensitive to short days, but their testes did not regress as rapidly nor as consistently. This effect was obtained regardless of the pattern of photostimulation after spontaneous recrudescence. There was some indication that episodes of photostimulation can summate over intervals of 1, but not 1 weeks of short days or darkness. The results indicate that scotorefractoriness is not an all-or-none phenomenon; photostimulation during the refractory period acts principally to alter the rate of regression upon reexposure to short days. It is unlikely that a restricted long day-sensitive phase exists in the golden hamster. INTRODUTION The seasonal reproductive patterns of temperate zone vertebrates appear to increase species fitness by minimizing births during times when parental support would be difficult and survival of young doubtful (Sadleir, 1969). Proximate causes of reproductive seasonality include fluctuations of temperature and rainfall and availability of food, but many endotherms modulate their breeding activities by reference to highly reliable annual changes in daylength (photoperiodic time measurement, PTM). Mechanisms of PTM have been extensively studied in certain species which require long days (in hamsters, 12.5 h photoperiods or longer) for the induction or maintenance of gonadal function. Ingenious experiments on birds (Hamncr, 1963) and mammals (Elliott et al., 1972) imply that PTM is mediated by endogenous circadian pacemakers. An understanding of the organization of circadian systems provides powerful insights into the mechanisms by which reproductive seasonality is achieved (Elliott, 1976; Morin et al., 1977; Rusak and Accepted December 14, Received July 29, Morin, 1976; Stetson and Watson-Whitmyre, 1976). The seasonal cycles of some birds (van Tienhoven and Planck, 1974) and mammals (Reiter, 1973; Thorpe and Herbert, 1976) are characterized by a phase of unresponsiveness to previously effective daylengths. Testicular regression occurs eventually in photoperiodic birds despite continued exposure to long daylengths (photorefractoriness). A related effect is the spontaneous recrudescence of atrophied gonads in hamsters maintained on the same short daylengths that initially induced testicular regression (Reiter, 1972). The recrudesced testes remain fully functional regardless of photoperiod; this condition has been termed photorefractoriness by some workers (Stetson et al., 1976, 1977) and scotorefractoriness by others (Morin et a!., 1977; Zucker and Morin, 1977). The author prefers the latter term because it more clearly designates the insensitivity of the neuroendocrine axis to short days or darkness. The restoration of sensitivity to long days in photorefractory birds and to short days in scotorefractory hamsters requires exposure to many weeks of short or long days, respectively. In both instances, termination of refractoriness is mediated by the same circadian system that measures daylength in nonrefractory animals (Hamner, 871
2 872 BITTMAN 1968; Turek, 1972; Stetson et al., 1976). According to Reiter (1975), the hamster requires at least 14 weeks of long day exposure to break scotorefractoriness. The present experiments were concerned with several aspects of scotorefractoriness and the role of circadian rhythms in its termination. Specific questions asked were: a) does termination of scotorefractoriness require continuous exposure to long days or might the hamster require long day stimulation only during a restricted period subsequent to testicular recrudescence? The existence of a long day sensitive phase of the annual cycle would be analagous to the photosensitive phase of a circadian rhythm posited by an external coincidence model of photoperiodism (Pittendrigh, 1972). b) What is the duration of scotorefractoriness subse- quent to spontaneous recrudescence and c) are there long term effects of subthreshold durations of long day stimulation on scotorefractormess of the hamster reproductive system? MATERIALS AND METHODS Male hamsters (LVG-LAK) were obtained from the Lakeview Hamster olony, Newfield, NJ or were born in our laboratory from similar stock. All animals were maintained at approximately 23#{176}and allowed ad libitum access to Simonsen rat pellets (Maintenance Diet) throughout the experiment. Hamsters were