Sexually Dimorphic Processing of Somatosensory and Chemosensory Inputs to Forebrain Luteinizing Hormone-Releasing Hormone Neurons in Mated Ferrets

Abstract

The ferret is a reflexively ovulating species in which mating induces a preovulatory LH surge in the estrous female but significantly decreases LH secretion in the breeding male. This sexually dimorphic hormonal response is reflected in a sex difference in Fos-like immunoreactivity (Fos-IR) in forebrain LHRH and non-LHRH neurons after mating. We used dual immunocytochemistry for Fos and LHRH to determine whether the sex dimorphism occurs in the initial detection and transmission or in the central processing of sensory stimuli associated with mating? We also assessed the ability of chemosensory cues alone to augment neuronal Fos-IR in the ferret forebrain. Breeding male and female ferrets were paired, whereupon the male partner achieved an intromission lasting for 16–90 min. Mated male and female subjects were always perfused 90 min after the onset of the male’s intromission. Additional male and female subjects were placed alone in a cage in which an opposite sex ferret in breeding condition had been housed for 48 h. Other control ferrets were placed alone in a clean cage. Chemosensory-stimulated and unpaired control subjects were perfused 90 min after being placed in their respective cages. In both sexes mating augmented neuronal Fos-IR in the granular layer of the main olfactory bulb, the caudal thalamic central tegmental field, and the medial amygdala, regions situated early in the putative input pathway to mediobasal hypothalamic LHRH neurons. Neuronal Fos-IR was also increased in these same forebrain regions (the central tegmental field excluded) in both sexes after exposure to chemosensory cues alone. However, more central components of this input pathway, including the preoptic area, the bed nucleus of the stria terminalis, and the ventrolateral portion of the ventromedial hypothalamus as well as the mediobasal hypothalamic LHRH neurons themselves were activated by mating only in the female. In estrous females, exposure only to chemosensory stimuli from a breeding male augmented Fos-IR in the preoptic area and the ventrolateral portion of the ventromedial hypothalamus, but not in the bed nucleus of the stria terminalis or mediobasal hypothalamic LHRH neurons. In breeding males, exposure only to chemosensory cues from an estrous female failed to affect Fos-IR in any of these proximal components of the input pathway or in LHRH neurons themselves. These results suggest that the sex dimorphism in mating-induced LH secretion reflects a sex difference in the central processing of genital-somatosensory stimuli and possibly of chemosensory inputs as well.