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A. Anishchenko, J. Elstrott, M. Greschner, A. Sher, A. Litke, M. B. Feller, E. J. Chichilnisky; Functional Mosaics of Retinal Ganglion Cells Are Established Independent of Visual Experience. Invest. Ophthalmol. Vis. Sci. 2009;50(13):1426.
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© ARVO (1962-2015); The Authors (2016-present)
A characteristic feature of the adult retina is mosaic organization: a spatial arrangement of cells of each morphological and functional type that ensures uniform sampling over visual space. The primary mechanism implicated in the formation of mosaics relies on homotypic repulsive interactions to prevent cells of the same type from overlapping. However, visual experience can significantly influence the development of retinal circuits, as has been demonstrated by the impact of dark rearing on the dendritic morphology and stratification of retinal ganglion cells (RGCs). Here, we test the hypothesis that early visual experience is required for the development of visual space coverage by the receptive field mosaics of RGCs.
We use a large-scale multielectrode array to record from isolated retinas of mice right after eye opening (postnatal day 14; P14). To exclude the influence of the limited vision that occurs through closed eyelids, we dark reared the mice starting at P7. Spatiotemporal receptive fields (RFs) were estimated based on RGC responses to white-noise checkerboard stimulation.
We identified and characterized two distinct functional types of Off RGCs in P14 dark-reared mice. One type was comprised of cells with the largest RFs, the shortest light response latency, and the highest degree of response transience compared to all other Off cells observed at the same eccentricity. For both of the identified types, their RFs formed a spatial mosaic. To compare these early mosaics with the functional organization of mature retina, we repeated the experiments using adult mice. The RGC type that was most reliably identified across adult preparations consisted of the largest, fastest, and most transient Off RGCs. We speculate that this is the same large transient Off cell type that we observe in P14 retina. On P14 this type had slower and significantly less transient responses to light stimulation, consistent with immature functionality. Comparison of the mosaic properties revealed small differences between adult and P14 in the exclusion radius, nearest neighbor distance, and the degree of RF overlap. Despite these differences, the characteristic mosaic pattern of spatial RFs was already well established in the retina of P14 dark-reared mice.
These findings suggest that although the light-response properties of RGCs might require vision to reach full maturity, the coverage of visual space by the individual RGC types is established without visual experience.
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