exposed to 14 h of light/day (LD14:1O). The light period began at 2 h (Pacific Standard Time); light intensity during the light phase varied from 2-1 fc depending upon cage location. Some animals served as controls in another experiment (Zucker and Morin, 1977); this did not entail any treatment difference from that of hamsters not so utilized. Thirteen animals experienced a 3 week exposure to LD2:22 prior to the start of this experiment. This treatment induced neither regression nor scotorefractoriness. Since the results from these hamsters were similar to those of animals not so treated, their data were included in the general tabulation. All hamsters except those in group 3 were housed individually in wire mesh hanging cages. Hamsters in group 3 were maintained in group cages (3/cage) for the first 32 weeks of the experiment; they were then transferred to hanging cages. Such variations in housing do not affect the time course of testicular regression and recrudescence (Elliott, 1976; E. Bittman, unpublished observations). Animals were transferred to LD2:22 (lights on at 8 h PST) or LD8:16 (lights on at 145 h) photoperiods at week and were subsequently laparotomized under pentobarbital sodium anesthesia (8 mg/kg body weight) at predetermined intervals. The left testis was externalized and its maximum length and width measured with calipers. The testis was then sprinkled with saline, returned to the scrotum and the wound repaired. The testicular index (TI) obtained by multiplying these testis deminsions and dividing by body weight provides a reliable indication of gonadal condition (Rusak and Morin, 1976; Zucker and Morin, 1977). TI s in excess of 1.8 indicate functional testes; TI s below 1.4 indicate arrest of spermatogenesis and steroidogenesis (Rusak and Morin, 1976, Fig. 1). Only data from hamsters weighing 1 g or more are included in this report. Although many of the individual hamsters were not laparotomized prior to week 3, the time course of regression and spontaneous recrudescence were provided by data obtained from 91 hamsters arbitrarily selected for laparotomy. All comparisons were statistically evaluated by two-tailed tests. Refractoriness was studied in hamsters whose testes had spontaneously recrudesced, rather than in animals in which recrudescence was accelerated by long photoperiods. Spontaneous recrudescence more closely approximates the annual cycle as it is thought to occur in nature (Reiter, 1974). A second consideration favoring this choice is our previous observation that scotorefractoriness is not evident in a substantial proportion of hamsters whose testes are recrudesced by exposure to 1 or fewer weeks of long days subsequent to testicular regression (G. Eskes, B. Rusak and E. Bittman, unpublished observations). Twenty-two weeks of long day exposure is adequate to break scotorefractoriness in hamsters with newly recrudesced gonads (Reiter, 1972). To assess whether all portions of this interval are equally sensitive to such photostimulation, hamsters whose testes had recrudesced were allocated to 1 of 5 groups and transferred after at least 3 weeks of exposure to the short photoperiod to the original LD14: 1 cycle. Different groups received long day exposure at different phases of the next 22 week period (see Fig. 1). The intent was to hold the duration of photostimulation constant in order to discover whether the pattern of long day exposure influences scotorefractoriness. In all cases, scotorefractoriness was assessed by returning hamsters to the LD2:22 photoperiod (lights on at 8 h). Laparotomies were performed in animals of groups 1, 2 and S at 1 and 2 weeks after this transfer. Hamsters in group 4 were laparotomized 8 weeks after transfer to LD2:22. In a supplementary experiment, regression and recrudescence were verified by periodic laparotomies of 11 hamsters maintained in the LD2:22 photoperiod; all animals then were blind /J//////////J7i/////////A,,,,,,,,w,,,A ////////A #{149}#{149}t A //,/// - V/,,,A%W,///,//, y//7////////4 A#{149}#{149}#{149}#{149} 7, 7Z.. //Z. ZZ, - w,_,_,z1#{189}s-,,_;or,,,, :8 LO FIG. 1. Protocol of experimental treatments. Arrows indicate laparotomies; DD designates total darkness and LD2:22, LD8:16 and LD14:1O designate photoperiods providing 2, 8 and 14 h of light/day, respectively.
