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The Neuroendocrinology of Reproduction: an Overview1

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The Neuroendocrinology of Reproduction: an Overview1 BIOLOGY OF REPRODUCTION 20, 111-127 (1979) The Neuroendocrinology of Reproduction: An Overview1 ROGER A. GORSKI Department of Anatomy and Brain Research Institute, UCLA School of Medicine, Los Angeles, California 90024 Downloaded from https://academic.oup.com/biolreprod/article/20/1/111/4559056 by guest on 27 September 2021 INTRODUCTION isms, it may be useful to divide the reproductive Each of the preceding speakers in this process into several distinct phases (Table symposium has already reviewed one important 1). A very early step in the reproductive process facet of the neuroendocrinology of reproduc­ is the differentiation of the two individuals tion. Therefore, it is clearly unnecessary to which will eventually be capable of reproducing present a thorough review of this entire field when mature. Although the concept of the and my approach will be to attempt to present sexual differentiation of the reproductive one overall perspective of the role of the brain system is well-known for the internal reproduc­ in the reproductive process while attempting to tive organs and the external genitalia (Wilson, emphasize that which has not already been dis­ 1978), this same concept applies to brain cussed. At best, this discussion will complement function as well. With respect to the peripheral the other presentations, which together do reproductive system, remember that for a form a rather complete overview of the neuro­ period during development, the male and endocrinology of reproduction. To begin with, female are morphologically indistinguishable. it will be helpful to consider the role of the After subsequent differntiation of the gonadal brain in the reproductive process in very anlage into testis or ovary, the secretory activity general terms. of the male gonad appears to be critical for masculine differentiation of both internal A possible fundamental division of the level reproductive organs and of the external genitalia. of involvement of the brain in reproduction is This concept is apparently also directly applic­ presented in Fig. 1. Control mechanisms able to brain function (Fig. 2). It is well-estab­ which can be independent of another individual lished that the brain of the male and female rat constitute the intrinsic regulatory processes differ functionally; however, these differences involving brain, pituitary and gonad. Those in brain function are not determined directly mechanisms which involve two individuals, the by the neuronal genome, rather, these sex extrinsic regulatory processes, can be further differences in brain function are established by subdivided into those interactions which the hormone environment during the early involve general afferent stimuli or primary perinatal period, apparently by the modification sensory input such as olfaction. Since sexual of an inherently female brain (Beach, 1975; reproduction by definition involves two indivi­ Flerko, 1975; Gorski, 1971; Gorski et al., duals, the existence of this extrinsic regulatory 1977, Quadagno et al., 1977; Reinisch, 1976). system should not be surprising. However, Note that if development occurs in the absence relatively little attention has been paid to this of gonadal hormones (e.g., the intact or neo- aspect of reproduction, yet there can be impor­ natally spayed female and the neonatally tant endocrine responses to behavioral and castrated male) regardless of the genetic sex of sensory input, as will be described below. the animal, the brain is functionally female in the adult. In contrast, if differentiation occurs Sexual Differentiation of the Brain in the presence of endogenous or exogenous With respect to intrinsic regulatory mechan- gonadal steroids, such a hormone-exposed animal exhibits masculine brain function when adult. There are a number of brain functions which Original research from the author's laboratory supported by USPHS Grant HD-01182 and by the Ford have been suggested to undergo this process of Foundation. sexual differentiation, although not all in 111 112 GORSKI GENETIC FEMALE INTACT MALE NEONATALLY SPAYED FEMALE INTACT OR SPAYED FEMALE, OR NEONATALLY CASTRATED MALE CASTRATED MALE EXPOSED TO EXOGENOUS STEROIDS Downloaded from https://academic.oup.com/biolreprod/article/20/1/111/4559056 by guest on 27 September 2021 FIG. 1. Highly schematic representation of two levels of involvement of the brain in the regulation of FUNCTIONALLY FUNCTIONALLY reproduction: 1) intrinsic regulatory processes which FEMALE MALE include the reciprocal interactions between brain, pituitary (P) and gonad and 2) extrinsic regulatory FIG. 2. Schematic representation of the influence processes which involve an interaction between two of the perinatal hormone