Rod nuclear architecture determines contrast transmission of the retina and behavioral sensitivity in mice
- Max Planck Institute of Molecular Cell Biology and Genetics, Germany
- Technische Universität Dresden, Germany
- 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
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)"
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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Rod nuclear architecture determines contrast transmission of the retina and behavioral sensitivity in mice
eLife 8:e49542.
https://doi.org/10.7554/eLife.49542
