Regulation by the medial amygdala of copulation and medial preoptic dopamine release

Abstract

The medial preoptic area (MPOA) is a critical integrative site for male copulatory behavior in most vertebrate species. Extracellular dopamine (DA) is increased in the MPOA of male rats immediately before and during copulation. DA agonists microinjected into the MPOA of male rats facilitate and DA antagonists inhibit sexual behavior. A major source of input to the MPOA is the medial amygdala (MeA), which processes and relays olfactory information to the MPOA. We now report that microinjections of a DA agonist into the MPOA of animals with excitotoxic lesions of the amygdala restored copulatory ability that was lost after the lesions. Moreover, radio-frequency lesions of the MeA impaired copulation and blocked the increases in extracellular DA seen in animals with sham lesions during exposure to a receptive female and during copulation. Thus, both copulatory ability and the MPOA DA response, during exposure to a receptive female and during copulation, are facilitated by input from the MeA to the MPOA.

Fig. 1.

A, B, Ejaculation frequency and total intromission frequency for animals with amygdala lesions or sham lesions in experiment 1. There were no significant differences in ejaculation frequency or total intromission frequency for animals with sham lesions. Animals with amygdala lesions displayed significantly fewer ejaculations and fewer total intromissions after surgery (POST) compared with before surgery (PRE). Microinjections of apomorphine (APO), but not vehicle (VEH), restored measures of copulation for animals with amygdala lesions. Values are expressed as mean ± SEM (*p < 0.05).

Fig. 2.

Representative perimeters of smallest lesion (black) and largest lesion (dash) for animals with ibotenic lesions of the amygdala in experiment 1. Coordinates for this figure are (top tobottom) from bregma −0.2, −0.8, and −1.2 mm, drawn from Pellegrino et al. (1979).

Fig. 3.

A–D, Behavioral measures obtained from animals with MeA lesions or sham lesions in experiment 2.A, Ejaculation frequency; B, the number of intromissions preceding the first ejaculation; C, latency to the first ejaculation, after the first intromission; andD, the postejaculatory interval. MeA lesions impaired most measures of copulation. Values are expressed as mean ± SEM (**p < 0.01; ***p < 0.001).

Fig. 4.

Levels of DA in dialysate from the MPOA of animals with MeA lesions or sham lesions. Levels represent percent changes from baseline (BL) in response to precopulatory exposure to an estrous female (PRE) during copulation (C1–C3) and after copulation (POST). Extracellular levels of DA significantly increased during the precopulatory and copulatory stages of testing for animals with sham lesions but not for animals with MeA lesions. The baseline value used for computation was obtained by dividing the value of the last baseline by the mean of all three baselines. Values are expressed as mean ± SEM (*p < 0.05; **p < 0.01).

Fig. 5.

Representative perimeters of smallest lesion (black) and largest lesion (dash) for animals with radio-frequency lesions of the MeA in experiment 2. The lateral ventricle and the dorsal third ventricle are alsoblack. Most lesions were similar to the smallest lesion depicted above. Coordinates for this figure are (top tobottom) from bregma −2.56, −3.14, and −3.60 mm, drawn from Paxinos and Watson (1998).