Plasticity in the development of topographic order in the mammalian retinocollicular projection

The topographically ordered retinocollicular projection in rats emerges from an initially diffuse projection present in neonates through the elimination of aberrantly positioned axons and arbors. We explore developmental plasticity in this process by making partial retinal lesions at birth and determining the topographic mapping of the remaining retina at later ages when the map normally has a mature, retinotopic order. In normal mature rats, DiI focally injected into the retina labels axons that form a dense focus of overlapping arbors at the topographically correct location in the superior colliculus (SC). Similar injections in rats with partial retinal lesions label axons that form two discrete foci of arborizations; one at the topographically appropriate region of the SC and another in the region of the SC deprived of its normal retinal input by the retinal lesion. A focal injection of DiI into the "deprived" SC region retrogradely labels ganglion cells widely scattered in the retina. Therefore, a partial retinal lesion in developing rats does not lead to an orderly expansion of the remaining retinal projection to cover the entire SC, as it does in amphibians and fish following optic nerve regeneration. Rather, in rats, the remaining partial retina forms two distinct, contiguous projections to the SC: a retinotopically ordered one that retains normal topographic relationships and an aberrant, diffusely ordered one to the SC region topographically matched with the lesioned part of the retina. This abnormal persistence of topographically aberrant axons and arbors indicates that competitive interactions between retinal axons drive the remodeling of the initially diffuse retino-collicular projection into a topographically ordered one.