Ontogeny of the primate fovea: a central issue in retinal development

The formation of the primate fovea has fascinated a substantial number of histologists, pathologists, ophthalmologists and physiologists for more than a century. In this article, using data from the literature as well as our own observations, we identify events which we believe are crucial in this process and present a developmental neurobiologist's view of the formation of the primate fovea. The fovea is a region of the retina specialized for diurnal, high acuity functions which require a high spatial density of cone photoreceptors as well as a large number of inner retinal cells in order to establish the distinct retinofugal pathways (ganglion cell axons) receiving from individual cones in the foveal cone mosaic. A unique feature of the fovea is the displacement of cells connected to the foveal cones onto the rim of the fovea. It is generally believed that this displacement counteracts the problems caused by the scattering of the incoming light by cells and blood vessels of the inner retina. We believe that one of the crucial events in the formation of the primate fovea is the early centripetal migration of photoreceptors towards the central area (centripetal displacement). This process, initiated early in development, continues throughout intrauterine life until some months or years postnatal. We propose that the displacement of cells from the inner layers is related to the earlier developmental accumulation of photoreceptors and inner retinal cells centrally. This, we propose, leads to metabolic "starvation" of the inner retina, resulting from the complete absence of retinal vessels from the vicinity of the incipient fovea. It is suggested that these factors in turn trigger centrifugal displacement of inner retinal cells towards the encroaching perifoveal capillary network and lead to the formation of the foveal depression.