The Mystery of Mammalian Puberty: How Much More Do We Know?

THE MYSTERY OF MAMMALIAN PUBERTY: HOW MUCH MORE DO WE KNOW? SERGIO R. OJEDA* Introduction The advent of sexual maturation is one of the most remarkable events in the life span of an individual. In both humans and lower species the attainment of puberty signals sexual availability, but in even the most primitive cultures puberty also represents the end of absolute parental dependence and the initiation of greater (and not necessarily welcomed) social responsibilities. The ancients were fascinated, as we are, by the somatic changes associated with sexual development but were not particularly attentive to the psychological manifestations of the process. Nowadays this is recognized as important, but in contrast to the somatic changes, little if anything is known about the influence that hormones may have in shaping and/or initiating pubertal psychological and behavioral shifts. Strong morphological , biochemical, and molecular evidence now exists, indicating that steroid hormones of gonadal and adrenal origin are recognized by specific receptor molecules in discrete brain areas, thereby affecting neuronal function in various manners. Thus, it would not be unreasonable to suspect that the underlying biological component of pubertal changes in mood, cognitive behavior, and social adaptation involves the action of steroid hormones on relevant neuronal populations. While detection of psychological changes during human puberty may require considerable experience, the somatic changes are so conspicuous that they cannot pass unnoticed by even the most casual observer. There is little doubt that a major part of these changes is determined by the integrated activation of different components of the neuroendocrine system. For instance, breast development in girls requires the concerted action of many hormones, including gonadal steroids, prolactin, and *Division of Neuroscience, Oregon Regional Primate Research Center, 505 N. W. 185th Avenue, Beaverton, Oregon 97006.© 1991 by The University of Chicago. AU rights reserved. 0031-5982/91/3403-0738$01.00 Perspectives in Biology and Medicine, 34, 3 ¦ Spring 1991 365 growth hormone, whereas muscle buildup and broadening of the shoulders in boys largely depend on androgens and growth hormone. The neuroendocrine mechanisms involved in the onset of mammalian puberty are exceedingly complex and not readily accessible to detailed scrutiny. It is thus not surprising that progress toward their elucidation has been slow and painstakingly acquired. This article does not intend to review the existing literature in the field; rather, it will attempt to provide a perspective of how our thinking has evolved over the years, where we are now, and what may be some new avenues of research that may lead us to solve the mystery of puberty. Necessarily succinct—and to provide a more focused perspective on the problem, the article will draw mainly from evidence gathered in rats and rhesus monkeys (Macaca mulatta). Those readers interested in more details are referred to recent in-depth review articles [1-3]. No attempt will be made to discuss the intriguing but still poorly understood area of psychoneuroendocrinology of puberty. Finally, in discussing the neuroendocrine regulation of puberty, we shall make the assumption that the anatomical and functional core of this process is the hypothalamic-pituitary-gonadal axis. Basic interactions within the axis include production of the neuropeptide luteinizing hormone-releasing hormone (LHRH) by a group of specialized hypothalamic neurons, the transportation of LHRH via the portal vasculature to the anterior pituitary where it stimulates gonadotropin secretion, the stimulatory effect of gonadotropins on gonadal function, and the regulatory effects of gonadal hormones on hypothalamic -pituitary function. The Early Days An early implication that sexual maturation was controlled by the central nervous system came with the clinical observation that delayed puberty in patients with Frohlich's syndrome was associated with ventral brain damage [4]. It was not until 1932, however, that Hohlweg and Junkmann [5] advanced the concept of a neural "sex center" involved in controlling puberty and reproductive cyclicity. Unexpectedly, this concept did not gain acceptance until 20 years later, when Harris and Jacobsohn conclusively demonstrated the pivotal role of the hypothalamus in controlling anterior pituitary function [6]. These findings initiated an era in which experimental situations were imposed to manipulate the neuroendocrine axis and attempts were made to measure hormonal changes. Surprisingly, many basic conclusions and core assumptions that have governed our understanding of...