In some species, including gerbils, guinea pigs, mice, rams and rats, some apparently normal males fail to mate. These kinds of animals have been named 'noncopulating (NC)'. The cause of this behavioural deficit is unknown. The present study aimed to determine whether NC male rats have alterations in the amount of androgen (AR) and oestrogen receptor alpha (ERalpha) in a neuronal circuit important for the control of male sexual behaviour; the vomeronasal projection pathway. We evaluated the number of AR and ERalpha immunoreactive (AR-IR and ERalpha-IR) cells in the accessory olfactory bulb (AOB), the bed nucleus of the stria terminalis (BNST), the anterior-dorsal medial amygdala (MeAD), the posterior dorsal amygdala (MePD) and the medial preoptic area (MPOA). The results demonstrate that the number of AR-IR cells in NC males was significantly higher compared to copulating (C) males in the MePD, but no significant differences were found in any of the other structures analysed. ERalpha-IR cells were more abundant in NC than in C males in the MeAD and the MePD. However, in the MPOA the number of ERalpha-IR cells was significantly reduced in NC males. No significant differences were found in the AOB or in the BNST. A similar pattern of results was observed when regions within these structures that are activated by Fos expression, on mating or exposure to sexually relevant cues were analysed. The differences in the number of AR and ER in particular brain areas could be associated with alterations in sexual behaviour as well as partner and olfactory preference for receptive females seen in NC male rats.

The present study investigated the role of oestrogen receptor (ER)α in the ventromedial nucleus of the hypothalamus (VMN), the preoptic area (POA), the medial amygdala (MePD) and the bed nucleus of stria terminalis (BNST) in sociosexual behaviour in female rats. This was conducted in two sets of experiments, with the VMN and POA investigated in the first set, and the MePD and BNST in the second set. The VMN and POA received intense projections from the MePD and BNST. We used a short hairpin RNA encoded within an adeno-associated viral vector directed against the gene for ERα to reduce the number of ERα in the VMN or POA (first set of experiments) or in the BNST or MePD (second set of experiments) in female rats. The rats were housed in groups of four ovariectomised females and three males in a seminatural environment for 8 days. Compared with traditional test set-ups, the seminatural environment provides an arena in which the rats can express their full behavioural repertoire, which allowed us to investigate multiple aspects of social and sexual behaviour in groups of rats. Behavioural observation was performed after oestrogen and progesterone injections. A reduction of ERα expression in the VMN or POA diminished the display of paracopulatory behaviours and lordosis responses compared to controls, whereas the lordosis quotient remained unaffected. This suggests that ERα in the VMN and POA play an important role in intrinsic sexual motivation. The reduction in ERα did not affect the social behaviour of the females, although the males sniffed and pursued the females with reduced ERα less than the controls. This suggests that the ERα in the VMN and POA is involved in the regulation of sexual attractiveness of females. The ERα in the MePD and BNST, on the other hand, plays no role in sociosexual behaviour.

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Noncopulating (NC) male rats are those males that do not mount, intromit or ejaculate when repeatedly tested with receptive females. The lack of sexual behaviour in these males is not associated with alterations in testosterone or oestradiol (E2) plasma concentrations. Instead, it has been shown that androgen receptors are higher and oestrogen receptors are lower in the medial preoptic area (MPOA) of NC male rats than those observed in copulating (C) male rats. We have also observed reduced aromatase activity in the MPOA (but not in other brain regions) of NC male rats. The aim of the present study was to determine whether testosterone or E2 implants in the MPOA of NC male rats could induce sexual behaviour. Accordingly, in Experiment 1, we evaluated the long-term effects of testosterone or E2 implants in the MPOA, the ventromedial nucleus of the hypothalamus or the medial amygdala with respect to inducing sexual behaviour in castrated C male rats. Male rats were bilaterally implanted with a guide cannula, either empty or containing testosterone or E2. Starting 1 week later, all male rats were mated once weekly for 5 months. As described previously, the site where hormone implants most consistently induced sexual behaviour in castrated C male rats was the MPOA. Experiment 1 extended these findings showing that the males continued mating even 5 months after the implant. In the second experiment, NC males were implanted in the MPOA with a guide cannula empty or filled with testosterone or E2. One week after the testosterone or E2 implant, the percentage of males that mounted and intromitted started to increase and, 5 weeks after the implant, 50% of the subjects displayed mounts and intromissions. All NC males implanted with testosterone ejaculated consistently from week 11 after the implant until the end of testing (5 months), whereas all subjects implanted with E2 ejaculated from week 16 after the implant until the end of testing. These results support the hypothesis that, in the MPOA of NC male rats, there is a hormonal alteration associated with the lack of sexual behaviour.