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Sensorimotor pathway controlling stopping behavior during chemotaxis in the Drosophila melanogaster larva

  1. Ibrahim Tastekin
  2. Avinash Khandelwal
  3. David Tadres
  4. Nico D Fessner
  5. James W Truman
  6. Marta Zlatic
  7. Albert Cardona
  8. Matthieu Louis  Is a corresponding author
  1. The Barcelona Institute of Science and Technology, Spain
  2. Janelia Research Campus, Howard Hughes Medical Institute, United States
  3. University of California, Santa Barbara, United States
Research Article
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Cite this article as: eLife 2018;7:e38740 doi: 10.7554/eLife.38740

Abstract

Sensory navigation results from coordinated transitions between distinct behavioral programs. During chemotaxis in the Drosophila melanogaster larva, the detection of positive odor gradients extends runs while negative gradients promote stops and turns. This algorithm represents a foundation for the control of sensory navigation across phyla. In the present work, we identified an olfactory descending neuron, PDM-DN, which plays a pivotal role in the organization of stops and turns in response to the detection of graded changes in odor concentrations. Artificial activation of this descending neuron induces deterministic stops followed by the initiation of turning maneuvers through head casts. Using electron microscopy, we reconstructed the main pathway that connects the PDM-DN neuron to the peripheral olfactory system and to the pre-motor circuit responsible for the actuation of forward peristalsis. Our results set the stage for a detailed mechanistic analysis of the sensorimotor conversion of graded olfactory inputs into action selection to perform goal-oriented navigation.

Article and author information

Author details

  1. Ibrahim Tastekin

    EMBL-CRG Systems Biology Program, Centre for Genomic Regulation, The Barcelona Institute of Science and Technology, Barcelona, Spain
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3661-9115
  2. Avinash Khandelwal

    EMBL-CRG Systems Biology Program, Centre for Genomic Regulation, The Barcelona Institute of Science and Technology, Barcelona, Spain
    Competing interests
    The authors declare that no competing interests exist.
  3. David Tadres

    EMBL-CRG Systems Biology Program, Centre for Genomic Regulation, The Barcelona Institute of Science and Technology, Barcelona, Spain
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7570-0162
  4. Nico D Fessner

    EMBL-CRG Systems Biology Program, Centre for Genomic Regulation, The Barcelona Institute of Science and Technology, Barcelona, Spain
    Competing interests
    The authors declare that no competing interests exist.
  5. James W Truman

    Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9209-5435
  6. Marta Zlatic

    Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Albert Cardona

    Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4941-6536
  8. Matthieu Louis

    Department of Molecular, Cellular and Development Biology, University of California, Santa Barbara, Santa Barbara, United States
    For correspondence
    mlouis@lifesci.ucsb.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2267-0262

Funding

Spanish Ministry of Economy and Competitiveness (BFU2011-26208)

  • Ibrahim Tastekin
  • Avinash Khandelwal
  • David Tadres
  • Nico D Fessner
  • Matthieu Louis

EU Marie Curie FP7 Programme (ITN-FLiACT)

  • Ibrahim Tastekin
  • Matthieu Louis

Howard Hughes Medical Institute

  • James W Truman
  • Marta Zlatic
  • Albert Cardona

University of California, Santa Barbara

  • David Tadres
  • Matthieu Louis

La Caixa International PhD program

  • Avinash Khandelwal

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Ronald L Calabrese, Emory University, United States

Publication history

  1. Received: May 29, 2018
  2. Accepted: November 7, 2018
  3. Accepted Manuscript published: November 22, 2018 (version 1)
  4. Version of Record published: November 29, 2018 (version 2)

Copyright

© 2018, Tastekin et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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