Changing Patterns of Vasculature in the Developing Amphibian Retina

Abstract

Patterns of vascularisation were examined in whole-mounted retinae from tadpole stages to adulthood in the tree frog Litoria moorei using perfusion with Indian ink. Changing cell densities in the underlying ganglion cell layer were studied in a parallel Cresyl-stained series. Throughout development, the vasculature was pan-retinal and the hyaloid vessel was prominent. In early tadpole stages, capillaries were arranged as a honeycomb, and their number increased at a rate sufficient to maintain high densities in the face of increasing retinal area; major arteries and veins condensed within the capillary network. By early post-metamorphic life, the retinal vasculature was remodelled by the loss of four-fifths of the capillaries; the reduction in their density was far greater than could be accounted for by continuing retinal growth. This loss resulted in a change from the honeycomb appearance to one with largely parallel vessels linked by fewer connecting ones, an arrangement that became increasingly pronounced. In post-metamorphic life, the number of branch points increased such that their density decreased only slightly in the face of considerable increases in retinal area. The density of branch points varied across the retina and changed with age. Initially, the vasculature was most dense centrally, but by mid-larval life densities were highest in two patches located in the mid-temporal and mid-nasal retina. Thereafter, the vasculature increasingly assumed gradients resembling an area centralis and visual streak, a profile that survived the vascular remodelling. The development of density gradients in the vasculature preceded that of cells in the ganglion cell layer, the latter appearing only following metamorphosis. However, in post-metamorphic life, the topographies of the retinal vasculature and cells in the ganglion cell layer were closely related.