Elsevier

Hormones and Behavior

Volume 59, Issue 1, January 2011, Pages 193-199
Hormones and Behavior

Olfactory preference in the male rat depends on multiple chemosensory inputs converging on the preoptic area

https://doi.org/10.1016/j.yhbeh.2010.11.011Get rights and content

Abstract

Both volatile and nonvolatile molecules are involved in chemosensory communication in rodents. Volatile odors from physically inaccessible estrous females induced increased numbers of c-Fos-positive cells in the preoptic area (POA) and in the cortical nucleus of the amygdala (CoA) of male rats. The numbers of c-Fos-positive cells in the medial nucleus of the amygdala (MeA) increased in response to the nonvolatile odors of bedding soiled with the excreta of estrous females. In an alternate choice paradigm, male rats carrying ibotenic acid lesions in either the MeA or the CoA—or a combination of both—distinguished the odors of estrous females from those of males, although the time spent sniffing the stimuli was diminished. Males with POA lesions showed complete loss of this capability. Males carrying either of the lesions did not detect differences between estrous and anestrous females or between intact and orchidectomized males. Lesions in the POA or MeA severely impaired male sexual behavior, whereas a CoA lesion had no effects. Thus, c-Fos-positive cells in the CoA might be involved in chemosensory transmission relevant to certain social contexts, but not in the execution of male sexual behavior. The POA is indispensable for both olfactory preferences and sexual behavior. The residual olfactory preference in males with MeA or CoA lesions or the combination of both could reflect an additional route for chemosensory transmission from the main olfactory bulb to the POA.

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.

References (37)

Cited by (29)

  • Why does castrated male odor attract sexually active male rats?–Attractivity induced by hypothalamus-pituitary-gonad axis block.

    2021, Physiology and Behavior
    Citation Excerpt :

    A clear evolutionary advantage is conferred by preferring opposite-sex odors. However, sexually experienced intact male rats [7, 9, 34, 35] and mice [1, 8] also show an unexpected, but robust, preference for castrated male odors compared to gonadally intact males. The initial hypothesis when observing this response was that it reflected males’ tendency to avoid gonadally intact males because they are potential adversaries.

  • The neuroendocrinology of sexual attraction

    2018, Frontiers in Neuroendocrinology
  • Hormone-dependent medial preoptic/lumbar spinal cord/autonomic coordination supporting male sexual behaviors

    2018, Molecular and Cellular Endocrinology
    Citation Excerpt :

    This outcome was later extended (Paredes and Baum, 1995) with the finding that excitotoxic lesions of the sexually dimorphic subdivision of the mPOA caused castrated, E-treated male ferrets to seek out and mate with a stud male whereas control males continued to prefer to approach and mate with an estrous female. A similar effect of electrolytic mPOA lesions was reported in the adult male rat (Paredes et al., 1998b), although a more recent study (Dhungel et al., 2011) using rats found that excitotoxic lesions of the POA eliminated males' preference to investigate female pheromones without causing a sex reversal in subjects’ mating partner preference. Taken together, results from males of several mammalian and avian species suggest that T and/or E act in neurons of the mPOA to augment both appetitive and consummatory sexual responses.

View all citing articles on Scopus
View full text