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A subset of ipRGCs regulates both maturation of the circadian clock and segregation of retinogeniculate projections in mice

  1. Kylie S Chew
  2. Jordan M Renna
  3. David S McNeill
  4. Diego Carlos Fernandez
  5. William Thomas Keenan
  6. Michael B Thomsen
  7. Jennifer L Ecker
  8. Gideon S Loevinsohn
  9. Cassandra VanDunk
  10. Daniel C Vicarel
  11. Adele Tufford
  12. Shijun Weng
  13. Paul A Gray
  14. Michel Cayouette
  15. Erik D Herzog
  16. Haiqing Zhao
  17. David M Berson  Is a corresponding author
  18. Samer Hattar  Is a corresponding author
  1. Johns Hopkins University, United States
  2. University of Akron, United States
  3. National Institute of Mental Health, National Institute of Health, United States
  4. Brown University, United States
  5. Washington University, United States
  6. Insistut de Recherches Cliniques de Montréal, Canada
Research Article
  • Cited 13
  • Views 2,134
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Cite this article as: eLife 2017;6:e22861 doi: 10.7554/eLife.22861

Abstract

The visual system consists of two major subsystems, image-forming circuits that drive conscious vision and non-image-forming circuits for behaviors such as circadian photoentrainment. While historically considered non-overlapping, recent evidence has uncovered crosstalk between these subsystems. Here we investigated shared developmental mechanisms. We revealed an unprecedented role for light in the maturation of the circadian clock and discovered that intrinsically photosensitive retinal ganglion cells (ipRGCs) are critical for this refinement process. In addition, ipRGCs regulate retinal waves independent of light, and developmental ablation of a subset of ipRGCs disrupts eye-specific segregation of retinogeniculate projections. Specifically, a subset of ipRGCs, comprising ~200 cells and which project intraretinally and to circadian centers in the brain, are sufficient to mediate both of these developmental processes. Thus, this subset of ipRGCs constitute a shared node in the neural networks that mediate light-dependent maturation of the circadian clock and light-independent refinement of retinogeniculate projections.

Article and author information

Author details

  1. Kylie S Chew

    Department of Biology, Johns Hopkins University, Baltimore, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Jordan M Renna

    Department of Biology, Program in Integrated Bioscience, University of Akron, Akron, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. David S McNeill

    Department of Biology, Johns Hopkins University, Baltimore, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Diego Carlos Fernandez

    Section on Light and Circadian Rhythms, National Institute of Mental Health, National Institute of Health, Bethesda, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. William Thomas Keenan

    Department of Biology, Johns Hopkins University, Baltimore, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3381-744X
  6. Michael B Thomsen

    Department of Biology, Johns Hopkins University, Baltimore, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Jennifer L Ecker

    Department of Biology, Johns Hopkins University, Baltimore, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Gideon S Loevinsohn

    Department of Neuroscience, Brown University, Providence, United States
    Competing interests
    The authors declare that no competing interests exist.
  9. Cassandra VanDunk

    Department of Anatomy and Neurobiology, Washington University, St. Louis, United States
    Competing interests
    The authors declare that no competing interests exist.
  10. Daniel C Vicarel

    Department of Biology, Program in Integrated Bioscience, University of Akron, Akron, United States
    Competing interests
    The authors declare that no competing interests exist.
  11. Adele Tufford

    Cellular Neurobiology Research Unit, Insistut de Recherches Cliniques de Montréal, Montreal, Canada
    Competing interests
    The authors declare that no competing interests exist.
  12. Shijun Weng

    Department of Neuroscience, Brown University, Providence, United States
    Competing interests
    The authors declare that no competing interests exist.
  13. Paul A Gray

    Department of Anatomy and Neurobiology, Washington University, St. Louis, United States
    Competing interests
    The authors declare that no competing interests exist.
  14. Michel Cayouette

    Cellular Neurobiology Research Unit, Insistut de Recherches Cliniques de Montréal, Montreal, Canada
    Competing interests
    The authors declare that no competing interests exist.
  15. Erik D Herzog

    Department of Biology, Washington University, St. Louis, United States
    Competing interests
    The authors declare that no competing interests exist.
  16. Haiqing Zhao

    Department of Biology, Johns Hopkins University, Baltimore, United States
    Competing interests
    The authors declare that no competing interests exist.
  17. David M Berson

    Department of Neuroscience, Brown University, Providence, United States
    For correspondence
    david_berson@brown.edu
    Competing interests
    The authors declare that no competing interests exist.
  18. Samer Hattar

    Section on Light and Circadian Rhythms, National Institute of Mental Health, National Institute of Health, Bethesda, United States
    For correspondence
    shattar@jhu.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3124-9525

Funding

National Institute of General Medical Sciences (GM076430)

  • Samer Hattar

National Eye Institute (F32-EY20108)

  • Jordan M Renna

National Eye Institute (R15EY026255)

  • Jordan M Renna

Canadian Institutes of Health Research (MOP-77570)

  • Michel Cayouette

National Eye Institute (R01-EY019053)

  • Samer Hattar

David and Lucile Packard Foundation

  • Samer Hattar

Alfred P. Sloan Foundation

  • Samer Hattar

Johns Hopkins University

  • Samer Hattar

National Eye Institute (R01-EY017137)

  • David M Berson

National Institute on Deafness and Other Communication Disorders (DC007395)

  • Haiqing Zhao

National Institute of General Medical Sciences (R01-GM104991)

  • Erik D Herzog

National Heart, Lung, and Blood Institute (R01-HL089742)

  • Paul A Gray

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: Animals were housed and treated in accordance with NIH and IACUC guidelines, and used protocols approved by the Johns Hopkins University and Brown University Animal Care and Use Committees (Protocol numbers MO16A212 and 1010040).

Reviewing Editor

  1. Joseph S Takahashi, Howard Hughes Medical Institute, University of Texas Southwestern Medical Center, United States

Publication history

  1. Received: November 1, 2016
  2. Accepted: June 14, 2017
  3. Accepted Manuscript published: June 15, 2017 (version 1)
  4. Version of Record published: July 17, 2017 (version 2)

Copyright

© 2017, Chew 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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