Arrestin-mediated desensitization enables intraneuronal olfactory discrimination in Caenorhabditis elegans

Abstract

In the mammalian olfactory system, cross-talk between olfactory signals is minimized through physical isolation: individual neurons express one or few olfactory receptors among those encoded in the genome. Physical isolation allows for segregation of stimuli during signal transduction; however, in the nematode worm Caenorhabditis elegans, ∼1,300 olfactory receptors are primarily expressed in only 32 neurons, precluding this strategy. Here, we report genetic and behavioral evidence that β-arrestin-mediated desensitization of olfactory receptors, working downstream of the kinase GRK-1, enables discrimination between intraneuronal olfactory stimuli. Our findings suggest that C. elegans exploits β-arrestin desensitization to maximize responsiveness to novel odors, allowing for behaviorally appropriate responses to olfactory stimuli despite the large number of olfactory receptors signaling in single cells. This represents a fundamentally different solution to the problem of olfactory discrimination than that which evolved in mammals, allowing for economical use of a limited number of sensory neurons.