Olfactory preference in the male rat depends on multiple chemosensory inputs converging on the preoptic area
Research Highlights
► Lesion in the preoptic area eliminated olfactory preferences for conspecifics. ► Fos experiment suggested the conspecific odors received in the olfactory epithelium. ► Medial, but not cortical, amygdala lesion suppressed copulatory behavior. ►Both medial and cortical amygdala lesions impaired olfactory preferences. ► Large lesion including both areas failed to produce complete loss of the preference.
Introduction
Chemosensory signals emitted by conspecific individuals of opposite sexes play key roles in sexual and social behavior in most mammalian species. The signals are received in sensory neurons of the olfactory epithelium (OE) and the vomeronasal organ (VNO) and processed and relayed in the main and accessory olfactory bulbs (MOB and AOB, respectively). They are then integrated in the medial and cortical nuclei of the amygdala (MeA and CoA, respectively) and/or the preoptic area (POA). The MeA and POA include a large number of neurons with sex steroid receptors (Simerly et al., 1990), suggesting an involvement of the MeA and POA in regulating sex-specific and sex steroid-dependent olfactory preference for the odor of conspecific individuals (Xiao et al., 2004). Receptive female rats are attracted by the odor of sexually active males rather than by that of females or orchidectomized males, whereas sexually active male rats prefer the odor of receptive females over that of ovariectomized (ovx) females or of intact males (Xiao et al., 2004). In a social context, male rats usually show a distinct olfactory preference for castrated males over intact males (Xiao et al., 2004). This preference toward same-sex conspecific animals is male specific. Orchidectomy eliminates both of the preferences (Xiao et al., 2004) and hormonal replacement with either testosterone or estradiol restores them (Kondo et al., 2004).
On the other hand, we have little knowledge about the neural circuitry of olfactory preference. Chemosensory stimulation with soiled bedding collected from estrous females markedly increased the number of c-Fos immunoreactive cells in the MeA and POA of male rats (Hosokawa and Chiba, 2005, Hurtazo and Paredes, 2005, Paredes et al., 1998a, Paredes et al., 1998b). For female rats, we have reported that destruction of these areas impaired the olfactory preference for sexually active males over inactive males (Xiao et al., 2005). Small lesions in the MeA impaired noncontact penile erection in male rats induced by estrous female odors but were not sufficient to suppress the olfactory preference for estrous females (Kondo and Sachs, 2002).
In this study, we examined the effect of destruction in the POA and its chemosensory pathways—the medial and cortical nucleus of the amygdala—to clarify the neural basis of control of olfactory preferences. Infusions of ibotenic acid produced neuron-specific and axon-sparing lesions in the MeA, the CoA and the POA. In these animals, olfactory preferences were tested for three pairs of stimulus animals: (1) receptive vs. ovx females; (2) receptive females vs. intact males and (3) intact vs. orchidectomized males. The aim was to elucidate the chemosensory pathways essential for olfactory preference.
Section snippets
Animals
Male and female 8-week-old Long-Evans rats were purchased from the Institute for Animal Reproduction (Ibaraki, Japan). All the animals were housed two or three per cage under controlled temperature (23 ± 2 °C) and reversed light/dark illumination (lights off from 11:00 to 23:00) with free access to food and water. The experiments were performed according to protocols approved by the Nippon Medical School Committee for Animal Experimentation. As stimulus partners for behavioral tests, females were
Neurotoxic lesions
In all the lesioned and SHAM rats, needle tracks were identified in Nissl-stained sections. The tip of each cannula was located within the appropriate brain nucleus of each animal that demonstrated the expected damage (see below). We excluded all the data from males with insufficient or misplaced damaged regions confirmed by NeuN histochemistry in identifying the extent of the excitotoxic lesion. Finally, we had seven males with POA lesions, six with MeA lesions, five with CoA lesions and five
Discussion
Chemosensory signals play a key role in social and sexual behavior in both male and female rats. As mentioned before, the nasal cavity of the rat has two distinctive chemosensory organs: the OE involved in general olfaction and the VNO receiving pheromonal (social) odors. The signals received in the OE travel to the olfactory tubercle and the piriform cortex via the MOB; then they are delivered to various olfactory regions of the brain. In addition, some signals containing biological and innate
Acknowledgments
This study was partly supported by Grants-in-Aid for Scientific Research to Y.K. (18590225) and Y.S. (S081035) from Japan Society for the Promotion of Science.
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