1. Developmental Biology
  2. Neuroscience
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The laminar organization of the Drosophila ellipsoid body is semaphorin-dependent and prevents the formation of ectopic synaptic connections

  1. Xiaojun Xie
  2. Masashi Tabuchi
  3. Matthew P Brown
  4. Sarah P Mitchell
  5. Mark N Wu
  6. Alex L Kolodkin  Is a corresponding author
  1. The Johns Hopkins University School of Medicine, United States
Research Article
  • Cited 23
  • Views 2,575
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Cite this article as: eLife 2017;6:e25328 doi: 10.7554/eLife.25328

Abstract

The ellipsoid body (EB) in the Drosophila brain is a central complex (CX) substructure that harbors circumferentially laminated ring (R) neuron axons and mediates multifaceted sensory integration and motor coordination functions. However, what regulates R axon lamination and how lamination affects R neuron function remain unknown. We show here that the EB is sequentially innervated by small-field and large-field neurons, and that early-developing EB neurons play an important regulatory role in EB laminae formation. The transmembrane proteins semaphorin-1a and plexin A function together to regulate R axon lamination. R neurons recruit both GABA and GABA-A receptors to their axon terminals in the EB, and optogenetic stimulation coupled with electrophysiological recordings show that Sema-1a–dependent R axon lamination is required for preventing the spread of synaptic inhibition between adjacent EB lamina. These results provide direct evidence that EB lamination is critical for local pre-synaptic inhibitory circuit organization.

Article and author information

Author details

  1. Xiaojun Xie

    The Solomon H. Snyder Department of Neuroscience, The Johns Hopkins University School of Medicine, Baltimore, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Masashi Tabuchi

    Department of Neurology, The Johns Hopkins University School of Medicine, Baltimore, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Matthew P Brown

    The Solomon H. Snyder Department of Neuroscience, The Johns Hopkins University School of Medicine, Baltimore, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Sarah P Mitchell

    The Solomon H. Snyder Department of Neuroscience, The Johns Hopkins University School of Medicine, Baltimore, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Mark N Wu

    The Solomon H. Snyder Department of Neuroscience, The Johns Hopkins University School of Medicine, Baltimore, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Alex L Kolodkin

    The Solomon H. Snyder Department of Neuroscience, The Johns Hopkins University School of Medicine, Baltimore, United States
    For correspondence
    kolodkin@jhmi.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7562-5513

Funding

Howard Hughes Medical Institute

  • Xiaojun Xie
  • Matthew P Brown
  • Sarah P Mitchell
  • Alex L Kolodkin

National Institutes of Health (1R01 NS079584)

  • Masashi Tabuchi
  • Mark N Wu

National Institutes of Health (1R21 NS088521)

  • Masashi Tabuchi
  • Mark N Wu

National Institutes of Health (P30 NS50274)

  • Alex L Kolodkin

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

Publication history

  1. Received: January 20, 2017
  2. Accepted: June 19, 2017
  3. Accepted Manuscript published: June 20, 2017 (version 1)
  4. Accepted Manuscript updated: June 21, 2017 (version 2)
  5. Version of Record published: July 14, 2017 (version 3)

Copyright

© 2017, Xie 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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