Aversion and attraction through olfaction

Abstract

Sensory cues that predict reward or punishment are fundamental drivers of animal behavior. For example, attractive odors of palatable food or a potential mate predict reward, while aversive odors of pathogen-laced food or a predator predict punishment. Aversive and attractive odors can be detected by intermingled sensory neurons that express highly related olfactory receptors and display similar central projections. These findings raise basic questions of how innate odor valence is extracted from olfactory circuits, how such circuits are developmentally endowed and modulated by state, and how innate and learned odor responses are related. Here, we review odors, receptors and neural circuits associated with stimulus valence, discussing salient principles derived from studies on nematodes, insects and vertebrates. Understanding the organization of neural circuitry that mediates odor aversion and attraction will provide key insights into how the brain functions.

Figure 1. Aversion and attraction in C. elegans

(A) Location of olfactory sensory neurons (AWA, AWB, AWC) in the worm head. Each AWA, AWB, and AWC neuron pair extends sensory cilia that are embedded in the sheath near the amphid pore. Image adapted from [134]. (B) AWC neurons are inhibited by attractive odors, and control turning rate by gating the activity of AIB and AIY interneurons through glutamate release.

Figure 2. Anatomical organization of fly olfactory circuits

(A) Distinct olfactory circuits mediate innate (blue) and learned (red) odor responses. Image adapted from [76]. (B) Glomeruli in the fly antennal lobe that mediate aversion (red) and attraction (blue) are intermingled and can be adjacent. Depicted glomeruli respond to vinegar (low threshold: VA2, DM1; high threshold: DM5), farnesol (DC3), amines (VM1), geosmin (DA2), acids (DC4), and CO₂ (V). Anterior to posterior antennal lobe representations are depicted clockwise from the top left. Image adapted from [63, 64].

Figure 3. Olfactory pathways in the mouse

(A) The main olfactory system involves different brain nuclei that may mediate innate (blue) and learned (red) responses. Signals from the main olfactory epithelium (MOE) are transmitted to the main olfactory bulb (MOB) and then to several brain regions including the anterior olfactory nucleus (AON), piriform cortex (PC), olfactory tubercle (OT), posterolateral cortical amygdaloid nucleus (PLCN), and anterior cortical nucleus (ACN). In the accessory olfactory pathway (green), signals from the VNO are sent to the accessory olfactory bulb (AOB) and then to the medial amygdala (MeA) and posteromedial cortical amygdalaoid nucleus (PMCN). (B) The adjacent projections of TAAR4 (green) and TAAR5 (red) sensory neurons were revealed by antibody staining [110].