Olfactory mechanisms of stereotyped behavior: on the scent of specialized circuits

Abstract

Investigation of how specialized olfactory cues, such as pheromones, are detected has primarily focused on the function of receptor neurons within a subsystem of the nasal cavity, the vomeronasal organ (VNO). Behavioral analyses have long indicated that additional, non-VNO olfactory neurons are similarly necessary for pheromone detection; however, the identity of these neurons has been a mystery. Recent molecular, behavioral, and genomic approaches have led to the identification of multiple atypical sensory circuits that display characteristics suggestive of a specialized function. This review focuses on these non-VNO receptors and neurons, and evaluates their potential for mediating stereotyped olfactory behavior in mammals.

Figure 1. Olfactory sub-systems implicated in mediating innate behavior

Upper: Organization of olfactory subsystems in the mouse; vomeronasal organ neurons (VNO) innervate the accessory olfactory bulb (AOB), canonical main olfactory epithelium (MOE) neurons project axons to the main olfactory bulb (MOB, yellow), Gruenberg ganglion (GG) neurons project to the MOB hemi-necklace (green), and molecularly specialized MOE neurons project to the MOB necklace (blue). Lower: Innate, pheromone, or specialized olfactory responses reported to be mediated through each sub-system.

Figure 2. Mechanisms encoding innate behavior: beyond the vomeronasal organ

Multiple mechanisms have been postulated to encode innate olfactory information. Three current hypotheses: A) Anatomical segregation of sensory neurons distinguishes specialized processing (red) from general odor detection (grey). The VNO and GG (represented) are being investigated to support this mechanism. B) Molecular specialization of MOE neurons may enable pheromone detection (red). GC-D (represented) or TAAR expressing neurons may utilize this mechanism. C) The MOB glomeruli may be organized in functional zones. Analysis of mice lacking the dorsal zone (shaded light) suggests its necessity for innate coding.