3 PHOTOPERIODI REGULATION OF TESTIULAR REFRATORINESS 873 ed by orbital enucleation (week 31). Additional laparotomies were performed 1 and 2 weeks later. RESULTS Testicular regression occurred after 1 weeks in LD2:22 (TI =.51 ±.2,n=42);spontaneous testicular recrudescence was complete after 3 weeks (TI = 1.9 ±.4, n = 39) in this photoperiod. Testes remained large during subsequent LD2:22 exposure; a pooled TI of 2.2 was obtained for spontaneously recrudesced hamsters testes measured after weeks of short day exposure (n = 32) and this value was used for statistical comparisons with other groups where appropriate. Twenty weeks of exposure to LD14:1 beginning at week 41 was effective in terminating scotorefractoriness (group 2A, Fig. 2). The testes of these hamsters uniformly regressed within 1 weeks of returning the animals to LD2:22 (TI week 61 vs TI week 71, P<.1). Similar results were obtained from hamsters receiving 22 weeks of photostimulation (group 2B, not illustrated). Results from other treatments were more variable. Ten weeks of exposure to LD14:1O was generally sufficient to break scotorefractoriness regardless of whether photostimulation began at week 3 (group 1B, Fig. 3) or at week 41 (group 1A, Fig. 4). The latter treatment also was effective in hamsters whose testes had 8< U, ) I 5 I //////// - 5 b. es is k5 6 minimum FIG. 3. Testis index (mean ± SEM) of hamsters exposed to experimental photoperiods of Experiment lb. Lettered points indicate testis indices of individual animals at weeks 5 and 6. Hamsters f and h died in the interval between these laparotomies. Minimum values indicate the mean ± SEM of the lowest testis indices found in each animal in each of these 2 laparotomies. Photoperiod designations as in Figs. 1 and 2. regressed and spontaneously recrudesced on LD8:16 (group 5B, Fig. 5). The mean Tls did not differ significantly among these 3 groups ///4_ 41 7/////////// 51 7 ///A 2.5 (6) a b s ds 8< U, U) I (7) U,, I fs FIG. 2. Testis index (mean ± standard error of mean) of animals exposed to experimental photoperiods of Experiment 2A. The chronology of the LD2:22 photoperiod (hatched bars) and LD14:1 photoperiod (open bars) is indicated in the upper part of each panel. Sample sizes shown in parentheses minimum FIG. 4. Testis index (mean ± SEM) of hamsters exposed to experimental photoperiods of Experiment 1 A. Lettered points indicate testis indices of individual animals laparotomized at weeks 61 and 71. Hamsters c, e, h and j died in the interval between laparotomies. Minimum values and photoperiod designations as in Fig. 3.
4 874 BITTMAN Gop 5 2, w 2/) 22 9 IS 3 4 o ) - II l /,/,1 o 41 5) 61 1) - I I 9 2 IS ) 3)ni IS) 71 I Groop SA 2e95 SB FIG. 5. Testis index (mean ± SEM) of hamsters exposed to various experimental photoperiods. Line graph (left) plots spontaneous recrudescence of all animals (groups 5A and SB). Hamsters were divided into groups receiving the different photoperiods at week 41. Bar graphs represent mean testis indices of hamsters laparotomized at weeks 61 and 71. Photoperiods are indicated as in previous figures; black bars indicate constant darkness and stippling indicates LD8:16. Sample sizes indicated in parentheses. (1A, 1B, 5B). Each group s mean TI was smaller than the pooled TI of spontaneously recrudesced nonphotostimulated hamsters (P<.1). In no group receiving 1 weeks of photostimulation did the testes regress quite as consistently as in animals exposed to 2 weeks of long days; regression was assessed 1 weeks after return to short days (group 1A week 61 vs 2A week 71.1<P<.2). Inspection of results from individual animals is instructive (lettered points Figs. 3, 4). In each group re- LO 8 ceiving 1 weeks of photostimulation, a major- LD 222 ity of hamsters had TIs of 1.6 or less when lap- 4 arotomized 1 weeks after their return to LD 2:22 (6/1 in group 1A; 1/12 in group 1B; 6/9 in group 5B). In all cases, hamsters whose testes manifested little or no regression in the first 1 