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Neuropeptide feedback modifies odor-evoked dynamics in Caenorhabditis elegans olfactory neurons

Abstract

Many neurons release classical transmitters together with neuropeptide co-transmitters whose functions are incompletely understood. Here we define the relationship between two transmitters in the olfactory system of C. elegans, showing that a neuropeptide-to-neuropeptide feedback loop alters sensory dynamics in primary olfactory neurons. The AWC olfactory neuron is glutamatergic and also expresses the peptide NLP-1. Worms with nlp-1 mutations show increased AWC-dependent behaviors, suggesting that NLP-1 limits the normal response. The receptor for NLP-1 is the G protein-coupled receptor NPR-11, which acts in postsynaptic AIA interneurons. Feedback from AIA interneurons modulates odor-evoked calcium dynamics in AWC olfactory neurons and requires INS-1, a neuropeptide released from AIA. The neuropeptide feedback loop dampens behavioral responses to odors on short and long timescales. Our results point to neuronal dynamics as a site of behavioral regulation and reveal the ability of neuropeptide feedback to remodel sensory networks on multiple timescales.

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Figure 1: AWC releases NLP-1, which acts on NPR-11 in AIA.
Figure 2: Calcium responses in AIA interneurons require AWC glutamate and NLP-1.
Figure 3: Altered AWC calcium responses in nlp-1 and npr-11 mutants.
Figure 4: Worms with mutations in nlp-1 and npr-11 are defective in olfactory adaptation.
Figure 5: ins-1 is a component of the nlp-1-npr-11 pathway.

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Acknowledgements

We thank the C. elegans knockout consortium and the Caenorhabditis Genetic Center (CGC) for strains, Y.H. Wang for the α16Z chimera, L. Looger for GCaMP2.2b, Y. Iino for discussions about ins-1, and L. Vosshall, G. Lee, E. Feinberg, M. Tsunozaki, J. Gray, J. Garrison, P. McGrath and members of the Bargmann laboratory for critical help, advice and insights. Peptide synthesis was performed by the Proteomics Resource Center of the Rockefeller University. This work was funded by the Mathers Foundation and by the Howard Hughes Medical Institute (C.I.B.). D.R.A. holds a Career Award at the Scientific Interface from the Burroughs Wellcome Fund.

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S.H.C. conceived, conducted and interpreted experiments and co-wrote the paper; S.K., D.R.A. and L.F.A. performed and interpreted data analysis; T.N. performed HEK expression experiments; C.I.B. conceived and interpreted experiments and co-wrote the paper.

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Correspondence to Cornelia I Bargmann.

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Chalasani, S., Kato, S., Albrecht, D. et al. Neuropeptide feedback modifies odor-evoked dynamics in Caenorhabditis elegans olfactory neurons. Nat Neurosci 13, 615–621 (2010). https://doi.org/10.1038/nn.2526

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