environment on the sexual individuals either at the level of special sensory input differentiation of the rat brain. Regardless of genetic (2a, e.g., olfaction, vision) or general afferent stimuli sex, at birth (or shortly before) the brain of the rat (2b, e.g., genital stimulation). Abbreviations: A, appears to be potentially female and exposure to adrenal; O, ovary; T, testis; U, uterus. gonadal steroids is required for the development of a functionally masculine brain. the rat, which is the mammal upon which the present comments will be focused. Note that 1975), gender role (Ehrhardt, 1978) and also this concept appears to apply to the regula­ territorial marking (Lumia et al., 1977). tion of pituitary secretion (Flerko, 1975; Two functional parameters of the reproduc­ Gorski, 1971; Neill, 1974), male and female sex tive neuroendocrine system can be used to behavior (Beach, 1975; Gorski, 1974; Reinisch, illustrate clearly this concept of the sexual 1976), aggressive behavior (Barr et al., 1976; differentiation of the brain. In the adult animal, vom Saal et al., 1976), social and play behavior the female rat has the potential to release (Goy and Resko, 1972; Quadagno et al., 1977), gonadotropins cyclically in the surge mode urination posturing in the dog (Beach, 1974), which is essential for ovulation (Brown-Grant, the influence of gonadal hormones on food 1974; Harlan and Gorski, 1977; Mennin and intake and body weight regulation (Nance and Gorski, 1975; Taleisnik et al., 1971) and the Gorski, 1975; Tarttelin et al., 1975), some female also exhibits lordosis behavior frequently aspects of learning behavior (Dawson et al., (Gorski, 1974). In contrast, in the adult male, 1975; Denti and Negroni, 1975; Scouten et al., even in the presence of exogenous ovarian hormones, there is no surge of luteinizing hormone (LH) nor is the genetic male able to exhibit lordosis behavior except occasionally TABLE 1. The neural regulation of reproduction. (Brown-Grant, 1974; Gorski, 1974; Gorski and Wagner, 1965; Harris, 1964; Harris and Levine, Intrinsic regulation Extrinsic regulation 1965; Taleisnik et al., 1971). If exogenous steroids are administered to rats during the Differentiation of brain Special sensory input perinatal period, what are the consequences to Puberty Olfactory cues these animals when they mature? In the case Gametogenesis Photoperiod of the male there are no apparent effects of Ovulation Visual displays Sexual behavior Vocalization such perinatal treatment provided the dose of Correlation: ovulation General sensory factors hormone is not excessive; the male will still with sexual behavior Genital stimulation exhibit the typical lack of cyclic gonadotropin Pregnancy Suckling stimulus release and only rarely exhibit lordosis behavior.. Parturition In contrast, if the female is exposed to gonadal NEUROENDOCRINE)LOGY OF REPRODUCTION 113 steroids early in life, there is a marked change; Sutherland and Gorski, 1972). Moreoever, she no longer will exhibit lordosis behavior nor antiestrogenic compounds or aromatase inhibi­ will she show the cyclic release of LH and in tors have been shown to inhibit masculinization fact such an animal is anovulatory and sterile due to testosterone injection (Booth, 1977; (Barraclough and Gorski, 1961, 1962; Gorski, Doughty and McDonald, 1974; McEwen et al., 1971, 1974; Harlan and Gorski, 1977; Harris 1977a; Vreeburg et al, 1977). It has also been and Levine, 1965). Although these results could demonstrated that within brain tissue, as represent a pharmacological artifact to exogen­ elsewhere in the body, steroids are metabolized, ous hormone exposure, the effects of neonatal and testosterone in the brain can be aromatized Downloaded from https://academic.oup.com/biolreprod/article/20/1/111/4559056 by guest on 27 September 2021 gonadectomy clearly indicate the importance of to estradiol (Naftolin et al., 1975; Selmanoff et the hormone environment for normal develop­ al., 1977). Finally, the nonaromatizable andro­ ment of brain function. If the perinatal female gen dihydrotestosterone fails to masculinize the is gonadectomized, when she is adult she still brain (Korenbrot et al., 1975; Sodersten, 1978; has the capacity (of course following ovarian Whalen and Rezek, 1974). Thus, as already transplantation) to ovulate (Gorski and Wagner, discussed with respect to behavior (Crews, 1965) and also to display high rates of lordosis 1979), we have the seemingly unusual situation responses (Gerall et al, 1973). The neonatally where estradiol appears to be the vehicle for gonadectomized female appears to be essentially masculinization of the brain. Since removal of comparable to the normal female; thus, the the ovary is without apparent consequence to ovaries may play little role in the process of sexual differentiation, it was logical to assume sexual differentiation.
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