weeks after return to LD2:22 (scotorefractory hamsters) had greatly or completely regressed testes 1 weeks later (Table 1). The TIs of groups 1A and 2A at week 71(2 and 1 weeks after return to LD2:22, respectively) did not differ significantly (P>.2). Individual animals whose testes had regressed during the first 1 weeks after return to LD2:22 showed the initiation of a second spontaneous recrudescence over the next 1 weeks regardless of whether they had received 1 (groups 1A, lb and SB, Figs. 3-5) or 2 (group 2, Fig. 2) weeks of photostimulation. This trend was significant only in group 2A (P<.1), which had shown consistent regression within 1 weeks of their return to short days. For present purposes, scotorefractoriness will be considered to have been broken only when regression occurs within the first 1 weeks after return to LD2:22. The conclusion that some long day exposure is necessary to break scotorefractoriness was confirmed by blinding hamsters with newly recrudesced testes (Fig. 6). Little or no regression occurred within the next 1 weeks. Substantial testicular regression occurred in the 4 hamsters surviving 21 weeks subsequent to blinding (TI at week 51 was 1.6 ±.2). TABLE 1. Regression in scotorefractory hamsters. Testis in dcx (TI) After 1 After 2 Animal weeks of weeks of no. Group LD2:22 LD2: A A A lb lb B B B B Mean ± SEM 1.99 ±.7.92 ±.9 The difference between TIs after 1 and 2 weeks of LD 2:22 was significant (P<.1, t-test).
5 PHOTOPERIODI REGULATION OF TESTIULAR REFRATORINESS (8),) ) In 8< a) I 5 - (q) I 5 I - I ) 4,) U) I.5-5 F- a I I I I I I I I I I I in LD 222 FIG. 6. Testis index (mean ± SEM) of hamsters maintained continuously in LD2:22. All hamsters were blinded by bilateral orbital enucleation at week 31. Sample sizes given in parentheses. FIG. 8. Testis index (mean ± SEM) of hamsters exposed to experimental photoperiods as indicated (group 4). Photoperiod designations as in previous figures. Sample sizes shown in parentheses. Unlike the 1 week exposure period, 5 week exposures to long days did not break scotorefractoriness; the testes of these animals did not undergo significant regression during the 8-1 weeks of short day challenge. This was true whether the 5 weeks of photostimulation commenced at 33 weeks (group 3, Fig. 7) or 47 weeks (group 4, Fig. 8) after the onset of LD2:22. A second 5 week period of LD 14:1 was only slightly more effective than the first in breaking scotorefractoriness: the 2 blocks of 2< In aso 2 a) I ) FIG. 7. Testis index (mean ± SEM) of hamsters exposed to experimental photoperiods as indicated (group 3). Photoperiod designations as in previous figures. Sample size indicated in parentheses. long days did not summate (group 3; week 63 vs week 48 P>.2; 11/15 hamsters had TIs> 1.6). The nonsignificant decrease in TI in hamsters photostimulated for 5 weeks late in the sensitive period delineated by Reiter (1975; weeks 47-52, group 4; weeks 48-53, group 3) raises the possibility that regression would have been observed in many of these animals had they been laparatomized after 2 weeks of LD 2:22 exposure. Unfortunately such data were not collected; it is noteworthy that TIs of these groups did not differ significantly from those of hamsters which had received 1 weeks of photostimulation ending at a similar time (group 1A, week 61 vs group 4, week 6,.1 <P<.2, vs group 3, week 63, P>.2). Ten weeks of LD14:1 initially appeared sufficient to terminate scotorefractoriness only if such photostimulation occurred in one continuous block. Although too few hamsters in group 5A survived the treatment for firm conclusions to be drawn, 1 weeks of LD14:1 interspersed with 1 weeks of DD on an alternating week-by-week basis were sufficient to terminate refractoriness in all cases (Fig. 5). Summation of long day photostimulation thus appears effective over intervals of at least 1 week of total darkness. DISUSSION Earlier findings concerning scotorefractoriness were corroborated and understanding of the phenomenon was refined and extended. In
