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

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 no...

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Autores principales: Subramanian, Kaushikaram, Weigert, Martin, Borsch, Oliver, Petzold, Heike, Garcia-Ulloa, Alfonso, Myers, Eugene W, Ader, Marius, Solovei, Irina, Kreysing, Moritz
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6974353/
https://www.ncbi.nlm.nih.gov/pubmed/31825309
http://dx.doi.org/10.7554/eLife.49542
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author Subramanian, Kaushikaram
Weigert, Martin
Borsch, Oliver
Petzold, Heike
Garcia-Ulloa, Alfonso
Myers, Eugene W
Ader, Marius
Solovei, Irina
Kreysing, Moritz
author_facet Subramanian, Kaushikaram
Weigert, Martin
Borsch, Oliver
Petzold, Heike
Garcia-Ulloa, Alfonso
Myers, Eugene W
Ader, Marius
Solovei, Irina
Kreysing, Moritz
author_sort Subramanian, Kaushikaram
collection PubMed
description 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.
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spelling pubmed-69743532020-01-22 Rod nuclear architecture determines contrast transmission of the retina and behavioral sensitivity in mice Subramanian, Kaushikaram Weigert, Martin Borsch, Oliver Petzold, Heike Garcia-Ulloa, Alfonso Myers, Eugene W Ader, Marius Solovei, Irina Kreysing, Moritz eLife Cell Biology 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. eLife Sciences Publications, Ltd 2019-12-11 /pmc/articles/PMC6974353/ /pubmed/31825309 http://dx.doi.org/10.7554/eLife.49542 Text en © 2019, Subramanian et al http://creativecommons.org/licenses/by/4.0/ http://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Cell Biology
Subramanian, Kaushikaram
Weigert, Martin
Borsch, Oliver
Petzold, Heike
Garcia-Ulloa, Alfonso
Myers, Eugene W
Ader, Marius
Solovei, Irina
Kreysing, Moritz
Rod nuclear architecture determines contrast transmission of the retina and behavioral sensitivity in mice
title Rod nuclear architecture determines contrast transmission of the retina and behavioral sensitivity in mice
title_full Rod nuclear architecture determines contrast transmission of the retina and behavioral sensitivity in mice
title_fullStr Rod nuclear architecture determines contrast transmission of the retina and behavioral sensitivity in mice
title_full_unstemmed Rod nuclear architecture determines contrast transmission of the retina and behavioral sensitivity in mice
title_short Rod nuclear architecture determines contrast transmission of the retina and behavioral sensitivity in mice
title_sort rod nuclear architecture determines contrast transmission of the retina and behavioral sensitivity in mice
topic Cell Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6974353/
https://www.ncbi.nlm.nih.gov/pubmed/31825309
http://dx.doi.org/10.7554/eLife.49542
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