The cell adhesion molecule Sdk1 shapes assembly of a retinal circuit that detects localized edges

Abstract

Nearly 50 different mouse retinal ganglion cell (RGC) types sample the visual scene for distinct features. RGC feature selectivity arises from their synapses with a specific subset of amacrine (AC) and bipolar cell (BC) types, but how RGC dendrites arborize and collect input from these specific subsets remains poorly understood. Here we examine the hypothesis that RGCs employ molecular recognition systems to meet this challenge. By combining calcium imaging and type-specific histological stains we define a family of circuits that express the recognition molecule Sidekick 1 (Sdk1) which include a novel RGC type (S1-RGC) that responds to local edges. Genetic and physiological studies revealed that Sdk1 loss selectively disrupts S1-RGC visual responses which result from a loss of excitatory and inhibitory inputs and selective dendritic deficits on this neuron. We conclude that Sdk1 shapes dendrite growth and wiring to help S1-RGCs become feature selective.

Data availability

Sample registration fields, registration code, and GCaMP6f datasets are available at Dryad (https://doi.org/10.5061/dryad.4xgxd2593).

The following data sets were generated
The following previously published data sets were used

Article and author information

Author details

  1. Pierre-Luc Rochon

    McGill University, Montreal, Canada
    Competing interests
    The authors declare that no competing interests exist.
  2. Catherine Theriault

    McGill University, Montreal, Canada
    Competing interests
    The authors declare that no competing interests exist.
  3. Aline Giselle Rangel Olguin

    McGill University, Montreal, Canada
    Competing interests
    The authors declare that no competing interests exist.
  4. Arjun Krishnaswamy

    McGill University, Montreal, Canada
    For correspondence
    arjun.krishnaswamy@mcgill.ca
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7706-4657

Funding

Canadian Institutes of Health Research (project grant)

  • Arjun Krishnaswamy

Natural Sciences and Engineering Research Council of Canada (discovery grant)

  • Arjun Krishnaswamy

Canadian Institutes of Health Research (Graduate Fellowship)

  • Pierre-Luc Rochon

Fonds de Recherche du Québec - Santé (Graduate Fellowship)

  • Aline Giselle Rangel Olguin

Consejo Nacional de Ciencia y Tecnología (Graduate Fellowship)

  • Aline Giselle Rangel Olguin

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

Ethics

Animal experimentation: Animals were used in accordance with the rules and regulations established by the Canadian Council on Animal Care and protocol (2017-7889) was approved by the Animal Care Committee at McGill University

Reviewing Editor

  1. Marla B Feller, University of California, Berkeley, United States

Publication history

  1. Received: June 1, 2021
  2. Preprint posted: June 9, 2021 (view preprint)
  3. Accepted: September 11, 2021
  4. Accepted Manuscript published: September 21, 2021 (version 1)
  5. Version of Record published: October 13, 2021 (version 2)

Copyright

© 2021, Rochon 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. Pierre-Luc Rochon
  2. Catherine Theriault
  3. Aline Giselle Rangel Olguin
  4. Arjun Krishnaswamy
(2021)
The cell adhesion molecule Sdk1 shapes assembly of a retinal circuit that detects localized edges
eLife 10:e70870.
https://doi.org/10.7554/eLife.70870

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