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Role of thyroid hormones in the neuroendocrine control of seasonal reproduction in red deer hinds

Anderson, Greg Muir
Fields of Research
ANZSRC::070206 Animal Reproduction
A series of eight experiments was conducted to investigate the requirement for thyroid hormones in neuroendocrine processes which lead to the seasonally anoestrous state in red deer hinds. The first two experiments used thyroidectomized, ovariectomized, oestradiol-treated hinds which received various thyroid hormone replacement treatments (n=5 per group) to investigate the timing and dose-responsiveness of thyroid hormones in bringing about seasonal oestradiol-induced suppression of plasma LH concentration. A significant seasonal decline in mean plasma LH concentration during September (coinciding with the onset of anoestrus in entire cycling hinds in New Zealand) was observed in all thyroidectomized hinds in both experiments regardless of T₄ or T₃ treatment. When oestradiol implants were removed in November or December, mean plasma LH concentrations increased significantly in all but one of hinds in which T₄ had been administered at very low doses by subcutaneous implants, and mean plasma LH concentrations and LH pulse amplitude increased in approximately half of hinds administered T₃ at varying doses by subcutaneous injections over a one-week period in October. These results suggested that thyroid hormones are not required for steroid-dependent reproductive suppression, but could possibly play a role in steroid-independent suppression of LH secretion. Because problems were encountered in delivering appropriate doses of thyroid hormones in both experiments, further confirmation of these findings was required. Therefore in the next experiment the role of thyroid gland secretions was examined in euthyroid (n=5) and thyroidectomized (n=4) ovariectomized hinds treated with oestradiol implants. These implants were removed for about one month on three occasions to examine the effect of thyroidectomy on steroid-independent control of seasonal LH secretion. During the non-breeding season basal and GnRH-induced plasma LH concentrations declined in all hinds in the presence of oestradiol, but returned to breeding season levels when oestradiol was withdrawn in November. In a concurrent experiment, thyroidectomy of ovary-entire hinds (n=7) during the breeding season prevented the cessation of oestrous cyclicity in spring; this was in contrast to oestrous cyclicity in T₄replaced (n=4) or euthyroid control (n=5) hinds which ceased to occur in early September. Collectively, these results indicate that thyroid hormones are required for the termination of the breeding season in cycling red deer hinds and that this action occurs via steroid-independent neuroendocrine pathways. Two experiments were conducted using neurotransmitter receptor agonists and antagonists to identify neural pathways in the brain which mediate LH suppression by oestradiol and by steroid-independent mechanisms, and to test if the thyroid gland is required for activation of these pathways during the non-breeding season. It was concluded from the lack of plasma LH responses to dopaminergic and opioidergic agonists and antagonists in ovariectomized and ovariectomized, thyroidectomized hinds (n=5) that neural pathways involving dopamine-D₂receptors do not mediate oestradiol-induced seasonal suppression of plasma LH concentrations, and neither dopaminergic or opioid neural pathways mediate non-steroidal suppression of plasma LH concentrations. However preliminary evidence was obtained for a stimulatory role of serotonergic neural pathways in controlling LH secretion. Another experiment was conducted to identify when the steroid-independent mechanisms which suppress LH concentrations during the non-breeding season are responsive to thyroid hormones. T₄treatment at the beginning of or during the non breeding season was effective in bringing about suppression of plasma LH concentration in thyroidectomized, ovariectomized hinds (n=5 per group), but this action of thyroid hormones did not occur during the breeding season. These results show that the steroid-independent mechanisms which contribute to seasonal suppression of plasma gonadotrophin concentrations require thyroid hormones to be present only from around the time of the end of the breeding season for their normal expression, and they remain responsive to thyroid hormones after this period. Lastly, the feasibility of achieving out-of-season breeding using thyroidectomized hinds (n=9) was evaluated by comparing oestrous behaviour, ovulation and pregnancy rates to those of euthyroid control hinds (n=7) following synchronization of oestrous cycles. There was a non-significant trend for a greater occurrence of oestrous behaviour and ovulation in thyroidectomized hinds compared with euthyroid controls during the non-breeding season, but the pregnancy rate following out-of season mating with a thyroidectomized stag was low, suggesting that a side effect of thyroidectomy may be impaired fertility. Six out-of-season pregnancies were obtained from eight matings, however because three of these pregnancies occurred in euthyroid control hinds no improvement in out-of-season reproductive performance could be attributed to thyroidectomy. It is likely that if the actions of the thyroid glands are to be exploited as a tool for achieving out-of-season breeding in this species, techniques will have to be developed for specifically blocking or overcoming the effects of thyroid hormones on the reproductive neuroendocrine centres without causing general hypothyroidism and its associated side-effects.
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