c-fos expression in vomeronasal pathways of mated or pheromone- stimulated male golden hamsters: contributions from vomeronasal sensory input and expression related to mating performance

Abstract

The vomeronasal system projects to the accessory olfactory bulb (AOB), to the medial (Me) and posterior medial cortical nuclei (PMCN) of the amygdala, to the bed nucleus of the stria terminalis (BNST), and to other central structures shown to be important in mating behavior, including the medial preoptic area (MPOA). In these experiments c-fos expression was used as a marker of neural activity to identify the contribution of vomeronasal sensory input during mating behavior in male golden hamsters, either intact or with vomeronasal organs removed (VNX). Inexperienced hamsters were either stimulated with a receptive female and allowed to mate, exposed to female hamster vaginal fluid (HVF), which contains stimuli known to act through the VN system, or placed in a clean cage alone. Densely stained Fos-positive nuclei were evident in mated animals in the central VN pathway [AOB, Me, posterior medial BNST (pmBNST)] and a VN target area (MPOA). HVF-exposed animals showed Fos expression in the AOB, Me, and BNST but not MPOA. Unstimulated animals showed almost no activation. Most VNX animals exposed to females did not mate, but performed intense chemoinvestigation. They had few Fos-positive nuclei in any of these areas except the caudal pmBNST. A few VNX animals that did mate had patterns of Fos activation that were similar but less intense than those of intact mating animals, suggesting a selective activation of VN central pathways during mating regardless of VN sensory input. The main olfactory system showed low levels of Fos expression in all animals (stimulated and unstimulated). Fos expression in the MPOA and rostral pmBNST was seen only in mated animals, suggesting that these regions are concerned with mating performance or its consequences, rather than the chemosensory input that triggers it. Fos expression in the caudal encapsulated pmBNST was evident in all groups of animals that performed chemosensory investigation, regardless of VN status or mating, suggesting that this region either directs or responds to chemosensory investigation.

Fos immunoreactivity in the rat brain following consummatory elements of sexual behavior: a sex comparison

“…These ejaculation-related Fos-IR neurons were situated in the lateral part of the MEApd, separately from the Fos-IR neurons observed following intromissions. This characteristic pattern has also been described by other investigators in rats [2] and is similar to the pattern observed in male hamsters, where two clusters of cells appear following mating including ejaculation in the lateral part of the MEApd [11,18,48].…”

“…One cluster was situated in the rostral extension of the BNSTpm close to the ventricle. This cluster was also observed in male hamsters following mating including ejaculations [11]. In male rats we ob served an additional cluster of Fos positive cells in the caudal aspect of the BNSTpm, in a subregion situated close to the fornix, following ejaculation.…”

“…Several investigators have studied neural activation in the male rodent brain following copu lation using Fos immunoreactivity (IR). Increases in Fos-IR were reported in the medial preoptic area (MPOA), the bed nucleus of the stria terminalis (BNST), the medial amyg dala (MEA), and in the midbrain central tegmental field in male rats [2,37,46] and hamsters [11,18,48],…”

The main and the accessory olfactory systems interact in the control of mate recognition and sexual behavior

“…This effect of olfactory deprivation on sexual behavior may be mediated by GnRH neurons. Indeed, as mentioned previously, GnRH cells receive olfactory information from both the main and the accessory olfactory system and an icv injection with GnRH is able to overcome the absence of olfactory inputs in a way similar to that of sexual experience [29,30,77,79]. Therefore, it is possible that sexual experience modulates the relative functional efficiency of these MOB to GnRH neuron connections; these connections gaining functional efficiency only after sexual experience.…”

The evolution of pheromonal communication

“…These two sensory organs have their own distinct primary projection targets, connecting to the main olfactory bulb (MOB) and the accessory olfactory bulb (AOB) respectively, which each then connect to different forebrain nuclei comprising the main olfactory system and the vomeronasal system [11]. The MOB sends projections to secondary processing areas including the piriform cortex, the anterior olfactory nucleus and the cortical amygdala, while the AOB has bidirectional connections with the medial amygdala and the bed nucleus of stria terminalis with further output to the ventral hypothalamus [28]. While the two systems converge at the level of the amygdala [82], the segregation of the two systems and the extensive functional differences between them have given rise to the traditional view that the MOE detects volatile odorants in the environment while the VNO detects non-volatile pheromones [14].…”