Seasonal Modulation of Luteinizing-Hormone Secretion in Female Rhesus Monkeys1

Abstract

The seasonal restriction of ovulations in rhesus monkeys is thought to be due to enhanced estradiol (E2)-negative feedback suppression of luteinizing hormone (LH) during the spring and summer anovulatory months. This hypothesis was examined in seven ovariectomized monkeys housed in an outdoor environment and treated with various doses of E2 in a counterbalanced design during both the anovulatory season (May-Jul) and the breeding season (Sep-Nov). Subcutaneous implants of E2 produced levels that mimicked late follicular (LF-100 pg/ml) or periovulatory concentrations (PO-190 pg/ml). Analyses of twice weekly serum samples revealed that during the period of no E2 treatment (NT), basal levels of bioactive LH were significantly lower in the summer than the fall. Although treatment with both doses of E2 lowered basal LH levels during both seasons, the decrease in LH was significantly greater during the summer. Samples collected at 15-min intervals for 2 h revealed that during NT, LH pulses were significantly slower during the summer than in the fall, whereas pulse amplitude did not differ between seasons. Treatment with both doses of E2 either abolished or significantly reduced both LH pulse amplitude and frequency in the summer. In contrast, LH pulses during the fall were not affected by E2 treatment. Response to treatment with LH-releasing hormone (5 micrograms/kg i.v.) revealed that release was significantly reduced during E2 treatment in the summer. These data indicate that seasonal changes in the environment influence both nongonadal control and E2-negative feedback inhibition of LH secretion. The reduced ability of E2 to maximally suppress LH release in the fall can thus account for the seasonally delimited pattern of ovulations observed in rhesus monkeys.

Social Subordination and Polymorphisms in the Gene Encoding the Serotonin Transporter Enhance Estradiol Inhibition of Luteinizing Hormone Secretion in Female Rhesus Monkeys1

“…This hypersensitivity to E2-negative feedback inhibition is similar to that observed during the initial stages of puberty [63][64][65], during lactational infertility [66], and in the regulation of LH secretion in seasonally breeding animals [45,67]. The inhibitory action of E2 is likely mediated through a number of neurochemical changes acting on hypothalamic gonadotropin-releasing hormone (GnRH) release as well as directly affecting pituitary gonadotropin secretion [68][69][70].…”

“…Consequently, we measured both cortisol and LH in single morning serum samples obtained 30 min after the saline or CRHA injection (i.e., at 0900 h) on Days 2-5 of each phase. A similar approach has been used to quantify the seasonal [37,45] and developmental [8,46] regulation of LH in socially housed rhesus monkeys. Because a single morning cortisol sample does not reliably discriminate dominant vs. subordinate females [28,47,48], the intent of the cortisol measurements was to assess treatment effects of E2 and the CRHA rather than consequences of social subordination.…”

The Effect of Season on the Induction of Sexual Behavior by Estradiol in Female Rhesus Monkeys1

“…Domestic ewes show seasonal differences in estrous response to very low levels of E, (Raeside and McDonald, 1959;Fletcher and Lindsay, 1971), but serum E, of 3 pg/ml or more induces estrus in all ewes regardless of season (Goodman et al, 1981). A seasonal difference in both nongonadal and E, -negative feedback-inhibiting LH occurs in outdoor-housed female rhesus monkeys (Wilson et al, 1986a), possibly through a reduction of endogenous LH-releasing hormone (LHRH) release during the summer months. A single injection of LHRH potentiates the lordosis response in E, -primed rats (Moss and McCann, 1973;Pfaff, 1973;Riskind and Moss, 1979) and enhances solicitational displays in ovariectomized, E, -implanted common marmosets (Kendrick and Dixson, 1985).…”

Metabolic and reproductive consequences of the serotonin transporter promoter polymorphism (5-HTTLPR) in adult female rhesus monkeys (Macaca mulatta)

“…The eighth l/l female was the female dropped from the overall analysis for clinical reasons stated above. Because rhesus monkeys housed in an outdoor environment breed seasonally, with ovulations restricted to the fall and winter months [34,35], all data were collected between Sep 10 and Dec 23. To characterize ovulatory cycles and patterns of menstruation, blood samples for the analysis of estradiol and progesterone were collected three days per week (Mon, Wed, Fri).…”

“…Following recovery from surgery, females were implanted with silastic capsules of estradiol that produced serum concentrations of approximately 40 pg/ml [35]. All females were then subjected to a dexamethasone suppression test.…”