The Effect of Photoperiod and Melatonin Injection on Serotonergic Immunoreactivity in Rat Brain Stem.
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The Djungarian hamster displays photoperiodic variations in gonadal size synchronized to the seasons by the nightly secretion of the pineal hormone melatonin. In short photoperiod (SP), the gonads regress in size, and circulating sex steroids levels decline. Thus, the brain is subject to seasonal variations of both melatonin and sex steroids. Tanycytes are specialized glial cells located in the ependymal lining of the third ventricle. They send processes either to the meninges or to blood vessels of the medio-basal hypothalamus. Furthermore, they are known to locally modulate GnRH release in the median eminence and to display seasonal structural changes. Seasonal changes in tanycyte morphology might be mediated either through melatonin or sex steroids. Therefore, we analyzed the effects of photoperiod, melatonin, and sex steroids 1) on tanycyte vimentin expression by immunohistochemistry and 2) on the expression of the neural cell adhesion molecule (NCAM) and polysialic acid as markers of brain plasticity. Vimentin immunostaining was reduced in tanycyte cell bodies and processes in SP. Similarly, tanycytes and their processes contained lower amounts of NCAM in SP. These changes induced by SP exposure could not be restored to long photoperiod (LP) levels by testosterone supplementation. Likewise, castration in LP did not affect tanycyte vimentin or NCAM expression. By contrast, late afternoon melatonin injections mimicking a SP-like melatonin peak in LP hamsters reduced vimentin and NCAM expression. Thus, the seasonal changes in vimentin and NCAM expression in tanycytes are regulated by melatonin independently of seasonal sex steroid changes.
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Abstract Many temperate‐zone species use photoperiod as an environmental cue to regulate reproductive timing. Strains of laboratory rats differ in their responsiveness to photoperiod, with the Fischer 344 (F344) strain being the most responsive known. F344 rats and closely related strains that differ in photoresponsiveness may be useful models to study the mechanisms and genetic basis for photoresponsiveness. We tested two hypotheses: (i) that melatonin mediates photoresponsiveness in F344 rats, as is the case in all other mammals tested, and (ii) that the location, abundance, or affinity of melatonin receptors, as estimated by the amount and location of binding of the radioligand 2‐[ 125 I]‐iodomelatonin (IMEL) in the brain, might cause variation in photoresponsiveness among rat strains. Melatonin injections 1 h before lights off in a stimulatory photoperiod (L14 : D10) induced reproductive inhibition and reduced weight gain in a manner similar to short days of L8 : D16, while injections of ethanolic saline vehicle did not. Interestingly, melatonin injections administered during an inhibitory photoperiod (L10 : D14) caused greater inhibition of both reproduction and weight gain than short photoperiod alone. Pinealectomized F344 rats implanted subcutaneously with melatonin in a silastic capsule did not differ in testis size or body weight from controls with blank implants. The brains and pars tuberalis of the pituitary from photoresponsive F344 rats and nonphotoresponsive Harlan Sprague‐Dawley (HSD) rats were processed for autoradiography using IMEL. We found significantly higher specific IMEL binding in the anterior and posterior regions of the paraventricular nucleus of the thalamus (PVNt) and reuniens nucleus of the thalamus of F344 rats than in the same areas in HSD rats. There were no differences between strains in specific IMEL binding in the medial PVNt, anteroventral and anterodorsal nucleus of the thalamus, suprachiasmatic nucleus, or the pars tuberalis. These results indicate that melatonin mediates photoresponsiveness in F344 rats. In addition, they provide support for the hypothesis that F344 rats may be photoresponsive due to differences from other strains in the location, density, or affinity of melatonin receptors.
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Day-night differences in the concentrations of melatonin and serotonin (5HT) were measured in several regions of the chicken brain, pineal gland and serum. Melatonin concentrations are higher at midnight than at midday in 8 of the 10 tissues studied although the amplitudes of these rhythms varied greatly. Day-night differences in the pineal, hypothalamus, thalamus, retina and pons-midbrain regions had the highest amplitudes. 5HT concentrations were rhythmic in only 3 of the tissues studied: the hypothalamus, thalamus and retina. These were also the areas of highest 5HT concentration. Exogenous melatonin, injected at midday, was taken up with similar patterns; the pineal, hypothalamus, thalamus and pons-midbrain contained more melatonin 20 min after injection than did other tissues. The rate of decline of melatonin concentration varied little among all tissues studied, suggesting that the differences among tissue concentrations were due to selective uptake mechanisms rather than specialized degradation pathways. The effects of exogenous melatonin on 5HT concentration were restricted to hypothalamus, thalamus, pons-midbrain, retina and pineal. No effect was seen in cerebellum, optic tectum, neostriatum, hippocampus and medulla oblongata. Together, these data strongly suggest that pineal (and exogenous) melatonin is selectively taken up primarily by three brain regions, hypothalamus, thalamus and pons-midbrain, in which it produces increases in 5HT concentrations. Regional selectivity of uptake may be the mechanism by means of which the effects of melatonin on 5HT-mediated function are restricted to specific brain areas.
