Studies in male nonprimate mammals

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Turning to males, the situation is somewhat clearer. This is probably because we have more data on males than on females, as is so often the case. If a male rat is castrated shortly after birth, on postnatal day 0 to be exact, and treated with estra-diol + progesterone when adult, he will not only display lordosis, ear wiggling and hop-darting with the same frequency as a female, bur he will also approach a sexually active male more than a receptive female. When these males received a testosterone implant in adulthood, they changed their behavior and approached a sexually receptive female more than a male (Matuszczyk et al., 1988). This fascinating result suggests that male rats are similar to females in the way that adult hormonal environment determines the preferred sex, while early hormone exposure or lack of such is of minor importance. Similar results were obtained in a study by Meyerson et al. (1979). Their males, castrated shortly after birth, also approached a male more than a female when given estradiol and they approached a female more than a male when given testosterone. Another experiment, this time performed in the residential maze, which was popular in the Netherlands some years ago as we might have noticed by now, obtained slightly different results. Males were castrated within 24 hours of birth and implanted with Silastic® capsules containing either testosterone, dihydrotestosterone or estradiol when adults. In the maze, they could approach an inaccessible female made receptive with sequential treatment of estradiol and progesterone, or an ovariectomized, non-treated female. Animals implanted with capsules containing testosterone or estradiol approached the receptive female more than the non-receptive. Dihydrotestosterone was ineffective (Merkx, 1984b). This result is somewhat different from those reported by Matuszczyk et al. (1988) and Meyerson et al. (1979), but the choices were also different. In the latter studies, the males chose between a receptive female and a male, as might be remembered, which is not at all the same as choosing between females differing in hormonal status. Had the subjects in the Merkx (1984b) study had the same choice as those in the Matuszczyk et al. (1988) and the Meyerson et al. (1979) experiments, results might have been similar. What is perhaps more important is that the neonatally castrated animals in Merkx (1984b) study responded to hormone treatments in a way identical to that of males castrated in adulthood (Merkx, 1984a). The obvious conclusion was that neonatal testicular hormones have little effect on adult sociosexual preference behavior. This coincides with the conclusion of the Matusczcyk (1988) and Meyerson et al. (1979) studies.

Instead of subjecting the experimental subjects to neonatal castration, rats can be treated with an aromatase inhibitor from birth until puberty. Since there is abundant data suggesting that estrogens are crucial for sexual differentiation in male rats (see Chapter 5), this treatment should be equivalent to castration with regard to central nervous effects. Peripheral effects of testosterone should not be blocked, though, because these effects are mediated by dihydrotestosterone. When such an experiment was done, it turned out that the male rats treated with the aro-matase inhibitor showed the same preference for odors of receptive females compared to odors of males as control rats did. The test was performed in adulthood and all subjects had been left intact. Furthermore, no group difference was found when these animals could choose between an inaccessible male and an inaccessible receptive female. On the contrary, copulatory behaviors were affected by the aro-matase inhibitor. All treated males displayed lordosis every time they were mounted and they had a reduced intensity of male sexual behaviors (Bakker et al., 1996).

Similar results were obtained in another experiment (Domínguez-Salazar et al., 2002). Here, the experimental males could interact sexually either with a male or with a receptive female during the test for sexual preference. Moreover, a group treated with an androgen receptor antagonist was included in addition to a group treated with an aromatase inhibitor. None of the treatments affected the males' intensity of approach to a receptive female, although the androgen antagonist impaired male-like copulatory behaviors. On the contrary, the aromatase inhibitor failed to modify male-like copulatory behaviors, while lordosis was much enhanced. These studies nicely coincide in suggesting that neonatal hormone manipulations have little or no influence on sexual preferences in adult animals.

Further support for this notion comes from an experiment in which dams were treated with an estrogen receptor antagonist, an androgen receptor antagonist, or vehicle. The male offspring were tested for sexual behavior and sexual preferences when adult both when unmanipulated and after treatment with testosterone. Both antagonists had a minor effect on the intensity of approach to a receptive female, but in no case did the treated males show any preference for the male. Male copu-latory behavior was affected by both antagonists. A small reduction of the proportion of animals displaying intromission and ejaculation was observed. With regard to female sexual behavior, the estrogen antagonist enhanced the propensity to respond with lordosis to a mounting male. In fact, almost every mount induced the lordosis posture (Matuszczyk and Larsson, 1995). Again, we find marked effects of early hormone manipulations on copulatory behaviors but only minor effects on the intensity of approach to a female.

I have been unable to find any study evaluating the effects of early hormonal manipulations on sexual approach behaviors in the male ferret. There are a number of studies analyzing the effects of such manipulations on copulatory behaviors, but they are not of any relevance for the present discussion. Nevertheless, I do not believe that there is any need to insist on a discussion of more data. We should already be convinced that, whereas adult copulatory behaviors may be quite heavily influenced by neonatal hormone treatment, the choice of sexual partner is much less so. This probably means that the propensity to respond to certain stimuli with the display of a stereotyped motor pattern is determined during sexual differentiation of the brain early in life. These responses are, or are similar to, reflexes and conceivably dependent on pre-established brain circuitry. The sexual incentive properties of distant stimuli do not seem to be differentiated in the same way. The responses to distant sexual incentives are, as we know quite well by now, arbitrary. There is no reason to assume that the extremely varied approach responses activated by sexual incentives should be entirely controlled by pre-established brain circuitry, not even in rats.

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