1. Neuroscience

Preserving inhibition with a disinhibitory microcircuit in the retina

  1. Qiang Chen
  2. Robert G Smith  Is a corresponding author
  3. Xiaolin Huang
  4. Wei Wei  Is a corresponding author
  1. The University of Chicago, United States
  2. University of Pennsylvania, United States
https://doi.org/10.7554/eLife.62618
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  1. Qiang Chen
  2. Robert G Smith
  3. Xiaolin Huang
  4. Wei Wei
(2020)
Preserving inhibition with a disinhibitory microcircuit in the retina
eLife 9:e62618.
https://doi.org/10.7554/eLife.62618
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Abstract

Previously, we found that in the mammalian retina, inhibitory inputs onto starburst amacrine cells (SACs) are required for robust direction selectivity of On-Off direction-selective ganglion cells (On-Off DSGCs) against noisy backgrounds (Chen et al., 2016). However, the source of the inhibitory inputs to SACs and how this inhibition confers noise resilience of DSGCs are unknown. Here, we show that when visual noise is present in the background, the motion-evoked inhibition to an On-Off DSGC is preserved by a disinhibitory motif consisting of a serially connected network of neighboring SACs presynaptic to the DSGC. This preservation of inhibition by a disinhibitory motif arises from the interaction between visually evoked network dynamics and short-term synaptic plasticity at the SAC-DSGC synapse. While the disinhibitory microcircuit is well studied for its disinhibitory function in brain circuits, our results highlight the algorithmic flexibility of this motif beyond disinhibition due to the mutual influence between network and synaptic plasticity mechanisms.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files. Custom scrpts are available at https://github.com/chrischen2/eLife2020Stimulus.git

Article and author information

Author details

  1. Qiang Chen

    Department of Neurobiology, The University of Chicago, Chicago, United States
    Competing interests
    The authors declare that no competing interests exist.

  2. Robert G Smith

    Department of Neuroscience, University of Pennsylvania, Philadelphia, United States
    For correspondence
    rob@bip.anatomy.upenn.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5703-1324

  3. Xiaolin Huang

    Department of Neurobiology, The University of Chicago, Chicago, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7367-8347

  4. Wei Wei

    Department of Neurobiology, The University of Chicago, Chicago, United States
    For correspondence
    weiw@uchicago.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7771-5974

Funding

NIH (NIH R01 EY024016)

  • Wei Wei

McKnight Foundation (McKnight Scholarship Award)

  • Wei Wei

NIH (EY022070)

  • Robert G Smith

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 to maintain and use mice were in accordance with the University of Chicago Institutional Animal Care and Use Committee (Protocol number ACUP 72247) and in conformance with the NIH Guide for the Care and Use of Laboratory Animals and the Public Health Service Policy.

Copyright

© 2020, Chen 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. Qiang Chen
  2. Robert G Smith
  3. Xiaolin Huang
  4. Wei Wei
(2020)
Preserving inhibition with a disinhibitory microcircuit in the retina
eLife 9:e62618.
https://doi.org/10.7554/eLife.62618

Share this article

https://doi.org/10.7554/eLife.62618

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Further reading

    1. Neuroscience

    Stimulus-dependent recruitment of lateral inhibition underlies retinal direction selectivity

    Qiang Chen, Zhe Pei ... Wei Wei
    Research Article Updated

    The dendrites of starburst amacrine cells (SACs) in the mammalian retina are preferentially activated by motion in the centrifugal direction, a property that is important for generating direction selectivity in direction selective ganglion cells (DSGCs). A candidate mechanism underlying the centrifugal direction selectivity of SAC dendrites is synaptic inhibition onto SACs. Here we disrupted this inhibition by perturbing distinct sets of GABAergic inputs onto SACs – removing either GABA release or GABA receptors from SACs. We found that lateral inhibition onto Off SACs from non-SAC amacrine cells is required for optimal direction selectivity of the Off pathway. In contrast, lateral inhibition onto On SACs is not necessary for direction selectivity of the On pathway when the moving object is on a homogenous background, but is required when the background is noisy. These results demonstrate that distinct sets of inhibitory mechanisms are recruited to generate direction selectivity under different visual conditions.