Rod nuclear architecture determines contrast transmission of the retina and behavioral sensitivity in mice

  1. Kaushikaram Subramanian
  2. Martin Weigert
  3. Oliver Borsch
  4. Heike Petzold
  5. Alfonso Garcia-Ulloa
  6. Eugene W Myers
  7. Marius Ader
  8. Irina Solovei
  9. Moritz Kreysing  Is a corresponding author
  1. Max Planck Institute of Molecular Cell Biology and Genetics, Germany
  2. Technische Universität Dresden, Germany
  3. Ludwig Maximilians Universität, Germany

Abstract

Rod photoreceptors of nocturnal mammals display a striking inversion of nuclear architecture, which has been proposed as an evolutionary adaptation to dark environments. However, the nature of visual benefits and the underlying mechanisms remains unclear. It is widely assumed that improvements in nocturnal vision would depend on maximization of photon capture at the expense of image detail. Here we show that retinal optical quality improves 2-fold during terminal development, and that this enhancement is caused by nuclear inversion. We further demonstrate that improved retinal contrast transmission, rather than photon-budget or resolution, enhances scotopic contrast sensitivity by 18-27%, and improves motion detection capabilities up to 10-fold in dim environments. Our findings therefore add functional significance to a prominent exception of nuclear organization and establish retinal contrast transmission as a decisive determinant of mammalian visual perception.

Data availability

Data and specifications of simulations supporting the findings of this study are available via https://owncloud.mpi-cbg.de/index.php/s/SaCJjsMCfyOAaTb . The biobeam software is available publicly from: https://maweigert.github.io/biobeam

Article and author information

Author details

  1. Kaushikaram Subramanian

    Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany
    Competing interests
    The authors declare that no competing interests exist.
  2. Martin Weigert

    Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Oliver Borsch

    Center for Regenerative Therapies, Technische Universität Dresden, Dresden, Germany
    Competing interests
    The authors declare that no competing interests exist.
  4. Heike Petzold

    Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany
    Competing interests
    The authors declare that no competing interests exist.
  5. Alfonso Garcia-Ulloa

    Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany
    Competing interests
    The authors declare that no competing interests exist.
  6. Eugene W Myers

    Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany
    Competing interests
    The authors declare that no competing interests exist.
  7. Marius Ader

    Center for Regenerative Therapies, Technische Universität Dresden, Dresden, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9467-7677
  8. Irina Solovei

    Biozentrum, Ludwig Maximilians Universität, München, Germany
    Competing interests
    The authors declare that no competing interests exist.
  9. Moritz Kreysing

    Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany
    For correspondence
    kreysing@mpi-cbg.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7432-3871

Funding

Max-Planck-Gesellschaft

  • Kaushikaram Subramanian
  • Martin Weigert
  • Heike Petzold
  • Alfonso Garcia-Ulloa
  • Eugene W Myers
  • Moritz Kreysing

Technische Universität Dresden

  • Oliver Borsch
  • Marius Ader

Deutsche Forschungsgemeinschaft (AD375/6-1)

  • Oliver Borsch
  • Marius Ader

Bundesministerium für Bildung und Forschung (031L0044)

  • Kaushikaram Subramanian
  • Eugene W Myers
  • Moritz Kreysing

Deutsche Forschungsgemeinschaft (SO1054/3)

  • Irina Solovei

Deutsche Forschungsgemeinschaft (FZT111)

  • Oliver Borsch
  • Marius Ader

Deutsche Forschungsgemeinschaft (EXC68)

  • Oliver Borsch
  • Marius Ader

Deutsche Forschungsgemeinschaft (SFB1064)

  • Irina Solovei

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 animal studies were performed in accordance with European and German animal welfare legislation (Tierschutzgesetz), the ARVO Statement for the Use of Animals in Ophthalmic and Vision Research, and the NIH Guide for the care and use of laboratory work in strict pathogen-free conditions in the animal facilities of the Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany and the Center for Regenerative Therapies Dresden, Germany. Protocols were approved by the Institutional Animal Welfare Officer (Tierschutzbeauftragter) and the ethics committee of the TU Dresden. Necessary licenses 24-9168.24-9/2012-1, DD24.1-5131/451/8 and TVV 16/2018 (DD24-5131/354/19) were obtained from the regional Ethical Commission for Animal Experimentation of Dresden, Germany (Tierversuchskommission, Landesdirektion Sachsen)"

Reviewing Editor

  1. Jeremy Nathans, Johns Hopkins University School of Medicine, United States

Publication history

  1. Received: June 20, 2019
  2. Accepted: December 11, 2019
  3. Accepted Manuscript published: December 11, 2019 (version 1)
  4. Version of Record published: January 21, 2020 (version 2)

Copyright

© 2019, Subramanian 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. Kaushikaram Subramanian
  2. Martin Weigert
  3. Oliver Borsch
  4. Heike Petzold
  5. Alfonso Garcia-Ulloa
  6. Eugene W Myers
  7. Marius Ader
  8. Irina Solovei
  9. Moritz Kreysing
(2019)
Rod nuclear architecture determines contrast transmission of the retina and behavioral sensitivity in mice
eLife 8:e49542.
https://doi.org/10.7554/eLife.49542

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