Relation of an array of early-differentiating cones to the photoreceptor mosaic in the primate retina

Abstract

THE retina of diurnal primates, including humans, contains a reiterative mosaic of red-, green- and blue-sensitive cones whose visual pigments are maximally sensitive to long, middle or short wavelengths, respectively1. Although the distribution of the cone subtypes in the adult rhesus monkey has been quantified using opsin-specific antisera2, the mechanism for the phenotypic specification of the cone subtypes and the establishment of their ratios in the retinal mosaic remain unknown. Here we present immunocytochemical evidence that a subset of cones (about 10%) express their cell-specific opsin two to three weeks before the surrounding cones. Remarkably, these precocious cones are evenly stationed throughout undifferentiated regions of the retinal surface from several weeks after their last mitotic division3, and at least one month before the formation of their synapses with bipolar and horizontal cells4. Use of confocal laser microscopy reveals that the inner segments of immunolabelled and surrounding unlabelled cones are transiently in apposition with one another, enabling surface mediated interactions to occur during this period. We suggest that the early maturing cones induce neighbouring undifferentiated cones to express an appropriate opsin phenotype, and therefore constitute a 'protomap' for the emergence of the species-specific retinal mosaic.