Abstract
SummaryIn development, almost all stratified neurons must migrate from their birthplace to the appropriate neural layer. Photoreceptors reside in the most apical layer of the retina, near their place of birth. Whether photoreceptors require migratory events for fine-positioning and/or retention within this layer is not well understood. Here, we show that photoreceptor nuclei of the developing mouse retina cyclically exhibit rapid, dynein-1-dependent translocation toward the apical surface, before moving more slowly in the basal direction, likely due to passive displacement by neighboring retinal nuclei. Attenuating dynein 1 function in rod photoreceptors results in their ectopic basal displacement into the outer plexiform layer and inner nuclear layer. Synapse formation is also compromised in these displaced cells. We propose that repeated, apically directed nuclear translocation events are necessary to ensure retention of post-mitotic photoreceptors within the emerging outer nuclear layer during retinogenesis, which is critical for correct neuronal lamination.
Highlights
The central nervous system is characterized by its stratified organization, and the arrangement of newly born neurons into distinct layers is critical for synaptic connectivity and function
Basal to the outer nuclear layer (ONL) lies the interneurons of the inner nuclear layer (INL), which form synaptic connections to PRs within the outer plexiform layer (OPL)
The accurate positioning of PRs between the retinal pigment epithelium (RPE) and INL facilitates the establishment of correctly located PR synapses, which is essential for vision (Dick et al, 2003; Maddox et al, 2015; Sarin et al, 2018)
Summary
The central nervous system is characterized by its stratified organization, and the arrangement of newly born neurons into distinct layers is critical for synaptic connectivity and function. Photoreceptors (PRs) reside exclusively in the outer nuclear layer (ONL) (Figure 1A). They are bordered apically by the retinal pigment epithelium (RPE), which supports PR function and survival. Basal to the ONL lies the interneurons of the inner nuclear layer (INL), which form synaptic connections to PRs within the outer plexiform layer (OPL). The nascent ONL overlaps with the neuroblastic layer (NBL) that exists before the ONL and INL separate with the forming OPL (Sarin et al, 2018). Cone PRs are born early in development and are initially displaced throughout the NBL (Suzuki et al, 2013), before becoming restricted to their adult location at the apical margin of the ONL (Rich, et al, 1997)
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