Neuronal Fos activation in olfactory bulb and forebrain of male rats having erections in the presence of inaccessible estrous females

Abstract

Volatile odors from estrous female rats are necessary and sufficient to induce non-contact penile erections in male rats. It is not known whether these pheromones are detected by the accessory as opposed to the main olfactory system or whether they are processed by forebrain regions that receive olfactory inputs. Using nuclear Fos immunoreactivity as a marker of neuronal activation, we asked how the detection and processing of distal cues from inaccessible estrous females, which elicited non-contact penile erections, compared with the processing of sensory cues from soiled estrous bedding which did not elicit non-contact penile erections. In Experiment 1, groups of sexually experienced males were given one of five treatments. A control group was placed on clean bedding. A second group displayed non-contact penile erections when exposed to the smell, sight and sound of an estrous female restrained behind a permeable barrier. A third group was exposed to the same stimuli as the second (an estrous female) but failed to exhibit non-contact penile erections during the first hour of testing. A fourth group was placed on soiled estrous bedding, and a fifth group was allowed two ejaculations with an estrous female. All males were perfused with 4% paraformaldehyde 2 h after the onset of these respective treatments, and their brains were later processed for Fos immunoreactivity. Non-contact penile erections were observed in males that were exposed to distal cues from an estrous female but not in males exposed to soiled estrous bedding. Males that displayed non-contact penile erections or that were exposed to estrous bedding showed significantly more neuronal Fos immunoreactivity than clean-bedding controls in the nucleus accumbens core and shell, anterior and posterior medial amygdala, bed nucleus of the stria terminalis and the medial preoptic nucleus. Even greater neuronal Fos responses occurred in these regions in mated males. In Experiment 2 these same treatments were given to another cohort of sexually experienced males. Increased neuronal Fos immunoreactivity was observed in the granule and mitral cell layers of the accessory olfactory bulb of males that were either mated or exposed to estrous bedding, but not in males that displayed non-contact penile erections in response to distal cues from an estrous female. The volatile odors which presumably caused non-contact penile erections failed to stimulate significant neuronal Fos immunoreactivity in five main olfactory bulb sites examined. Even so, it seems likely that these pheromones are detected via the main olfactory system and are subsequently processed by the same projection circuit that responds to other pheromones present in estrous bedding that are incapable of eliciting non-contact penile erections.