Local processing in neurites of VGluT3-expressing amacrine cells differentially organizes visual information

  1. Jen-Chun Hsiang
  2. Keith Johnson
  3. Linda Madisen
  4. Hongkui Zeng
  5. Daniel Kerschensteiner  Is a corresponding author
  1. Washington University School of Medicine, United States
  2. Allen Institute for Brain Science, United States

Abstract

Neurons receive synaptic inputs on extensive neurite arbors. How information is organized across arbors and how local processing in neurites contributes to circuit function is mostly unknown. Here, we used two-photon Ca2+ imaging to study visual processing in VGluT3-expressing amacrine cells (VG3‑ACs) in the mouse retina. Contrast preferences (ON vs. OFF) varied across VG3‑AC arbors depending on the laminar position of neurites, with ON responses preferring larger stimuli than OFF responses. Although arbors of neighboring cells overlap extensively, imaging population activity revealed continuous topographic maps of visual space in the VG3‑AC plexus. All VG3‑AC neurites responded strongly to object motion, but remained silent during global image motion. Thus, VG3‑AC arbors limit vertical and lateral integration of contrast and location information, respectively. We propose that this local processing enables the dense VG3‑AC plexus to contribute precise object motion signals to diverse targets without distorting target-specific contrast preferences and spatial receptive fields.

Article and author information

Author details

  1. Jen-Chun Hsiang

    Department of Ophthalmology and Visual Sciences, Washington University School of Medicine, Saint Louis, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Keith Johnson

    Department of Ophthalmology and Visual Sciences, Washington University School of Medicine, St. Louis, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Linda Madisen

    Allen Institute for Brain Science, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Hongkui Zeng

    Allen Institute for Brain Science, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0326-5878
  5. Daniel Kerschensteiner

    Department of Ophthalmology and Visual Sciences, Washington University School of Medicine, St. Louis, United States
    For correspondence
    kerschensteinerd@wustl.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6794-9056

Funding

National Eye Institute (EY023341)

  • Daniel Kerschensteiner

Research to Prevent Blindness

  • Daniel Kerschensteiner

National Eye Institute (EY026978)

  • Daniel Kerschensteiner

National Eye Institute (EY 027411)

  • Daniel Kerschensteiner

McDonnell International Scholars Academy

  • Jen-Chun Hsiang

National Institute of General Medical Sciences (GM008151-32)

  • Keith Johnson

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 in this study were approved by the Institutional Animal Care and Use Committee of Washington University School of Medicine (Protocol # 20170033 and were performed in compliance with the National Institutes of Health Guide for the Care and Use of Laboratory Animals.

Reviewing Editor

  1. Fred Rieke, Howard Hughes Medical Institute, University of Washington, United States

Publication history

  1. Received: August 16, 2017
  2. Accepted: October 11, 2017
  3. Accepted Manuscript published: October 12, 2017 (version 1)
  4. Version of Record published: October 23, 2017 (version 2)
  5. Version of Record updated: October 26, 2017 (version 3)

Copyright

© 2017, Hsiang 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. Jen-Chun Hsiang
  2. Keith Johnson
  3. Linda Madisen
  4. Hongkui Zeng
  5. Daniel Kerschensteiner
(2017)
Local processing in neurites of VGluT3-expressing amacrine cells differentially organizes visual information
eLife 6:e31307.
https://doi.org/10.7554/eLife.31307
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