Adaptation in cone photoreceptors contributes to an unexpected insensitivity of primate On parasol retinal ganglion cells to spatial structure in natural images

  1. Zhou Yu
  2. Maxwell H Turner
  3. Jacob Baudin
  4. Fred Rieke  Is a corresponding author
  1. University of Washington, United States

Abstract

Neural circuits are constructed from nonlinear building blocks, and not surprisingly overall circuit behavior is often strongly nonlinear. But neural circuits can also behave near linearly, and some circuits shift from linear to nonlinear behavior depending on stimulus conditions. Such control of nonlinear circuit behavior is fundamental to neural computation. Here, we study a surprising stimulus dependence of the responses of macaque On (but not Off) parasol retinal ganglion cells: these cells respond nonlinearly to spatial structure in some stimuli but near-linearly to spatial structure in others, including natural inputs. We show that these differences in the linearity of the integration of spatial inputs can be explained by a shift in the balance of excitatory and inhibitory synaptic inputs that originates at least partially from adaptation in the cone photoreceptors. More generally, this highlights how subtle asymmetries in signaling - here in the cone signals - can qualitatively alter circuit computation.

Data availability

Source data for Figures 2, 3, 5, and 7 is provided.

Article and author information

Author details

  1. Zhou Yu

    Department of Physiology and Biophysics, University of Washington, Seattle, United States
    Competing interests
    No competing interests declared.
  2. Maxwell H Turner

    Department of Physiology and Biophysics, University of Washington, Seattle, United States
    Competing interests
    No competing interests declared.
  3. Jacob Baudin

    Department of Physiology and Biophysics, University of Washington, Seattle, United States
    Competing interests
    No competing interests declared.
  4. Fred Rieke

    Department of Physiology and Biophysics, University of Washington, Seattle, United States
    For correspondence
    rieke@uw.edu
    Competing interests
    Fred Rieke, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1052-2609

Funding

National Institutes of Health (EY028542)

  • Fred Rieke

National Institutes of Health (F31-EY026288)

  • Maxwell H Turner

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: Experiments were performed on primate retina obtained through the Tissue Distribution Program of the University of Washington's Regional Primate Research Center. Recordings were made from retinas from Macaca fascicularis, Macaca nemestrina, and Macaca mulatta of both sexes, aged 2 through 20 years. All use of primate tissue was in accordance with the University of Washington Institutional Animal Care and Use Committee (protocol 4140-01).

Version history

  1. Received: May 22, 2021
  2. Preprint posted: June 30, 2021 (view preprint)
  3. Accepted: March 13, 2022
  4. Accepted Manuscript published: March 14, 2022 (version 1)
  5. Version of Record published: March 25, 2022 (version 2)

Copyright

© 2022, Yu 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. Zhou Yu
  2. Maxwell H Turner
  3. Jacob Baudin
  4. Fred Rieke
(2022)
Adaptation in cone photoreceptors contributes to an unexpected insensitivity of primate On parasol retinal ganglion cells to spatial structure in natural images
eLife 11:e70611.
https://doi.org/10.7554/eLife.70611

Share this article

https://doi.org/10.7554/eLife.70611

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