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The objective of this study was to characterize a site at which it is likely that melatonin mediates photoperiodic control of reproduction in the male Syrian hamster. The first experiment was a comparison of the distributions of iodomelatonin (IMEL)-binding sites and cells immunoreactive to androgen receptors (AR-ir) in the medio-basal hypothalamus (MBH). AR-ir cells extended throughout the MBH, whereas IMEL binding was restricted to the dorsomedial nucleus (DMN). Comparisons between IMEL binding and AR-ir on adjacent cryostat sections revealed a clear overlap between the IMEL-binding sites and a distinct subpopulation of AR-ir cells within the DMN. The second experiment examined whether lesions of these IMEL- and androgen-responsive cells affected the response of the hamsters to short-day (SD)-like infusions of melatonin. Animals received sham or bilateral electrolytic lesions of the IMEL-binding sites within the DMN of the hypothalamus (MBH-X). Animals were pinealectomized and 4 wk later fitted with an s.c. cannula for the daily infusion of either melatonin (50 ng/h) or saline (500μl/10 h). After 6 wk the animals with sham lesions showed gonadal atrophy and lower serum concentrations of LH and prolactin (PRL) after infusions with melatonin. In contrast, MBH-X animals given melatonin had large testes and long-day (LD)-like serum LH concentrations. Infusions of melatonin did, however, cause a significant decline in serum PRL level. This study shows that an intact MBH is essential for the expression of gonadotrophic but not lactotrophic responses to melatonin and/or photoperiod. It also suggests that cells responsive to both gondal steroids and melatonin may be involved in the seasonal variation in GnRH release, and indicates a site at which melatonin might influence sensitivity to steroid feedback, a hypothalamic function known to be regulated by photoperiod.
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The neural components underlying the influence of photoperiod upon reproductive functioning are poorly understood. In this study, we have used immunocytochemistry to examine whether changes in photoperiod may influence specific neuronal cell populations implicated in mediating gonadal steroid feedback actions on GnRH neurons. Short day (SD) exposed ewes in the midluteal stage of the estrous cycle and long day (LD) anestrous ewes were perfused in pairs and hypothalamic brain sections immunostained for tyrosine hydroxylase (TH), neuropeptide Y (NPY), β-endorphin (βE), and the estrogen receptor (ER). The number of ER-immunoreactive cells detected within the preoptic area, but not the hypothalamus, was approximately 20% higher (P< 0.05) in LD ewes compared with SD animals. The numbers of TH-immunoreactive neurons comprising the A12, A14, and A15 cell groups were not different between LD and SD ewes, and the percentage of A12 (∼15%) and A14 (∼25%) neurons expressing ERs was similarly unaffected by photoperiod. The number of βE neurons detected in the arcuate nucleus was 50% lower (P < 0.05) in SD vs. LD ewes, whereas NPY-immunoreactive cell numbers in the median eminence were 300% higher (P < 0.05). Approximately 3% of NPY neurons in the median eminence, and 10% in the arcuate nucleus, expressed ER immunoreactivity in a photoperiod-independent manner. These studies indicate that changes in photoperiod may regulate ER expression within the preoptic area and suggest that hypothalamic NPY and βE neurons are involved in the seasonal regulation of reproductive activity in the ewe.
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Using quantitative autoradiography, melatonin receptors have been studied during post-natal and pubertal development of the rat in 2 brain and 2 pituitary structures. In the pars distalis of anterior pituitary, melatonin receptors decrease gradually in density after birth and disappear in 30 day-old animals. In contrast melatonin binding is only expressed in the paraventricular nuclei of the thalamus at the age of 21-23 days and is always present in adult animals. In the suprachiasmatic nuclei and in the pars tuberalis of the pituitary, melatonin receptor density decreases after birth, remains stable for approximately 1 month and increases again at puberty to reach the birth values in the adult. This increase was absent in pinealectomized and in castrated animals but present in castrated animals receiving testosterone suggesting that it depends upon circulating testosterone and melatonin levels. These results show that melatonin receptors are differentially regulated during post-natal development in each of the 4 structures studied, and that melatonin and testosterone are 2 factors which could be involved in the regulation of melatonin receptor density in the suprachiasmatic nuclei and pars tuberalis.
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