New role for the primate fovea: a retinal excavation determines photoreceptor deployment and shape

In humans, an increasing density of foveal cone photoreceptors occurs slowly over several years after birth, and accounts for a region that subserves high visual acuity. Concurrently, inner retinal cells move centrifugally away from the foveal center. Such developmental rearrangements reflect complex cellular remodeling after the retinal neuronal cells have differentiated and have formed synapses. Explaining foveal morphogenesis is difficult, because differentiated neuronal cells seem incapable of moving actively. Presented here is a biomechanical explanation of how the above events occur. This hypothesis assumes that the cellular movements throughout the retinal layers occur passively as the eye grows and the retina is stretched. Retinal stretch was simulated using virtual engineering models that were analyzed with finite element analysis. A pit combined with retinal stretch causes the retinal layers to deform in a way that accounts for both the centrifugal and centripetal movement of various retinal cell types. Axially directed, tensile forces associated with stretching the retinal tissue surrounding the pit also accounts for the elongated morphology of foveal cone photoreceptors. These simulations suggest that a pit is required for both the centripetal displacement of cone cells toward the center of the fovea, and for the elongated foveal cone morphology. Since the primate fovea may have minimal impact on acuity, its primary role may be to initiate foveal morphogenesis in slowly developing eyes.