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

Abstract

20Rod 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 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 25 terminal development, which, confirmed by a mouse model, happens due to nuclear inversion.We further reveal that improved retinal contrast-transmission, rather than photon-budget or resolution, leads to enhanced contrast sensitivity under low light condition. 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 30 perception.

Viewing Nuclear Architecture through the Eyes of Nocturnal Mammals

“…This suggests about 1.8-fold higher volume density in the chromocenter than in the rest of the chromatin, and is consistent with an approximately 2-fold higher density in the densest region in the conventional interphase nucleus and mitotic chromosomes measured by ChromEMT [29]. Nonetheless, the physical properties of the densely packed heterochromatic core, formed by cHC and HC, are pretty unusual for instance, it is not penetrable to free GFP molecules in rods, whereas in conventional nuclei GFP molecules freely go through heterochromatin of both types [14]. Moreover, the core is highly refractive and shows physical properties of a lens focusing light [3,30].…”

“…Since rod perikarya are almost entirely occupied by nuclei, regular columns of rod perikarya in nocturnal retinas (up to 10-12 perikarya in a column) are practically composed of lenses stacked upon each other (Figure 2A,B). Due to this arrangement, light travelling through the columns of lenses is significantly less scattered, facilitating light sensitivity in low-light (scotopic) conditions [3,14,30]. In agreement with this, the inverted nuclear arrangement is found only in nocturnal mammals, whereas rod nuclei of diurnal mammals (living in photopic conditions) have conventional architecture [3,31,32] (Figure 2B,C).…”

“…In rod nuclei, the positions of EC and HC are inverted: heterochromatin, including both cHC and HC, occupies the nuclear center, while euchromatin is displaced to the periphery [3] (Figure 1B). Remarkably, nuclear inversion, albeit not currently known to hinder any nuclear processes, is likely to be strongly disadvantageous for nuclear function (see the next chapter) but, as it turned out, confers improved vision under low-light conditions [3,14].…”