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True S-cones are concentrated in the ventral mouse retina and wired for color detection in the upper visual field

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Cite this article as: eLife 2020;9:e56840 doi: 10.7554/eLife.56840

Abstract

Color, an important visual cue for survival, is encoded by comparing signals from photoreceptors with different spectral sensitivities. The mouse retina expresses a short wavelength-sensitive and a middle/long wavelength-sensitive opsin (S- and M-opsin), forming opposing, overlapping gradients along the dorsal-ventral axis. Here, we analyzed the distribution of all cone types across the entire retina for two commonly used mouse strains. We found, unexpectedly, that 'true S-cones' (S-opsin only) are highly concentrated (up to 30% of cones) in ventral retina. Moreover, S-cone bipolar cells (SCBCs) are also skewed towards ventral retina, with wiring patterns matching the distribution of true S-cones. In addition, true S-cones in the ventral retina form clusters, which may augment synaptic input to SCBCs. Such a unique true S-cone and SCBC connecting pattern forms a basis for mouse color vision, likely reflecting evolutionary adaption to enhance color coding for the upper visual field suitable for mice's habitat and behavior.

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All data generated or analyzed during this study are included in the manuscript and supporting files

Article and author information

Author details

  1. Francisco M Nadal-Nicolás

    Retinal Neurophysiology Section, National Eye Institute (NIH), Bethesda, United States
    For correspondence
    nadalnicolasfm@nih.gov
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4121-514X
  2. Vincent P Kunze

    Retinal Neurophysiology Section, National Eye Institute (NIH), Bethesda, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7869-9793
  3. John M Ball

    Retinal Neurophysiology Section, National Eye Institute (NIH), Bethesda, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Brian T Peng

    Retinal Neurophysiology Section, National Eye Institute (NIH), Bethesda, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Akshay Krishnan

    Retinal Neurophysiology Section, National Eye Institute (NIH), Bethesda, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Gaohui Zhou

    Retinal Neurophysiology Section, National Eye Institute (NIH), Bethesda, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Lijin Dong

    Genetic Engineering Facility, National Eye Institute (NIH), Bethesda, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Wei Li

    Retinal Neurophysiology Section, National Eye Institute (NIH), Bethesda, United States
    For correspondence
    liwei2@nei.nih.gov
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2897-649X

Funding

National Eye Institute (Intramural Research Program)

  • Wei Li

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 experiments and animal care are conducted in accordance with protocols approved by the Animal Care and Use Committee of the National Institutes of Health and following the Association for Research in Vision and Ophthalmology guidelines for the use of animals in research. The protocol was approved by the Animal Care and Use Committee of the National Institutes of Health (ASP#606).

Reviewing Editor

  1. Fred Rieke, University of Washington, United States

Publication history

  1. Received: March 12, 2020
  2. Accepted: May 28, 2020
  3. Accepted Manuscript published: May 28, 2020 (version 1)
  4. Version of Record published: June 22, 2020 (version 2)

Copyright

This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

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