Local synaptic inputs support opposing, network-specific odor representations in a widely projecting modulatory neuron

  1. Xiaonan Zhang
  2. Kaylynn Coates
  3. Andrew M Dacks
  4. Cengiz Günay
  5. J Scott Lauritzen
  6. Feng Li
  7. Steven A Calle-Schuler
  8. Davi Bock
  9. Quentin Gaudry  Is a corresponding author
  1. University of Maryland, United States
  2. West Virginia University, United States
  3. Georgia Gwinnett College, United States
  4. Janelia Research Campus, Howard Hughes Medical Institute, United States

Abstract

Serotonin plays different roles across networks within the same sensory modality. Previously, we used whole-cell electrophysiology in Drosophila to show that serotonergic neurons innervating the first olfactory relay are inhibited by odorants (Zhang and Gaudry, 2016). Here we show that network-spanning serotonergic neurons segregate information about stimulus features, odor intensity and identity, by using opposing coding schemes in different olfactory neuropil. A pair of serotonergic neurons (the CSDns) innervate the antennal lobe and lateral horn, which are first and second order neuropils. CSDn processes in the antennal lobe are inhibited by odors in an identity independent manner. In the lateral horn, CSDn processes are excited in an odor identity dependent manner. Using functional imaging, modeling, and EM reconstruction, we demonstrate that antennal lobe derived inhibition arises from local GABAergic inputs and acts as a means of gain control on branch specific inputs that the CSDns receive within the lateral horn.

Data availability

All data is publicly available at https://drive.google.com/drive/folders/1KVh6aIQ6S_MWyuY7JOwXZ0efgrReFTPv?usp=sharing

The following previously published data sets were used

Article and author information

Author details

  1. Xiaonan Zhang

    Department of Biology, University of Maryland, College Park, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3181-3648
  2. Kaylynn Coates

    Department of Biology, West Virginia University, Morgantown, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2592-8908
  3. Andrew M Dacks

    Department of Biology, West Virginia University, Morgantown, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6805-4211
  4. Cengiz Günay

    School of Science and Technology, Georgia Gwinnett College, Lawrenceville, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7586-571X
  5. J Scott Lauritzen

    Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Feng Li

    Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Steven A Calle-Schuler

    Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Davi Bock

    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:" 0000-0002-8218-7926
  9. Quentin Gaudry

    Department of Biology, University of Maryland, College Park, United States
    For correspondence
    qgaudry@umd.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6869-1253

Funding

Whitehall Foundation

  • Quentin Gaudry

National Institute on Deafness and Other Communication Disorders (R21 DC015873-02)

  • Quentin Gaudry

National Institute on Deafness and Other Communication Disorders (RO1 DC016293)

  • Andrew M Dacks
  • Quentin Gaudry

Georgia Gwinnett College VPASA Seed Fund

  • Cengiz Günay

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

Reviewing Editor

  1. Mani Ramaswami, Trinity College Dublin, Ireland

Version history

  1. Received: March 14, 2019
  2. Accepted: July 1, 2019
  3. Accepted Manuscript published: July 2, 2019 (version 1)
  4. Version of Record published: July 26, 2019 (version 2)

Copyright

© 2019, Zhang 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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  1. Xiaonan Zhang
  2. Kaylynn Coates
  3. Andrew M Dacks
  4. Cengiz Günay
  5. J Scott Lauritzen
  6. Feng Li
  7. Steven A Calle-Schuler
  8. Davi Bock
  9. Quentin Gaudry
(2019)
Local synaptic inputs support opposing, network-specific odor representations in a widely projecting modulatory neuron
eLife 8:e46839.
https://doi.org/10.7554/eLife.46839

Share this article

https://doi.org/10.7554/eLife.46839

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