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

• Published in: eLife Vol. 8
• Main Authors: Subramanian, Kaushikaram, Weigert, Martin, Borsch, Oliver, Petzold, Heike, Garcia-Ulloa, Alfonso, Myers, Eugene W, Ader, Marius, Solovei, Irina, Kreysing, Moritz
• Format: Journal Article
• Language: English
• Published: England eLife Science Publications, Ltd 11.12.2019; eLife Sciences Publications Ltd; eLife Sciences Publications, Ltd
• Subjects: Animals; biophysics; Budgets; Cell Biology; Cell Nucleus - ultrastructure; Chromatin organisation; Computer Simulation; Contrast Sensitivity - physiology; Displays (Marketing); Female; Genes, Reporter; Light; Male; Mammals; Mice; Mice, Inbred C57BL; Mice, Transgenic; Motion detection; Motion Perception - physiology; Neuroblastoma; Nocturnal; optics; Photoreceptors; Physics of Living Systems; Retina; Retinal Bipolar Cells - physiology; Retinal Bipolar Cells - ultrastructure; Retinal Ganglion Cells - physiology; Retinal Ganglion Cells - ultrastructure; Retinal Rod Photoreceptor Cells - ultrastructure; Retirement benefits; Rhodopsin - deficiency; Rhodopsin - physiology; Scattering, Radiation; vision; visual ecology; Visual perception; United States; Germany; Chromatin organisation; mouse; vision; visual ecology; cell biology; retina; optics; biophysics; physics of living systems
• ISSN: 2050-084X; 2050-084X
• DOI: 10.7554/eLife.49542

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.