Genes of the major histocompatibility complex (MHC),
Summary Olfactory signals influence social interactions in a variety of species [1, 2]. In mammals, pheromones and other social cues can promote mating or aggression behaviors, can communicate information about social hierarchies, genetic identity and health status, and can contribute to associative learning [1–5]. However, the molecular, cellular and neural mechanisms underlying many olfactory-mediated social interactions remain poorly understood. Here, we report that a specialized olfactory subsystem that includes olfactory sensory neurons (OSNs) expressing the receptor guanylyl cyclase GC-D, the cyclic nucleotide-gated channel subunit CNGA3 and the carbonic anhydrase isoform CAII (GC-D+ OSNs) [6–11] is required for the acquisition of socially transmitted food preferences (STFPs) in mice. Using electrophysiological recordings from gene-targeted mice, we show that GC-D+ OSNs are highly sensitive to the volatile semiochemical carbon disulfide (CS2), a component of rodent breath and a known social signal mediating the acquisition of STFPs [12–14]. Responses to sub-micromolar concentrations of CS2 in the main olfactory epithelium or in identified GC-D+ OSNs are absent in mice lacking CNGA3 or CAII and drastically reduced in mice lacking GC-D. Mice in which GC-D+ OSN transduction mechanisms have been disrupted fail to acquire STFPs from either live or surrogate demonstrator mice and do not exhibit neuronal activation of the ventral subiculum of the hippocampus, a brain region implicated in STFP retrieval [15]. Our findings indicate that GC-D+ OSNs detect chemosignals that facilitate food-related social interactions.
In this study, we characterized more thoroughly the social behavior of vasopressin 1b receptor null (V1bR-/-) mice. We confirmed that V1bR-/- males exhibit less social aggression than their wild-type (V1bR+/+) littermates. We tested social preference by giving male subjects a choice between pairs of soiled or clean bedding. In general, V1bR+/+ mice spent significantly more time engaged in chemoinvestigation of these social stimuli than V1bR-/- mice. Male V1bR+/+ mice preferred female-soiled bedding over male-soiled bedding, male-soiled bedding over clean bedding, and female-soiled bedding over clean bedding. In contrast, V1bR-/- males failed to exhibit a preference for any bedding. This difference in behavior is not explained by an anosmic condition as there were no differences between V1bR-/- and V1bR+/+ mice in their abilities to detect a cookie buried in clean bedding, or in their ability to perform in an operant conditioning task using a fully automated liquid dilution olfactometer. In the latter task, male V1bR-/- mice were fully capable of discriminating between male and female mouse urine. The latencies to learn this task did not differ between the two genotypes. Thus, a V1bR-/- male's ability to differentiate between male and female chemosensory cues appears no different than that of a V1bR+/+ male's. We propose that the V1bR plays an important role in social motivation, perhaps by coupling the processing, integration, and/or interpretation of chemosensory cues with the appropriate behavioral response.
A carnivore, the ferret possesses a vomeronasal organ--accessory olfactory bulb (VNO-AOB) projection to the hypothalamus; however, little is known about its function. Pheromones in soiled bedding from estrous female ferrets or an artificial peppermint odor significantly augmented nuclear Fos protein immunoreactivity (Fos-IR), a marker of neural activation, in several main olfactory bulb (MOB) sites but not in the AOB of gonadectomized male and females. Testosterone propionate (TP) significantly augmented the MOB's neuronal Fos responses to estrous females' pheromones, but not to peppermint. Estrous odors, but not peppermint, also augmented neuronal Fos-IR in the medial preoptic area (mPOA) of female, but not male, subjects. Pheromones in soiled bedding from breeding male ferrets significantly augmented neuronal Fos-IR in the MOB and in the medial amygdala of gonadectomized, TP-treated male and female subjects. Again, male pheromones failed to influence neuronal Fos-IR in the AOB of either sex, and only females showed significant increases in neuronal Fos-IR in the lateral aspect of the ventromedial nucleus and mPOA. These results point to an essential role among higher mammals of the main olfactory epithelium-MOB projection to the hypothalamus in detecting and processing pheromones. Gonadectomized ferrets showed significant increases in sniffing behavior when placed on either female or male bedding. This occurred regardless of whether they had received TP or oil vehicle, suggesting that testosterone's facilitation of neuronal Fos responses to estrous females' odors in the MOB of both sexes cannot be attributed to increased scent gathering. Androgen receptor-IR was present in the MOB granule cell layer of male and female ferrets, raising the possibility that testosterone acts directly on these cells to augment their responsiveness to pheromones.
We review studies conducted in mouse and ferret that have specified roles of both the main and the accessory olfactory nervous systems in the detection and processing of body odorants (e.g., urinary pheromones, extraorbital lacrimal gland secretions, major histocompatibility complex peptide ligands, and anal scent gland secretions) that play an essential role in sex discrimination and attraction between males and females leading to mate choice and successful reproduction. We also review literature that compares the forebrain processing of inputs from the two olfactory systems in the two sexes that underlies heterosexual partner preferences. Finally, we review experiments that raise the possibility that body odorants detected by the main olfactory system contribute to mate recognition in humans.
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