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A Study of the Role of the Postnatal Testes in Determining the Ontogeny of Gonadotropin Secretion in the Male Rhesus Monkey (Macaca mulatto)^*

T. M. PLANT

Department of Physiology, University of Pittsburgh School of Medicine Pittsburgh, Pennsylvania 15261

Abstract

To further examine the role of the testes in determining the ontogeny of gonadotropin secretion in the male rhesus monkey, the time courses of circulating LH and FSH concentrations were determined using established RIAs in daytime and nighttime blood samples collected at weekly intervals from birth until 4 yr of age in intact animals (n = 7) and in males orchidectomized at approximately 1 week of age (n = 6). Estimates of plasma androgen (A) concentrations were obtained on nonchromatographed samples with a RIA that reacts with testosterone and other androgens. Plasma PRL concentrations were also determined by RIA, and body weight was monitored at weekly intervals. Testicular volumes were measured at weekly intervals after 1.8 yr of age in five animals.

In intact animals, mean daytime plasma A concentrations during the first 3 months of infantile development ranged from 1-6 ng/ml. Daytime plasma A concentrations then declined to reach 0.5-1 ng/ml by 9 months of age, where they were maintained usually until 3 yr of age when circulating levels progressively increased to reach, by approximately 3.5 yr of age, mean levels (6 ng/ml) characteristic of fully mature males. During the transition from infantile to prepubertal development, circulating LH and FSH concentrations snowed a pattern similar to that of A, with elevations during the first 2 months of life followed by a decline to undetectable concentrations. In contrast to A, however, distinct pubertal increments in circulating LH and FSH concentrations were not observed in daytime samples from intact animals. The first indication of the pubertal reactivation of the hypothalamic-pituitary-testicular axis was provided by a reemergence of nocturnal elevations in plasma A concentrations between 2-3 yr of age. These were followed shortly thereafter by detectable plasma LH concentrations in nighttime samples. Orchidectomy at 1 week of age resulted in a progressive and dramatic rise in circulating gonadotropin concentrations, which plateaued approximately 3 weeks later at values 1 order of magnitude greater than those observed in intact animals. This hypersecretion of LH and FSH was not sustained, however, and by 10 months of age, plasma gonadotropin concentrations in agonadal animals were indistinguishable from those in agematched intact controls. These low levels of the gonadotropic hormones were maintained, in the absence of the testes, for approximately 2 yr until a second or "pubertal" postcastration hypersecretion of LH and FSH was observed. Circulating gonadotropin levels rose dramatically to reach, by 3 yr of age, concentrations similar to those observed in orchidectomized infantile monkeys and in adults castrated postpubertally.

These observations provide further evidence to support the view that, in higher primates, the hiatus in gonadotropin secretion during prepubertal development is occasioned by mechanisms of extragonadal origin. Thus, it would appear that the gonadostat hypothesis, which proposes that the restraint of LH and FSH secretion during prepubertal development is occasioned by the inhibitory action of gonadal hormones on a hypersensitive hypothalamic-hypophysial apparatus, should no longer be invoked as the fundamental mechanism underlying the protracted delay in the onset of puberty in higher primates. The reactivation of the hypothalamic-pituitary apparatus in neonatally orchidectomized monkeys at an age (2V2 yr) when the initiation of the pubertal process may have been anticipated had the animals remained intact also suggests that testicular hormones have little impact on the postnatal ontogeny of central neural mechanisms that govern the intermittent release of hypothalamic GnRH.

Striking circannual like fluctuations in serum PRL concentrations were observed, after 1 yr of age, in both intact and agonadal animals throughout prepubertal and peripubertal development. On several occasions, the first evidence of a pubertal reactivation of gonadotropin secretion, namely the onset of nocturnal A secretion in intact animals and the reinitiation of FSH secretion in agonadal animals, was associated with a nadir in plasma PRL concentrations. Thus, it is possible that PRL may play a role in determining the precise timing of the onset of the pubertal process in this species. (Endocrinology 116: 1341-1350,1985)

Footnotes

^* This work was supported by NIH Grants HD-13254 and HD-08610.

To whom requests for reprints should be addressed.

Received September 21, 1984.

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