Abstract
Rod and cone photoreceptors differ in their shape, photopigment expression, synaptic connection patterns, light sensitivity, and distribution across the retina. Although rods greatly outnumber cones, human vision is mostly dependent on cone photoreceptors since cones are essential for our sharp visual acuity and color discrimination. In humans and other primates, the fovea centralis (fovea), a specialized region of the central retina, contains the highest density of cones. Despite the vast importance of the fovea for human vision, the molecular mechanisms guiding the development of this region are largely unknown. MicroRNAs (miRNAs) are small post-transcriptional regulators known to orchestrate developmental transitions and cell fate specification in the retina. Here, we have characterized the transcriptional landscape of the developing rhesus monkey retina. Our data indicates that non-human primate fovea development is significantly accelerated compared to the equivalent retinal region at the other side of the optic nerve head, as described previously. Notably, we also identify several miRNAs differentially expressed in the presumptive fovea, including miR-15b-5p, miR-342-5p, miR-30b-5p, miR-103-3p, miR-93-5p as well as the miRNA cluster miR-183/-96/-182. Interestingly, miR-342-5p is enriched in the nasal primate retina and in the peripheral developing mouse retina, while miR-15b is enriched in the temporal primate retina and increases over time in the mouse retina in a central-to-periphery gradient. Together our data constitutes the first characterization of the developing rhesus monkey retinal miRNome and provides novel datasets to attain a more comprehensive understanding of foveal development.
Highlights
Sight is often considered our most fundamental sense to perceive and navigate the world and, as a result, vision loss has a devastating impact on everyday life
By E16.5, most of the retina expresses miR-15b, but we found lower levels of expression in the peripheral tips (Figure 4B, white arrows) and the whole retina expresses high levels of miR15b by postnatal day 3 (P3). miR-30b is expressed throughout the thickness of the retina at P3 but we observed a moderate enrichment in the ganglion cell layer (GCL) and the basal part of the inner nuclear layer, suggesting higher expression in amacrine cells and possibly Retinal ganglion cells (RGCs) (Figure 4F and Supplementary 3)
Since the mouse retina does not contain a fovea and the rod-to-cone ratio in rodents resembles the most eccentric regions of the human retina, the molecular events that lead to the formation of the macula and the cone-dominated fovea remain largely unknown
Summary
Sight is often considered our most fundamental sense to perceive and navigate the world and, as a result, vision loss has a devastating impact on everyday life. Visual perception begins when photons of light enter the eye and are absorbed by the photoreceptors, the light-sensitive cells of the retina. There are two classes of photoreceptors named rods and cones because of their distinctive morphologies. While both populations contribute to the information transmitted to the visual centers of the brain by the optic nerve, these two cell types serve different purposes: rods miRNome of the Developing Fovea are highly sensitive to light and provide relatively coarse, colorless images, while cones require considerably brighter light and are responsible for our sharp chromatic vision and spatial acuity (Arshavsky and Burns, 2012). Despite the overall predominance of rod photoreceptors, primates have evolved to primarily utilize cone pathways, and most of our useful photopic vision depends on the cones in the fovea such that a 2-millimeter lesion in this area will result in legal blindness
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