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Dissecting a circuit for olfactory behaviour in Caenorhabditis elegans

Nature volume 450, pages 63–70 (2007)Cite this article

A Corrigendum to this article was published on 20 January 2016

A Corrigendum to this article was published on 03 January 2008

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Abstract

Although many properties of the nervous system are shared among animals and systems, it is not known whether different neuronal circuits use common strategies to guide behaviour. Here we characterize information processing by Caenorhabditis elegans olfactory neurons (AWC) and interneurons (AIB and AIY) that control food- and odour-evoked behaviours. Using calcium imaging and mutations that affect specific neuronal connections, we show that AWC neurons are activated by odour removal and activate the AIB interneurons through AMPA-type glutamate receptors. The level of calcium in AIB interneurons is elevated for several minutes after odour removal, a neuronal correlate to the prolonged behavioural response to odour withdrawal. The AWC neuron inhibits AIY interneurons through glutamate-gated chloride channels; odour presentation relieves this inhibition and results in activation of AIY interneurons. The opposite regulation of AIY and AIB interneurons generates a coordinated behavioural response. Information processing by this circuit resembles information flow from vertebrate photoreceptors to ‘OFF’ bipolar and ‘ON’ bipolar neurons, indicating a conserved or convergent strategy for sensory information processing.

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Figure 1: AWC responds to odour removal.
Figure 2: Both classes of AWC neurons respond to odour removal.
Figure 3: Calcium responses in AIB and AIY interneurons.
Figure 4: AWC neurons signal through glutamate and glutamate receptors.
Figure 5: AIB and AIY require different glutamate receptors.
Figure 6: Odour-regulated turning behaviours.

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Acknowledgements

We thank the C. elegans Knockout Consortium and the Caenorhabditis Genetic Center (CGC) for strains, A. Wolstenholme for the glc-3 cDNA, P. Sengupta for the srsx-3 promoter, and M. Meister, M. Zimmer, B. Snyder, G. Lee, D. Albrecht, M. Hilliard and other Bargmann laboratory members for critical help, insights and advice. S.H.C. was supported by the Damon Runyon Cancer Research Foundation and C.I.B. is an Investigator of the Howard Hughes Medical Institute. This work was supported by the Howard Hughes Medical Institute (C.I.B.) and the Klingenstein Fund for Neuroscience (M.B.G.).

Author Contributions S.H.C. designed and performed experiments, analysed data and wrote the paper; N.C., M.T. and J.M.G. designed and performed experiments; D.R. and M.B.G. developed analytical tools; and C.I.B. designed experiments, analysed data and wrote the paper.

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Authors and Affiliations

  1. Howard Hughes Medical Institute, Laboratory of Neural Circuits and Behaviour, The Rockefeller University, New York, New York 10065, USA ,

    Sreekanth H. Chalasani, Nikos Chronis, Makoto Tsunozaki, Jesse M. Gray & Cornelia I. Bargmann

  2. Program in Neurobiology and Department of Molecular and Cellular Physiology, Stanford University, Stanford, California 94305, USA,

    Daniel Ramot & Miriam B. Goodman

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Correspondence to Cornelia I. Bargmann.

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Supplementary information

Supplementary Information

The file contains Supplementary Methods with additional references, Supplementary Figures S1-S8 with Legends, Supplementary Movie Legends and Supplementary Table S1. (PDF 27989 kb)

Supplementary Movie 1

The file contains Supplementary Movie 1 showing calcium responses in AWC after removal of stimulus. (MOV 5858 kb)

Supplementary Movie 2

The file contains Supplementary Movie 2 showing calcium responses in AIB after removal of stimulus. (MOV 4663 kb)

Supplementary Movie 3

The file contains Supplementary Movie 3 showing calcium responses in AIY after addition of stimulus. (MOV 7487 kb)

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Chalasani, S., Chronis, N., Tsunozaki, M. et al. Dissecting a circuit for olfactory behaviour in Caenorhabditis elegans. Nature 450, 63–70 (2007). https://doi.org/10.1038/nature06292

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