Disruption of Reproductive Rhythms and Patterns of Melatonin and Prolactin Secretion Following Bilateral Lesions of the Suprachiasmatic Nuclei in the Ewe

Abstract

To determine whether the photoperiodic responses of reproductive and prolactin (PRL) rhythms in the ewe requires an intact suprachiasmatic nucleus (SCN) driving the pineal rhythm of melatonin secretion, four groups of ovary-intact ewes over a 6-year period were subjected to bilateral (n = 40) or sham lesions (n = 15) of the SCN. Animals were exposed to an alternating 90-120 day photoregimen of 9L:15D and 16L:8D photoperiods. Blood samples taken twice weekly were assayed for prolactin and for progesterone to monitor oestrous cycles. On several occasions blood samples also were taken at hourly intervals for 24 h and analyzed for melatonin. Melatonin concentrations in sham lesioned ewes were basal during the lights-on period and rose robustly during darkness. Those sheep bearing unilateral lesions of the SCN (n = 13) or where the lesion spared the SCN entirely (n = 8) had patterns of melatonin secretion similar to sham ewes. The remaining ewes, having complete (n = 9) or incomplete bilateral (n = 8) destruction of the SCN, with one exception, had disrupted patterns of melatonin secretion. The nature of this disruption varied from complete suppression to continuously elevated levels. In lesioned ewes where melatonin secretion was not affected the onset and cessation of ovarian cycles were similar to sham ewes; stimulation of oestrous cycles under 9L:15D and cessation of oestrous cycles under 16L:8D. In contrast, 13 of 17 ewes with disrupted melatonin secretion also exhibited disrupted patterns of ovarian activity. In these animals oestrous cycles were no longer entrained by photoperiod but still occurred in distinct clusters, that is, groups of cycles began and ended spontaneously. Sheep with normal melatonin patterns showed low levels of PRL secretion during short days and elevated PRL levels during long days. However, 8 of 13 ewes with disrupted melatonin showed patterns of PRL secretion that were no longer entrained by photoperiod. A minority of ewes with disrupted melatonin patterns still showed reproductive (n = 4) and PRL (n = 5) responses similar to those of sham-lesioned ewes. These results show that bilateral destruction of the SCN in the ewe disrupts the circadian pattern of melatonin secretion and that this disruption usually, but not always, is associated with altered photoperiodic responses. These results strongly suggest that the SCN are important neural elements within the photoperiod time-keeping system in this species. A role for the SCN in the generation of endogenous transitions in reproductive activity (refractoriness) and prolactin secretion is not supported.

Circadian rhythms and reproduction

“…The expected LH surge and ovulation were blocked, but only delayed by 24 h, since the following afternoon there was a normal LH surge in animals treated with the drug (Everett & Sawyer 1950). Lesions of the SCN results in the loss of the gating response to elevated oestrogen and hence the cessation of ovulation in rats (Mosko & Moore 1979), but not in sheep (Scott et al 1995), suggesting that different mechanisms may be present in different species. Nevertheless, the SCN is known to project to GnRH-positive neurons in the hypothalamus and the region also expresses oestrogen receptors (van der Beek et al 1993, 1997b, de la Iglesia et al 1995, Watson et al 1995, providing a possible pathway for the steroid to influence the timing of the ovulation.…”

Thyroid hormones and seasonal reproductive neuroendocrine interactions

“…In mammals, light signals are received by the eye and are then transmitted to the circadian pacemaker in the hypothalamus, i.e., the suprachiasmatic nucleus (SCN). The SCN drives the nocturnal rhythm of melatonin secretion by the pineal gland, and a lesion in the SCN abolishes the circadian rhythms that govern the production and secretion of this hormone (Scott et al 1995, Tessonneaud et al 1995. Hamsters and sheep have been shown to develop photoperiodic blindness following pinealectomy (Hoffman & Reiter 1965, Bittman et al 1983).…”

Biological Rhythms

“…This technique confirmed the links in the pathway from the SCN to the pineal gland, and also suggested that two parallel circuits from the SCN (one from the dorsomedial and one ventrolateral) likely drive melatonin secretion. This day -night regulation of melatonin is regulated by the SCN (for a review, see Cassone, 1990), and, as with other hormonal systems mentioned previously, lesions of the SCN abolish circadian rhythms in melatonin production and secretion (Scott, Jansen, Kao, Kuehl, & Jackson, 1995;Tessonneaud, Locatelli, Caldani, & Viguier -Martinez, 1995).…”