Reprogramming Chemotaxis Responses: Sensory Neurons Define Olfactory Preferences in C. elegans

Abstract

Different olfactory cues elicit distinct behaviors such as attraction, avoidance, feeding, or mating. In the nematode C. elegans, these cues are sensed by a small number of olfactory neurons, each of which expresses several different odorant receptors. The type of behavioral response elicited by an odorant could be specified by the olfactory receptor or by the olfactory neuron in which the receptor is activated. The attractive odorant diacetyl is detected by the receptor protein ODR-10, which is normally expressed in the AWA olfactory neurons. The repulsive odorant 2-nonanone is detected by the AWB olfactory neurons. Transgenic animals that express ODR-10 in AWB rather than AWA avoid diacetyl, while maintaining qualitatively normal responses to other attractive and repulsive odorants. Animals that express ODR-10 simultaneously in AWA and AWB have a defective response to diacetyl, possibly because of conflicting olfactory inputs. Thus, an animal's preference for an odor is defined by the sensory neurons that express a given odorant receptor molecule.

Generation and modulation of chemosensory behaviors in C. elegans

“…Fifth, to further emphasize the importance of avoiding noxious chemicals, the ability to sense noxious chemicals is largely segregated from the ability to respond to attractive chemicals at the level of the sensory neurons themselves (Table 1). Thus, the ASH, ADL, and AWB neurons mediate aversive behaviors more or less exclusively, whereas attraction is mediated by the remaining eight pairs of amphid chemosensory neurons [58, 65,71,72,[89][90][91]. This organization is similar to observations in the mammalian and Drosophila gustatory system, where sensory cells responding to sugars and other palatable compounds are segregated from those sensing bitter and hence, toxic compounds [92][93][94][95][96][97].…”

“…An obvious prediction from these observations is that expression of a receptor for an attractive odorant in a neuron that mediates avoidance should trigger avoidance of that chemical. This has been shown to be the case [91], underscoring that the sensory neuron, and not the molecules it expresses, is the arbiter of the behavioral outcome.…”

“…2b). Neurons use either the cyclic nucleotide or the PUFA-mediated signaling pathway, although CRs are capable of coupling to the alternate pathway upon misexpression [91].…”

Diversity and expression of odorant receptors in Drosophila

“…Molecular cloning of the gene defective in odr-10 mutants revealed it to be a seven transmembrane domain GPCR (Sengupta et al, 1996). Direct demonstration that the odr-10 protein is a diacetyl receptor came from experiments in which neurons normally non-responsive to diacetyl were reprogrammed to express odr-10, producing animals that were repelled by this normally attractive stimulus (Troemel et al, 1997). The availability of genetic approaches in Drosophila makes the generation of DOR mutants feasible and is likely to generate compelling data on how the complement of chemosensory receptors in the fly recognizes odors.…”

Reciprocal inhibition between sensory ASH and ASI neurons modulates nociception and avoidance in Caenorhabditis elegans

“…The polymodal ASH sensory neurons in C. elegans sense a variety of aversive stimuli and mediate avoidance of high osmotic, mechanical and chemical stimuli [8][9][10][11] . Notably, the neurotransmitters, such as neuropeptides, serotonin (5-HT), tyramine (TA) and octopamine (OA), have been increasingly shown to be transmitters or modulators of ASH-mediated aversive behaviours [12][13][14][15] .…”