The functional organization of excitation and inhibition in the dendrites of mouse direction-selective ganglion cells

Abstract

Recent studies indicate that the precise timing and location of excitation and inhibition (E/I) within active dendritic trees can significantly impact neuronal function. How synaptic inputs are functionally organized at the subcellular level in intact circuits remains unclear. To address this issue, we took advantage of the retinal direction-selective ganglion cell circuit, where tuned inhibition is known to shape non-directional excitatory signals. We combined two-photon calcium imaging with genetic, pharmacological, and single-cell ablation methods to examine the extent to which inhibition 'vetoes' excitation at the level of individual dendrites of direction-selective ganglion cells. We demonstrate that inhibition accurately shapes direction selectivity independently within small dendritic segments (<10 μm) with remarkable accuracy. This suggests that the parallel processing schemes proposed for direction encoding could be more fine-grained than previously envisioned.

Data availability

All data generated or analyzed during this study are included in the manuscript and supporting files. Source data files have been provided for all Figures

Article and author information

Author details

  1. Varsha Jain

    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:" 0000-0002-1620-4177
  2. Benjamin L Murphy-Baum

    Department of Biology, University of Victoria, Victoria, Canada
    For correspondence
    bmbaum@uvic.ca
    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
  3. 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
  4. Santhosh Sethuramanujam

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

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

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

    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:" 0000-0002-0610-5271

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 University of Victoria's Animal Care Committee (Protocol 2016 (15).

Reviewing Editor

  1. Markus Meister, California Institute of Technology, United States

Publication history

  1. Received: October 22, 2019
  2. Accepted: February 24, 2020
  3. Accepted Manuscript published: February 25, 2020 (version 1)
  4. Version of Record published: March 13, 2020 (version 2)

Copyright

© 2020, Jain 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. Varsha Jain
  2. Benjamin L Murphy-Baum
  3. Geoff deRosenroll
  4. Santhosh Sethuramanujam
  5. Mike Delsey
  6. Kerry Delaney
  7. Gautam Bhagwan Awatramani
(2020)
The functional organization of excitation and inhibition in the dendrites of mouse direction-selective ganglion cells
eLife 9:e52949.
https://doi.org/10.7554/eLife.52949

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