1. Neuroscience
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Spatially displaced excitation contributes to the encoding of interrupted motion by a retinal direction-selective circuit

  1. Jennifer Ding
  2. Albert Chen
  3. Janet Chung
  4. Hector Acaron Ledesma
  5. Mofei Wu
  6. David M Berson
  7. Stephanie E Palmer  Is a corresponding author
  8. Wei Wei  Is a corresponding author
  1. The University of Chicago, United States
  2. Harvard University, United States
  3. Brown University, United States
Research Article
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Cite this article as: eLife 2021;10:e68181 doi: 10.7554/eLife.68181

Abstract

Spatially distributed excitation and inhibition collectively shape a visual neuron's receptive field (RF) properties. In the direction-selective circuit of the mammalian retina, the role of strong null-direction inhibition of On-Off direction-selective ganglion cells (On-Off DSGCs) on their direction selectivity is well-studied. However, how excitatory inputs influence the On-Off DSGC's visual response is underexplored. Here, we report that On-Off DSGCs have a spatially displaced glutamatergic receptive field along their horizontal preferred-null motion axes. This displaced receptive field contributes to DSGC null-direction spiking during interrupted motion trajectories. Theoretical analyses indicate that population responses during interrupted motion may help populations of On-Off DSGCs signal the spatial location of moving objects in complex, naturalistic visual environments. Our study highlights that the direction-selective circuit exploits separate sets of mechanisms under different stimulus conditions, and these mechanisms may help encode multiple visual features.

Data availability

Data available on Dryad Digital Repository (doi:10.5061/dryad.vq83bk3s8). Source data files have been provided for all main text and supplemental figures.

The following data sets were generated

Article and author information

Author details

  1. Jennifer Ding

    Committee on Neurobiology, The University of Chicago, Chicago, United States
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2282-6615
  2. Albert Chen

    Biophysics Graduate Program, Harvard University, Boston, United States
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9306-8703
  3. Janet Chung

    Department of Neurobiology, The University of Chicago, Chicago, United States
    Competing interests
    No competing interests declared.
  4. Hector Acaron Ledesma

    Graduate Program in Biophysical Sciences, The University of Chicago, Chicago, United States
    Competing interests
    No competing interests declared.
  5. Mofei Wu

    Department of Neurobiology, The University of Chicago, Chicago, United States
    Competing interests
    No competing interests declared.
  6. David M Berson

    Department of Neuroscience, Brown University, Providence, United States
    Competing interests
    No competing interests declared.
  7. Stephanie E Palmer

    Organismal Biology and Anatomy, The University of Chicago, Chicago, United States
    For correspondence
    sepalmer@uchicago.edu
    Competing interests
    Stephanie E Palmer, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6211-6293
  8. Wei Wei

    Department of Neurobiology, The University of Chicago, Chicago, United States
    For correspondence
    weiw@uchicago.edu
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7771-5974

Funding

NIH (R01 NS109990)

  • Wei Wei

McKnight Endowment Fund for Neuroscience (McKnight Scholarship Award)

  • Wei Wei

NSF (GRFP DGE-1746045)

  • Jennifer Ding

NIH (F31 EY029156)

  • Hector Acaron Ledesma

NSF (Career Award 1652617)

  • Stephanie E Palmer

Physics of Biological Function (PHY-1734030)

  • Stephanie E Palmer

NIH (RO1 EY012793)

  • David M Berson

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

Ethics

Animal experimentation: All procedures regarding the use of mice were in accordance with the University of Chicago Institutional Animal Care and Use Committee (IACUC) (ACUP protocol 72247) and with the NIH Guide for the Care and Use of Laboratory Animals and the Public Health Service Policy.

Reviewing Editor

  1. Fred Rieke, University of Washington, United States

Publication history

  1. Received: March 8, 2021
  2. Accepted: June 6, 2021
  3. Accepted Manuscript published: June 7, 2021 (version 1)

Copyright

© 2021, Ding 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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