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 the relationship between innate and learned odor responses. 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.

A Single Set of Interneurons Drives Opposite Behaviors in C. elegans

“…Valence is then determined by which of these opposing pathways is activated [3, 58]. Here, we describe a novel mechanism of valence determination that instead involves a single pathway of interneurons.…”

“…Thus, the functional connectivity of sensory neuron to interneuron synapses rapidly changes to reflect the current ethological state of the animal. Valence-encoding interneurons have been identified in mammals [3, 59], but whether their activity is modulated to drive changes in innate valence has not yet been investigated. Our finding that C. elegans can generate opposite behavioral responses to the same chemosensory input as a result of experience-dependent modulation of sensory neuron to interneuron synapses raises the possibility that similar mechanisms operate in mammals to mediate rapid changes in innate valence.…”

Trace amine-associated receptors: ligands, neural circuits, and behaviors

“…Perhaps TAAR4 and TAAR5 provide stereotyped inputs to higher-order olfactory nuclei that mediate innate odor aversion and attraction behaviors, such as the cortical amygdala [47]. Future studies are generally needed to understand the structure and function of neural circuits that process odor valence, and how connections from particular classes of sensory neurons are specified [48]. …”

Oxytocin Mediates Entrainment of Sensory Stimuli to Social Cues of Opposing Valence

“…These stimuli are thought to be processed through developmentally determined, highly specific neural pathways connecting sensory inputs to behavioral outputs (Choi et al, 2005; Dulac and Wagner, 2006; Haga-Yamanaka et al, 2014; Holy et al, 2000; Hong et al, 2014; Li and Liberles, 2015; Stowers et al, 2002). Behavioral significance can also be imposed on sensory stimuli through experience.…”

“…The ubiquity of olfactory-guided social behaviors across vertebrate (Isogai et al, 2011; Kaur et al, 2014; Leypold et al, 2002; Liberles, 2014; Lin et al, 2005; Pfaus et al, 2001; Stowers et al, 2002) and invertebrate species (Li and Liberles, 2015; Michener, 1974; Sokolowski, 2010; Suh et al, 2004) strongly suggest that olfactory systems are important for recording and processing social information. Thus, in this study, we used odor-driven behavioral paradigms that capture the essence of social learning – the pairing of an olfactory conditioned stimulus (CS) with a social unconditioned stimulus (US) – to investigate the role of Oxt in social learning.…”