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

Kaushikaram Subramanian,Moritz Kreysing,Eugene W Myers,Irina Solovei,Marius Ader,Alfonso Garcia-Ulloa,Heike Petzold,Oliver Borsch,Martin Weigert

doi:10.7554/elife.49542

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.

Highlights

The structure of the vertebrate retina requires light to pass through multiple cell layers prior to 40 reaching the light-sensitive outer segments of the photoreceptors (Dowling, 1987)
To test how the presence of densely packed rod nuclei in the light path affects the propagation of light through the retina, we compared transmission of micro-projected stripe images through freshly excised retinae of wild type (WT) (Fig. 1A) and Rd1/Cpfl1 KO mice(Chang et al, 2002), which lack all photoreceptors including the outer nuclear layer (ONL) (Fig. 1B2)
We established nuclear inversion as a complementary strategy to maximize sensitivity under low light conditions. We show that it is the direction into which light is scattered inside retinal tissue that translates into differential contrast sensitivity

Summary

Introduction

The structure of the vertebrate retina requires light to pass through multiple cell layers prior to 40 reaching the light-sensitive outer segments of the photoreceptors (Dowling, 1987). Rod nuclei are inverted in nocturnal mammals (Błaszczak, Kreysing, & Guck, 2014; Kreysing, Boyde, Guck, & Chalut, 2010; Solovei et al, 2009; 2013), such that heterochromatin is detached from the nuclear envelope and found in the nuclear center, whereas the less-dense euchromatin is re-located to the nuclear periphery. Given that 50 this nuclear inversion is exclusive to nocturnal mammals and correlates with the light-focusing capabilities of isolated nuclei, it was proposed as an evolutionary adaptation to life under lowlight conditions (Błaszczak et al, 2014; Kreysing et al, 2010; Solovei et al, 2009). The nature of any visual improvements that could arise from nuclear inversion remains unclear

Methods

Results

Conclusion