Developmental Changes in the Luteinizing Hormone Secretory Pattern in Peripubertal Female Rhesus Monkeys: Comparisons between Gonadally Intact and Ovariectomized Animals*

Abstract

Developmental changes in LH release patterns were observed longitudinally in female rhesus monkeys at 10-65 months of age. The average ages of menarche and first ovulation in this experiment (n = 14) were 31.1 +/- 2.6 and 47.0 +/- 2.6 months (mean +/- SE), respectively. To assess the ovarian influence on developmental changes in LH, data were simultaneously obtained from neonatally ovariectomized animals at similar ages. The estimation of circulating LH was made with RIA as well as biological assay. During the prepubertal period (10-20 months of age), basal LH was very low, and there was no circadian fluctuation of LH in gonadally intact monkeys. During the early pubertal stage (20-30 months of age), before menarche, basal LH levels started to increase, and a circadian LH rhythm (nocturnal increases) appeared. At the midpubertal stage (30-50 months of age), a period between menarche and first ovulation, basal LH levels further increased, and the circadian LH rhythm was maximal. At the late pubertal stage (50-60 months of age), a period after the first ovulation during which the animals were not able to reproduce fully as adults, basal LH declined, and the circadian rhythm diminished. Similar but more exaggerated developmental changes in basal LH and the circadian fluctuation of LH were observed in females ovariectomized neonatally. Basal LH levels at 10-20 months were as low as those in intact animals with no circadian rhythm present. During the early pubertal period, a circadian fluctuation appeared at the time when a slight increase in the basal LH level occurred. Furthermore, the amplitude of circadian fluctuation (the difference between morning and evening LH values) increased linearly with the increase in basal LH during the midpubertal stage. These LH parameters in ovariectomized animals reached their peaks at 40-44 months, an age before the first ovulation in intact animals. As basal LH levels declined during the late pubertal stage to postpubertal stage, circadian fluctuation disappeared. The results suggest that the increase in LH output and concomitant circadian fluctuations occur in close association with the pubertal process, and this change in LH release is not dependent on the presence of the ovary. Therefore, we suggest that alteration of the LHRH release pattern during maturation, as reflected by LH release, rather than resetting of the gonadostat, is the key factor involved in the mechanism of the onset of puberty.

Short-day melatonin pattern advances puberty in seasonally breeding rhesus monkeys (Macaca mulatta)

“…Significant increases in serum oestradiol for Group H were not observed until 27 months of age, after the occurrence of menarche as found in other studies (Terasawa et al, 1984a;Wilson et al, 1986). Correspondingly, the pattern ofGH and somatomedin-C secretion paralleled that of oestradiol.…”

“…The loss of non-gonadal restraint at~25 months in these monkeys housed outdoors is similar to that of monkeys housed in a non-seasonal environment of 12 h light: 12 h dark (Terasawa et al, 1984a). Furthermore, under indoor housing conditions, intact females exhibit the increase in basal LH (Terasawa et al, 1984a) and menarche (Wilson et al, 1988) at an earlier age, with a greater percentage having first ovulation during their 2nd year, than animals housed in a seasonal environment (Wilson et al, 1988). These results suggest that the annual exposure to the warm, long days of spring and summer may delay sexual maturation, while the removal of these cues allows development to proceed unhindered by external events.…”

“…Those females which enter the breeding season of their 2nd year at a more advanced developmental age, based on age at increases in LH and menarche, are more likely to ovulate in that season (Wilson et al, 1986). The loss of non-gonadal restraint at~25 months in these monkeys housed outdoors is similar to that of monkeys housed in a non-seasonal environment of 12 h light: 12 h dark (Terasawa et al, 1984a). Furthermore, under indoor housing conditions, intact females exhibit the increase in basal LH (Terasawa et al, 1984a) and menarche (Wilson et al, 1988) at an earlier age, with a greater percentage having first ovulation during their 2nd year, than animals housed in a seasonal environment (Wilson et al, 1988).…”

“…This suggests that: (1) the earliest age possible for rhesus females to ovulate may be~31 months or (2) the fact that these females had lived in a seasonal environment before the start of treatment may have determined the 'window' within which first ovulation could occur. Although episodic administration of LH-releasing hormone (Wildt et al, 1980) (Krey et al, 1981;Norman & Spies, 1981;Resko et al, 1982;Terasawa et al, 1984a). Indeed, hypothalamic disconnection (Norman & Spies, 1981) and posterior hypothalamic lesions (Terasawa et al, 1984b) advance first ovulations relative to control females, but these still do not occur before 31 months of age.…”

Indirect assessment of pulsatile gonadotropin-releasing hormone release in agonadal prepubertal rhesus monkeys (Macaca mulatta)

“…Interestingly, the degree to which pulsatile GnRH release is suppressed during prepubertal development in primates appears to be sexually differentiated (see Plant 1994), a difference that is most notable following gonadectomy. For example, in the gonad-intact prepubertal female and male rhesus monkey, circulating LH and FSH levels are very low or not detected by RIA and therefore indistinguishable (Dierschke et al 1974, Terasawa et al 1984, Plant 1985. At a comparable age in the agonadal state, however, the female exhibits elevated plasma FSH concentrations and distinct increments in nocturnal LH secretion (Winter et al 1987, while in the male, gonadotropin levels remain not detected (Plant 1985).…”