6 876 BITTMAN agreement with Reiter (1972), 2 and 22 weeks of long day photostimulation were significantly more effective in terminating scotorefractoriness than were 1 consecutive weeks of long days. The present findings also also consistent with the recent report of Stetson et al. (1977), who found 7-9 weeks of photostimulation sufficient to allow rapid regression in approximately half of their animals upon return to short days. My extended testing revealed, however, that 1 weeks of long day exposure allowed regression to occur in every hamster, regardless of whether these 1 weeks fell early or late in the sensitive period. The latency to regression tended to be longer and its time course more variable than that of hamsters photostimulated for the full 22 weeks. Five weeks of long day stimulation did not allow rapid regression to occur upon return to short days. However, regression might have occurred even in these hamsters had they, like hamsters receiving 1 weeks of LD14:1, been tested after a sufficiently long interval. I suggest that the definition of scotorefractoriness be refined to refer only to the rate of regression rather than to an indefinite resistance to the regressive effects of short days. Regression tended to be more complete when hamsters exposed to 5 weeks of LD14:1 received such photostimulation later after spontaneous recrudescence, but this trend was not statistically significant. Stetson et al. (1977) reported a similar trend in animals exposed to 7 weeks of LD14:1 beginning 14 or 3 weeks after initial transfer to LD6:18. The present findings indicate the absence of any particular long day sensitive phase or of dramatic fluctuations in the sensitivity to such photostimulation after recrudescence. The analogy of the seasonal breeding rhythm to a model of circadian photoperiodism is not appropriate (Hamner, 1971). The eventual testicular regression of hamsters exposed to less than 2 weeks of long days is unlikely to be due to age alone. Reproductive decline in senescent hamsters, which apparently has only been studied in females, seems restricted to a 25% decrease in responsiveness to superovulatory doses of exogenous gonadotrophin and an increase in postconception mortality (Thorneycroft and Soderwall, 1969). The onset of a second recrudescence in the present experiment (Reiter, 1972) also suggests that the eventual testicular regression of these hamsters is not attributable to advancing age. The paucity of field data on the golden hamster is unfortunate; a true understanding of the importance of scotorefractoriness and the second regression is elusive in the absence of information on survivorship. The cause of the marked variability of regression rate of hamsters receiving 1 weeks of photostimulation is not immediately evident. There is appreciable variability in the phase angles of circadian entrainment to LD2:22 in hamsters with recrudesced testes (unpublished observations); it is possible that individual differences in the effectiveness of 1 weeks of long days in terminating scotorefractoriness result from such differences in phase angle. Those hamsters which are rendered sensitive to short days by 1 weeks of exposure to LD14:1 may have adopted photostimulatory phase angles (Elliott, 1976) to the prior short day cycle as they spontaneously recrudesced (unpublished observations). In such cases, the duration of photostimulatory entrainment to short days might summate with the subsequent exposure to long days, producing the appearance that the long days alone were sufficient to terminate scotorefractoriness. This is only one of several possible explanations of the observed variability; its investigation would require concurrent monitoring of circadian rhythms and assessment of reproductive status. Attention to both is necessary for an understanding of photoperiodism in the hamster. AKNOWLEDGMENTS This research was supported by USPHS Research Grant HD-2982, by