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

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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 GABA_A 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.

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

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Laura Hanson

Department of Biology, University of Victoria, Victoria, Canada

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-8737-9513
Santhosh Sethuramanujam

Department of Biology, University of Victoria, Victoria, Canada

Competing interests
The authors declare that no competing interests exist.
Geoff deRosenroll

Department of Biology, University of Victoria, Victoria, Canada

Competing interests
The authors declare that no competing interests exist.
Varsha Jain

Department of Biology, University of Victoria, Victoria, Canada

Competing interests
The authors declare that no competing interests exist.
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.

"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

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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.