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C. elegans odour discrimination requires asymmetric diversity in olfactory neurons

Abstract

Caenorhabditis elegans senses at least five attractive odours with a single pair of olfactory neurons, AWC, but can distinguish among these odours in behavioural assays1. The two AWC neurons are structurally and functionally similar, but the G-protein-coupled receptor STR-2 is randomly expressed in either the left or the right AWC neuron, never in both2. Here we describe the isolation of a mutant, ky542, with specific defects in odour discrimination and odour chemotaxis. ky542 is an allele of nsy-1, a neuronal symmetry, or Nsy, mutant in which STR-2 is expressed in both AWC neurons2. Other Nsy mutants exhibit discrimination and olfactory defects like those of nsy-1 mutants. Laser ablation of the AWC neuron that does not express STR-2 (AWCOFF) recapitulates the behavioural phenotype of Nsy mutants, whereas laser ablation of the STR-2-expressing AWC neuron (AWCON) causes different chemotaxis defects. We propose that odour discrimination can be achieved by segregating the detection of different odours into distinct olfactory neurons or into unique combinations of olfactory neurons.

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Figure 1: The ky542 mutant has defects in olfaction and olfactory discrimination.
Figure 2: Nsy mutants have defects in olfaction and olfactory discrimination.
Figure 3: AWCOFF and AWCON have distinct functions in olfaction and olfactory discrimination.
Figure 4: A model for the behavioural defects observed in Nsy mutants.

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Acknowledgements

We thank A. Sagasti and N. L'Etoile for for discussions and insights into AWC asymmetry; H. Nguyen for technical assistance; S. Wicks and R. Plasterk for sharing unpublished data; C. Adler and S. Kirch for advice on microscopy; and A. Sagasti, S. Shaham, N. L’Etoile, J. Gray and C. Adler for comments on the manuscript. P.D.W. was supported by a postdoctoral fellowship from the Jane Coffin Childs Memorial Fund for Medical Research. C.I.B. is an Investigator of the Howard Hughes Medical Institute. This work was supported by a grant from the National Institutes of Health.

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Correspondence to Cornelia I. Bargmann.

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Wes, P., Bargmann, C. C. elegans odour discrimination requires asymmetric diversity in olfactory neurons. Nature 410, 698–701 (2001). https://doi.org/10.1038/35070581

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