the ommittee on Research of the University of alifornia and by a predoctoral fellowship from the National Science Foundation. I thank Darlene Frost, Margaret Roisman and larence Turtle for technical assistance; Harvey J. Silverman and Benjamin Rusak for their thoughtful comments on an earlier draft of this paper and Shirley Reaves for typing the manuscript. I am especially grateful to Irving Zucker for his generous material and personal support and for his helpful criticisms in all phases of this work. REFERENES Elliott, J. A. (1976). ircadian rhythms and photoperiodic time measurement in mammals. Fed. Proc. 35, Elliott, J. A., Stetson, M. H. and Menaker, M. (1972). Regulation of testis function in golden hamsters: a circadian clock measures photoperiodic time. Science 178, Hamner, W. M. (1963). Diurnal rhythm and photoperiodism in testicular recrudescence of the House Finch. Science 142,
7 PHOTOPERIODI REGULATION OF TESTIULAR REFRATORINESS 877 Hamner, W. M. (1968). The photorefractory period of the House Finch. Ecology 49, Hamner, W. M. (1971). On seeking an alternative to the endogenous reproductive rhythm hypothesis in birds. In: Biochronometry. (M. Menaker, ed.). Washington, D, National Academy of Sciences. pp Morin, L. P., Fitzgerald, K. M., Rusak, B. and Zucker, I. (1977). ircadian organization and neural mediation of hamster reproductive rhythms. Psychoneuroendocrinology 2, Pittendrigh,. 5. (1972). ircadian surfaces and the diversity of possible roles of circadian organization in photoperiodic induction. Proc. Nat. Acad. Sci. 69, Reiter, R. J. (1972). Evidence for refractoriness of the pituitary-gonadal axis to the pineal gland in golden hamsters and its possible implications in annual reproductive rhythms. Anat. Rec. 173, Reiter, R. J. (1973a). Pineal control of a seasonal reproductive rhythm in male golden hamsters exposed to natural daylight and temperature. Endocrinology 92, Reiter, R. J. (1973b). omparative physiology: pineal gland. Ann. Rev. Physiol. 35, Reiter, R. J. (1974). ircannual reproductive rhythms in mammals related to photoperiod and pineal function: A review. hronobiologia 1, Reiter, R. J. (1975). Exogenous and endogenous control of annual reproductive cycle in male golden hamster: participation of the pineal gland. J. Exp. Zool. 191, Rusak, B. and Morin, L. P. (1976). Testicular responses to photoperiod are blocked by lesions of the suprachiasmatic nuclei in golden hamsters. Biol. Reprod. 15, Sadlier, R. M. F. S. (1969). The ecology of reproduction in wild and domestic animals. Methven, London. pp Stetson, M. H., Matt, K. S. and Watson-Whitmyre, M. (1976). Photoperiodism and reproduction in golden hamsters: circadian organization and the termination of photorefractoriness. Biol. Reprod. 14, Stetson, M. H. and Watson-Whitmyre, M. (1976). Nucleus suprachiasmaticus the biological clock in the hamster? Science 191, Stetson, M. H., Watson-Whitmyre, M. and Matt, K. S. (1977). Termination of photorefractoriness in golden hamsters-photoperiodic requirements. J. Exp. Zool. 22, Thorneycroft, I. H. and Soderwall, A. L. (1969). Ovarian morphological and functional changes in reproductively senescent hamsters. Anat. Rec. 165, Thorpe, P. A. and Herbert, J. (1976). Studies on the duration of the breeding season and photorefractoriness in female ferrets pinealectomized or treated with melatonin. J. Endocrinol. 7, Turek, F. W. (1972). ircadian involvement in termination of the refractory period in two sparrows. Science 178, Van Tienhoven, A. and Planck, R. J. (1973). The effect of light on avian reproductive activity. In: Handbook of Physiology. Vol. II. Female Reproductive System. Sect. 7. Endocrinology. (R.. Greep and E. B. Astwood, eds.) American Physiological Society, Washington. D. pp Zucker, I. and Morin, L. P. (1977). Photoperiodic influences on testicular gression, recrudescence and the induction of scotorefractoriness in male golden hamsters. Biol. Reprod. 17,
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