Steroidal Control of Behavioural, Neuroendocrine and Brain Sexual Differentiation: Studies in a Carnivore, the Ferret

Abstract

More than 30 years have passed since the publication ( I ) showing that transplacental administration of testosterone to female guinea-pigs caused permanent changes in their ability to exhibit reproductive behaviours in response to ovarian steroids in adulthood. Over the intervening years articles have appeared which have extended this type of observation to numerous other mammalian species, including rat, hamster, gerbil, mouse, dog, ferret, pig, sheep, rhesus monkey, and marmoset (2, 3). In many instances inferences have been made about the probable existence of steroid-induced changes in the structure and function of the nervous system which underlie these changes in behaviour. These so-called 'organizational' effects of perinatal steroid exposure on the developing nervous system are often distinguished from the later 'activational' effects of these same steroids on the expression of sociosexual behaviours in adulthood. The number of different mammalian species used for mechanistic studies on the organizational effects of steroids, such as determining the precise perinatal timing of hormone action, the identity of the steroid(s) responsible for behavioural sexual differentiation, and the neural sites of steroid action, has been relatively small, and generally restricted to rodents. In the late 1970's sex steroids acting during development were first implicated in the differentiation of sexually dimorphic telencephalic structures in passerine song birds which control singing associated with courtship (4, 5). Since this early work, numerous studies have exploited the canary and zebra finch to explore mechanisms of steroid action in controlling the ontogeny of song in the male and the underlying changes in the nervous system. Other studies using the rat have explored in detail the role of androgen and oestrogen in controlling the differentiation in males of patterns of reproductive behaviour (2) as well as aspects of neural sex dimorphisms in the preoptic area/anterior hypothalamus (POA/AH) (6) and in the lumbar spinal cord (7). The concentration of mechanistic (behavioural, biochemical, neuroanatomical) studies of steroidal effects on sexually dimorphic behavioural potential in a few avian and rodent species is understandable, in light of their relative availability, low expense, and rapid time-course of neural development.Despite the substantial progress already made using these lower vertebrate models in promoting our understanding of how sex steroids influence neural and behavioural development, extrapolation of the results obtained in these studies to higher mammals including man cannot occur in the absence of some degree of empirical verification. Obviously, experimental manipulations of steroidal exposure during the development of human subjects would be unethical, thus we are left with experiments of nature (e.g. congenital adreno-genital syndrome,androgen insensitivity syndrome, and Sa-reductase deficient pseudohermaphroditism; details in later sections) with which to ask questions about the role of sex...

Neuroendocrine Regulation of GnRH Release in Induced Ovulators

“…In male ferrets (32) LH secretion was actually reduced significantly after an intromission was achieved with a female. Such sex dimorphisms in mating-induced (and spontaneous) LH secretion probably originate from sex differences in the neural inputs to GnRH neurons since the anterior pituitary is not sexually differentiated (12,32). Gonadectomized male and female ferrets (32) showed similar LH responses to exogenous GnRH treatment, regardless of whether they were tested with or without concurrent estradiol treatment.…”

“…Likewise, there is little indication that administration of estradiol with or without progesterone induces preovulatory LH secretion in induced ovulators (e.g., 12,13,102,149,150,197). In addition, there is no clear evidence that progesterone has any positive feedback actions on LH release in induced ovulators.…”

“…By contrast, induced ovulating species generally do not show steroid-induced preovulatory LH surges. Regimens of estradiol treatment, either with or without concurrent progesterone, that successfully induced LH surges in rats failed to stimulate LH secretion in rabbits (197), voles (149,150), or ferrets (12). The cat seems to be an exception to this rule in which spontaneous ovulations have been observed occasionally in group-housed females (85,123).…”

Nares Occlusion Eliminates Heterosexual Partner Selection without Disrupting Coitus in Ferrets of Both Sexes

“…In the ferret, a carnivore, the preference of males to approach and copulate with estrous females is organized perinatally via the neural action of testosterone secreted by the testes (Baum et al, 1990a). The expression of male-typical partner preference has been linked to the differentiation in male ferrets of a sexually dimorphic nucleus in the dorsal medial preoptic area/anterior hypothalamus (dmPOA/ AH; for review, see Baum et al, 1990b).…”

Sexual Dimorphisms in Avian and Reptilian Courtship: Two Systems that Do Not Play by Mammalian Rules

“…The same steroid, estradiol, induces the development of masculine sexual behavior in many mammals while it prevents masculine development (or establishes feminine development) in avian species [Adkins-Regan, 1981;Feder, 1981;Whalen et al, 1985]. Testosterone or estradiol also inhibit the development of receptive copulatory behaviors in several mammalian species [Whalen et al, 1985;Yahr, 1988], although examples exist in mammals and birds (ferret, rhesus monkey and Japanese quail) in which female receptivity appears not to be organized by gonadal steroids [Adkins-Regan, 1981;Sachs and Meisel, 1988;Baum et al, 1990]. Results such as these suggest that it is critical to take a comparative approach in the investigation of neuroendocrine mechanisms mediating behavioral differences.…”