Spatiotemporal properties of glutamate input support direction selectivity in the dendrites of retinal starburst amacrine cells

Abstract

The asymmetric summation of kinetically distinct glutamate inputs across the dendrites of retinal 'starburst' amacrine cells is one of the several mechanisms that have been proposed to underlie their direction-selective properties, but experimentally verifying input kinetics has been a challenge. Here, we used two-photon glutamate sensor (iGluSnFR) imaging to directly measure the input kinetics across individual starburst dendrites. We found that signals measured from proximal dendrites were relatively sustained compared to those measured from distal dendrites. These differences were observed across a range of stimulus sizes and appeared to be shaped mainly by excitatory rather than inhibitory network interactions. Temporal deconvolution analysis suggests that the steady-state vesicle release rate was ~ 3 times larger at proximal sites compared to distal sites. Using a connectomics-inspired computational model, we demonstrate that input kinetics play an important role in shaping direction selectivity at low stimulus velocities. Together, these results provide direct support for the 'space-time wiring' model for direction selectivity.

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Author details

  1. Prerna Srivastava

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

    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:" 0000-0002-5431-2814
  3. Akihiro Matsumoto

    Department of Biomedicine, Aarhus University, Aarhus, Denmark
    Competing interests
    The authors declare that no competing interests exist.
  4. Tracy Michaels

    Department of Biology, University of Victoria, Victoria, Canada
    Competing interests
    The authors declare that no competing interests exist.
  5. Zachary Turple

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

    Department of Biology, University of Victoria, Victoria, Canada
    Competing interests
    The authors declare that no competing interests exist.
  7. Santhosh Sethuramanujam

    Department of Biology, University of Victoria, Victoria, Canada
    Competing interests
    The authors declare that no competing interests exist.
  8. Benjamin L Murphy-Baum

    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:" 0000-0001-6746-3091
  9. Keisuke Yonehara

    Department of Biomedicine, Aarhus University, Aarhus, Denmark
    Competing interests
    The authors declare that no competing interests exist.
  10. 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

European Research Council (638730)

  • Keisuke Yonehara

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

Reviewing Editor

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

Ethics

Animal experimentation: All procedures were performed in accordance with the Canadian Council on Animal Care and approved by the University of Victoria's Animal Care Committee, or in accordance with Danish standard ethical guidelines and were approved by the Danish National Animal Experiment Committee (Permission No. 2015-15-0201-00541; 2020-15-0201-00452).

Version history

  1. Received: July 1, 2022
  2. Preprint posted: July 13, 2022 (view preprint)
  3. Accepted: November 2, 2022
  4. Accepted Manuscript published: November 8, 2022 (version 1)
  5. Version of Record published: November 18, 2022 (version 2)

Copyright

© 2022, Srivastava 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. Prerna Srivastava
  2. Geoff deRosenroll
  3. Akihiro Matsumoto
  4. Tracy Michaels
  5. Zachary Turple
  6. Varsha Jain
  7. Santhosh Sethuramanujam
  8. Benjamin L Murphy-Baum
  9. Keisuke Yonehara
  10. Gautam Bhagwan Awatramani
(2022)
Spatiotemporal properties of glutamate input support direction selectivity in the dendrites of retinal starburst amacrine cells
eLife 11:e81533.
https://doi.org/10.7554/eLife.81533

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https://doi.org/10.7554/eLife.81533

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