The main but not the accessory olfactory system is involved in the processing of socially relevant chemosignals in ungulates

Abstract

Ungulates like sheep and goats have, like many other mammalian species, two complementary olfactory systems. The relative role played by these two systems has long been of interest regarding the sensory control of social behavior. The study of ungulate social behavior could represent a complimentary alternative to rodent studies because they live in a more natural environment and their social behaviors depend heavily on olfaction. In addition, the relative size of the main olfactory bulb (MOB) [in comparison to the accessory olfactory bulb (AOB)] is more developed than in many other lissencephalic species like rodents. In this review, we present data showing a clear involvement of the main olfactory system in two well-characterized social situations under olfactory control in ungulates, namely maternal behavior and offspring recognition at birth and the reactivation of the gonadotropic axis of females exposed to males during the anestrous season. In conclusion, we discuss the apparent discrepancy between the absence of evidence for a role of the vomeronasal system in ungulate social behavior and the existence of a developed accessory olfactory system in these species.

Keywords: male effect; maternal behavior; olfactory learning; olfactory systems; sociosexual interactions; vomeronasal organ.

Figure 1

Simplified representation of the processing of olfactory information in the case of both offspring recognition and male effect in sheep. (A) In the case of offspring recognition, lamb odor is processed by the main olfactory bulb and then by both the medial and cortical nuclei of the amygdala, before to reach the medial preoptic area, which is involved in the expression of maternal care and offspring acceptance at suckling. (B) In the case of the male effect, the main olfactory bulb is also involved but then only the cortical amygdala seems to be in charge of the processing of male odor. The final output is the GnRH pulse generator at least partly localized in the arcuate nucleus which controls LH pulsatility and the reactivation of the gonadotrope axis. Arc, arcuate nucleus; CoA, cortical amygdala; MeA, medial amygdala; MOB, main olfactory bulb; MPOA, medial preoptic area.