1. Neuroscience
Download icon

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

Research Article
  • Cited 1
  • Views 1,467
  • Annotations
Cite this article as: eLife 2019;8:e42392 doi: 10.7554/eLife.42392

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.

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.

Metrics

  • 1,467
    Page views
  • 317
    Downloads
  • 1
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.

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)

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

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