Drosophila Fezf coordinates laminar-specific connectivity through cell-intrinsic and cell-extrinsic mechanisms

  1. Jing Peng
  2. Ivan J Santiago
  3. Curie Ahn
  4. Burak Gur
  5. C Kimberly Tsui
  6. Zhixiao Su
  7. Chundi Xu
  8. Aziz Karakhanyan
  9. Marion Silies
  10. Matthew Y Pecot  Is a corresponding author
  1. Harvard Medical School, United States
  2. European Neuroscience Institute, Germany
  3. Stanford University, United States

Abstract

Laminar arrangement of neural connections is a fundamental feature of neural circuit organization. Identifying mechanisms that coordinate neural connections within correct layers is thus vital for understanding how neural circuits are assembled. In the medulla of the Drosophila visual system neurons form connections within ten parallel layers. The M3 layer receives input from two neuron types that sequentially innervate M3 during development. Here we show that M3-specific innervation by both neurons is coordinated by Drosophila Fezf (dFezf), a conserved transcription factor that is selectively expressed by the earlier targeting input neuron. In this cell, dFezf instructs layer specificity and activates the expression of a secreted molecule (Netrin) that regulates the layer specificity of the other input neuron. We propose that employment of transcriptional modules that cell-intrinsically target neurons to specific layers, and cell-extrinsically recruit other neurons is a general mechanism for building layered networks of neural connections.

Article and author information

Author details

  1. Jing Peng

    Department of Neurobiology, Harvard Medical School, Boston, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Ivan J Santiago

    Department of Neurobiology, Harvard Medical School, Boston, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Curie Ahn

    Department of Neurobiology, Harvard Medical School, Boston, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Burak Gur

    European Neuroscience Institute, Göttingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  5. C Kimberly Tsui

    Department of Genetics, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Zhixiao Su

    Department of Neurobiology, Harvard Medical School, Boston, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Chundi Xu

    Department of Neurobiology, Harvard Medical School, Boston, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Aziz Karakhanyan

    Department of Neurobiology, Harvard Medical School, Boston, United States
    Competing interests
    The authors declare that no competing interests exist.
  9. Marion Silies

    European Neuroscience Institute, Göttingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  10. Matthew Y Pecot

    Department of Neurobiology, Harvard Medical School, Boston, United States
    For correspondence
    matthew_pecot@hms.harvard.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8241-8002

Funding

Lefler Center for the Study of Neurological Disorders

  • Matthew Y Pecot

McKnight Foundation

  • Matthew Y Pecot

Howard Hughes Medical Institute (Gilliam Fellowship for Advanced Study)

  • Ivan J Santiago

Lefler Center for the Study of Neurological Disorders

  • Jing Peng

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

Reviewing Editor

  1. Liqun Luo, Howard Hughes Medical Institute, Stanford University, United States

Version history

  1. Received: November 30, 2017
  2. Accepted: March 6, 2018
  3. Accepted Manuscript published: March 7, 2018 (version 1)
  4. Version of Record published: March 15, 2018 (version 2)

Copyright

© 2018, Peng 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.

Metrics

  • 3,157
    views
  • 333
    downloads
  • 38
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Jing Peng
  2. Ivan J Santiago
  3. Curie Ahn
  4. Burak Gur
  5. C Kimberly Tsui
  6. Zhixiao Su
  7. Chundi Xu
  8. Aziz Karakhanyan
  9. Marion Silies
  10. Matthew Y Pecot
(2018)
Drosophila Fezf coordinates laminar-specific connectivity through cell-intrinsic and cell-extrinsic mechanisms
eLife 7:e33962.
https://doi.org/10.7554/eLife.33962

Share this article

https://doi.org/10.7554/eLife.33962