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

Subramanian K, Weigert M, Borsch O, Petzold H, Garcia-Ulloa A, Myers EW, Ader M, Solovei I, Kreysing M

eLife · 11 Dec 2019 · doi: 10.7554/eLife.49542

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The chromatin in the nucleus of rod photoreceptors has an inverted structure in nocturnal animals. Metabolically, this is expensive to maintain, so it has been proposed that the inverted architecture provides an advantage during night vision. Subramanian et al could show with our OptoDrum that the inverted nuclear architecture provides improved contrast sensitivity in dark environments.

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.