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ON selectivity in Drosophila vision is a multisynaptic process involving both glutamatergic and GABAergic inhibition

  1. Sebastian Molina-Obando
  2. Juan Felipe Vargas-Fique
  3. Miriam Henning
  4. Burak Gür
  5. T Moritz Schladt
  6. Junaid Akhtar
  7. Thomas K Berger
  8. Marion Silies  Is a corresponding author
  1. Johannes Gutenberg Universität Mainz, Germany
  2. Center of Advanced European Research (Caesar), Germany
Research Article
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Cite this article as: eLife 2019;8:e49373 doi: 10.7554/eLife.49373

Abstract

Sensory systems sequentially extract increasingly complex features. ON and OFF pathways, for example, encode increases or decreases of a stimulus from a common input. This ON/OFF pathway split is thought to occur at individual synaptic connections through a sign-inverting synapse in one of the pathways. Here, we show that ON selectivity is a multisynaptic process in the Drosophila visual system. A pharmacogenetics approach demonstrates that both glutamatergic inhibition through GluClα and GABAergic inhibition through Rdl mediate ON responses. Although neurons postsynaptic to the glutamatergic ON pathway input L1 lose all responses in GluClα mutants, they are resistant to a cell-type-specific loss of GluClα. This shows that ON selectivity is distributed across multiple synapses, and raises the possibility that cell-type-specific manipulations might reveal similar strategies in other sensory systems. Thus, sensory coding is more distributed than predicted by simple circuit motifs, allowing for robust neural processing.

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Author details

  1. Sebastian Molina-Obando

    Institute of Developmental Biology and Neurobiology, Johannes Gutenberg Universität Mainz, Mainz, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1222-723X
  2. Juan Felipe Vargas-Fique

    Institute of Developmental Biology and Neurobiology, Johannes Gutenberg Universität Mainz, Mainz, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Miriam Henning

    Institute of Developmental Biology and Neurobiology, Johannes Gutenberg Universität Mainz, Mainz, Germany
    Competing interests
    The authors declare that no competing interests exist.
  4. Burak Gür

    Institute of Developmental Biology and Neurobiology, Johannes Gutenberg Universität Mainz, Mainz, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8221-9767
  5. T Moritz Schladt

    Center of Advanced European Research (Caesar), Bonn, Germany
    Competing interests
    The authors declare that no competing interests exist.
  6. Junaid Akhtar

    Institute of Developmental Biology and Neurobiology, Johannes Gutenberg Universität Mainz, Mainz, Germany
    Competing interests
    The authors declare that no competing interests exist.
  7. Thomas K Berger

    Center of Advanced European Research (Caesar), Bonn, Germany
    Competing interests
    The authors declare that no competing interests exist.
  8. Marion Silies

    Institute of Developmental Biology and Neurobiology, Johannes Gutenberg Universität Mainz, Mainz, Germany
    For correspondence
    msilies@uni-mainz.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2810-9828

Funding

Deutsche Forschungsgemeinschaft (Emmy Noether SI 1991/1-1)

  • Miriam Henning
  • Burak Gür
  • Junaid Akhtar
  • Marion Silies

Deutsche Forschungsgemeinschaft (SFB889)

  • Sebastian Molina-Obando
  • Juan Felipe Vargas-Fique

Deutsche Forschungsgemeinschaft (Project C08)

  • Sebastian Molina-Obando
  • Juan Felipe Vargas-Fique

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

Reviewing Editor

  1. Claude Desplan, New York University, United States

Publication history

  1. Received: June 16, 2019
  2. Accepted: September 18, 2019
  3. Accepted Manuscript published: September 19, 2019 (version 1)

Copyright

© 2019, Molina-Obando 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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