Retinal direction selectivity in the absence of asymmetric starburst amacrine cell responses

Abstract

In the mammalian retina, direction-selectivity is thought to originate in the dendrites of GABAergic/cholinergic starburst amacrine cells, where it is first observed. However, here we demonstrate that direction selectivity in downstream ganglion cells remains remarkably unaffected when starburst dendrites are rendered non-directional, using a novel strategy combining a conditional GABAA α2 receptor knockout mouse with optogenetics. We show that temporal asymmetries between excitation/inhibition, arising from the differential connectivity patterns of starburst cholinergic and GABAergic synapses to ganglion cells, form the basis for a parallel mechanism generating direction selectivity. We further demonstrate that these distinct mechanisms work in a coordinated way to refine direction selectivity as the stimulus crosses the ganglion cell's receptive field. Thus, precise spatiotemporal patterns of inhibition and excitation that determine directional responses in ganglion cells are shaped by two 'core' mechanisms, both arising from distinct specializations of the starburst network.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files

Article and author information

Author details

  1. Laura Hanson

    Department of Biology, University of Victoria, Victoria, Canada
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8737-9513
  2. Santhosh Sethuramanujam

    Department of Biology, University of Victoria, Victoria, Canada
    Competing interests
    The authors declare that no competing interests exist.
  3. Geoff deRosenroll

    Department of Biology, University of Victoria, Victoria, Canada
    Competing interests
    The authors declare that no competing interests exist.
  4. Varsha Jain

    Department of Biology, University of Victoria, Victoria, Canada
    Competing interests
    The authors declare that no competing interests exist.
  5. Gautam Bhagwan Awatramani

    Department of Biology, University of Victoria, Victoria, Canada
    For correspondence
    gautam@uvic.ca
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0610-5271

Funding

Canadian Institutes of Health Research (159444)

  • Gautam Bhagwan Awatramani

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 were performed in accordance with the Canadian Council on Animal Care and approved by the Animal Care Committee (protocol 2016-015) of the University of Victoria

Reviewing Editor

  1. Fred Rieke, University of Washington, United States

Publication history

  1. Received: September 27, 2018
  2. Accepted: February 1, 2019
  3. Accepted Manuscript published: February 4, 2019 (version 1)
  4. Version of Record published: February 15, 2019 (version 2)

Copyright

© 2019, Hanson 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. Laura Hanson
  2. Santhosh Sethuramanujam
  3. Geoff deRosenroll
  4. Varsha Jain
  5. Gautam Bhagwan Awatramani
(2019)
Retinal direction selectivity in the absence of asymmetric starburst amacrine cell responses
eLife 8:e42392.
https://doi.org/10.7554/eLife.42392
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