Occlusion of the Melatonin‐Free Interval Blocks the Short Day Gonadal Response of the Male Syrian Hamster to Programmed Melatonin Infusions of Necessary Duration and Amplitude

Abstract

Photoperiodic control of the neuroendocrine axis is mediated by changes in the duration of the nocturnal melatonin signal. This study tested the hypothesis that reading of the signal depends upon the presence of a period free of melatonin between successive signals. Adult male Syrian hamsters were pinealectomized and received chronic subcutaneous infusions of melatonin or saline for 6 weeks. Animals which received saline had large testes. Those which received a single daily infusion which lasted for 10 h (50 ng/h) followed by 14 h without infusion underwent gonadal atrophy. Other animals received a compound melatonin signal in which the melatonin-free interval was occluded by a continuous infusion (25 nglh). Superimposed upon this was a 10 h phasic increase in infusion rate such that the maximum rate of infusion was equivalent to that observed in controls (25 ng/h increase, 50 nglh peak rate), or the increase in rate over the baseline was the same as in controls (50 nglh increase, 75 nglh peak rate). In neither group did the animals undergo gonadal regression. Analysis of iodomelatonin binding sites by in vitro autoradiography failed to reveal any systematic difference between animals which did and did not respond to melatonin and so the absence of a response could not be attributed to loss of receptors. These data demonstrate that the photoperiodic system cannot identify the melatonin signal solely upon the features of nocturnal peak height or amplitude of the peak over baseline. They are consistent with the hypothesis that the melatonin-free interval plays a significant role in photoperiodic time measurement.

Testicular Regression in Pinealectomized Syrian Hamsters following Infusions of Melatonin Delivered on Non-Circadian Schedules1

“…In sheep, it has also been shown that systemic infusions that restore a rhythm of melatonin in the blood of pinealectomized animals can also induce neuroendocrine responses characteristic of long or short photoperiods [8]. Experiment 1 demonstrated that the 10-h infusion protocol used in this and previous studies from this laboratory [11][12][13] raised circulating levels of melatonin for the duration of the 10-h infusion; it showed also that between infusions, melatonin concentrations were at the limit of sensitivity of the assay. There was no significant difference in the duration or amplitude of the melatonin peak between the infused animals in the present study and pineal-intact hamsters held on a schedule of 8L:16D (duration = 10 h in both groups; peak serum melatonin concentration: infused 68.68 ± 25.96 pg/ml, intact 63 ± 16.36 pg/ml) [14].…”

“…Long-day breeders such as the Syrian hamster respond to lengthening melatonin signals with gonadal regression and decreased serum concentrations of gonadotropins [3][4][5], whereas in short-day breeders such as sheep and deer, longer melatonin signals trigger gonadal activation [6,7]. The photoperiodic effects of the endogenous melatonin signal can be mimicked in pinealectomized animals by programmed systemic infusions of hormone, a procedure that has been used extensively in sheep [8], mink [9], Siberian hamsters [4,5,10], and Syrian hamsters [11][12][13]. Through this procedure it is possible to vary systematically individual parameters of the melatonin signal, such as its amplitude, duration, and frequency, and thereby determine which parameters are of primary importance in conveying photoperiodic information.…”

“…It is also clear that, in the Syrian hamster at least, there must be an interval between signals when melatonin is absent or present at very low levels if the photoperiodic cue is to be read effectively. The neuroendocrine axis will not respond simply to elevated levels of melatonin superimposed above a low, continuous infusion [12]. In addition, recent experiments have revealed that photoperiodic responses are also sensitive to the frequency at which melatonin signals are encountered.…”

Effects of Superior Cervical Ganglionectomy and Melatonin Replacement on Intra-hypothalamic LHRH Content and Pulsatile Luteinizing Hormone Release in the Mink

“…Furthermore, in male fallow deer investigated during the seasonal change from the non-breeding to breeding condition, a shortened transitional pattern, characterized by an earlier increase in the highly pulsatile pattern of LH following melatonin treatment, was observed (Asher and Peterson, 1991). The reverse is true for certain other species, where an interruption of the daily melatonin secretion is necessary for the gonadal activation in response to pituitary activation, as demonstrated in pinealectomized Syrian hamsters using a timed infusion protocol of melatonin (Maywood et al, 1991;Bartness et al, 1993;Grosse et al, 1993). From measurement of the LH levels in this species, suggested that the duration of the nightly release of melatonin was more important in the coding of day length, than the circadian phase in which melatonin was present.…”

Gonadal Responses of the Male Tau Mutant Syrian Hamster to Short-Day-Like Programmed Infusions of Melatonin1

“…Thus, in PX hamsters, timed daily infusions of melatonin lasting 4-6 h induce responses associated with long photoperiods, while longer infusions (10 h) delivered over several weeks result in gonadal atrophy typical of exposure to SD [10,[13][14][15]. Although the circadian system is responsible for the generation of the melatonin signal, its role in the interpretation of the signal, the basis of photoperiodic time measurement, is less clear.…”