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Dissecting a circuit for olfactory behaviour in Caenorhabditis elegans

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  • Sreekanth H. Chalasani

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

  • Nikos Chronis

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

  • Makoto Tsunozaki

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

  • Jesse M. Gray

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

  • Daniel Ramot

    (Stanford University, Stanford, California 94305, USA)

  • Miriam B. Goodman

    (Stanford University, Stanford, California 94305, USA)

  • Cornelia I. Bargmann

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

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.

Suggested Citation

  • Sreekanth H. Chalasani & Nikos Chronis & Makoto Tsunozaki & Jesse M. Gray & Daniel Ramot & Miriam B. Goodman & Cornelia I. Bargmann, 2007. "Dissecting a circuit for olfactory behaviour in Caenorhabditis elegans," Nature, Nature, vol. 450(7166), pages 63-70, November.
    • Handle: RePEc:nat:nature:v:450:y:2007:i:7166:d:10.1038_nature06292
    DOI: 10.1038/nature06292
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    Cited by:

    1. Javier J How & Saket Navlakha & Sreekanth H Chalasani, 2021. "Neural network features distinguish chemosensory stimuli in Caenorhabditis elegans," PLOS Computational Biology, Public Library of Science, vol. 17(11), pages 1-38, November.
    2. Tobias Clark & Vera Hapiak & Mitchell Oakes & Holly Mills & Richard Komuniecki, 2018. "Monoamines differentially modulate neuropeptide release from distinct sites within a single neuron pair," PLOS ONE, Public Library of Science, vol. 13(5), pages 1-22, May.

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