The comprehensive connectome of a neural substrate for 'ON' motion detection in Drosophila

  1. Shin-ya Takemura  Is a corresponding author
  2. Aljoscha Nern
  3. Dmitri B Chklovskii
  4. Louis K Scheffer
  5. Gerald M Rubin
  6. Ian A Meinertzhagen
  1. Janelia Research Campus, Howard Hughes Medical Institute, United States
  2. Simons Foundation, United States

Abstract

Analysing computations in neural circuits often uses simplified models because the actual neuronal implementation is not known. For example, a problem in vision, how the eye detects image motion, has long been analysed using Hassenstein-Reichardt (HR) detector or Barlow-Levick (BL) models. These both simulate motion detection well, but the exact neuronal circuits undertaking these tasks remain elusive. We reconstructed a comprehensive connectome of the circuits of Drosophila's motion-sensing T4 cells using a novel EM technique. We uncover complex T4 inputs and reveal that putative excitatory inputs cluster at T4's dendrite shafts, while inhibitory inputs localize to the bases. Consistent with our previous study, we reveal that Mi1 and Tm3 cells provide most synaptic contacts onto T4. We are, however, unable to reproduce the spatial offset between these cells reported previously. Our comprehensive connectome reveals complex circuits that include candidate anatomical substrates for both HR and BL types of motion detectors.

Article and author information

Author details

  1. Shin-ya Takemura

    Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States
    For correspondence
    takemuras@janelia.hhmi.org
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2400-6426
  2. Aljoscha Nern

    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:" 0000-0002-3822-489X
  3. Dmitri B Chklovskii

    Simons Center for Data Analysis, Simons Foundation, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Louis K Scheffer

    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:" 0000-0002-3289-6564
  5. Gerald M Rubin

    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:" 0000-0001-8762-8703
  6. Ian A Meinertzhagen

    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:" 0000-0002-6578-4526

Funding

Howard Hughes Medical Institute

  • Shin-ya Takemura
  • Aljoscha Nern
  • Dmitri B Chklovskii
  • Louis K Scheffer
  • Gerald M Rubin
  • Ian A Meinertzhagen

Natural Sciences and Engineering Research Council of Canada

  • Ian A Meinertzhagen

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

Reviewing Editor

  1. Alexander Borst, Max Planck Institute of Neurobiology, Germany

Version history

  1. Received: December 19, 2016
  2. Accepted: April 13, 2017
  3. Accepted Manuscript published: April 22, 2017 (version 1)
  4. Version of Record published: May 17, 2017 (version 2)
  5. Version of Record updated: June 23, 2017 (version 3)

Copyright

© 2017, Takemura 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. Shin-ya Takemura
  2. Aljoscha Nern
  3. Dmitri B Chklovskii
  4. Louis K Scheffer
  5. Gerald M Rubin
  6. Ian A Meinertzhagen
(2017)
The comprehensive connectome of a neural substrate for 'ON' motion detection in Drosophila
eLife 6:e24394.
https://doi.org/10.7554/eLife.24394

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https://doi.org/10.7554/eLife.24394

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