Mechanics of Optic Vesicle Morphogenesis in the Chick Embryo

Abstract

In the vertebrate embryo, the eyes are initially bulges that grow outward from the sides of the primitive forebrain. As these optic vesicles (OVs) elongate, they come into contact with the surrounding surface ectoderm (SE), and both layers then invaginate to create the optic cup (prospective retina) and lens vesicle. The initial shaping of the OVs sets the stage for these later events. To explore the mechanical factors involved in shaping the OVs, we used experiments on chick embryos along with computational models. First, mechanical dissections were used to remove the SE. Our analysis of OV shapes suggests that the SE exerts asymmetric loads that cause the OVs to flatten and shear caudally during the earliest stages of eye development and later to bend in the caudal and dorsal directions. These deformations cause the initially spherical OVs to become pear-shaped. Exposure to the myosin II inhibitor blebbistatin reduced these effects, suggesting that cytoskeletal contraction controls OV shape by regulating tension in the SE. To test the physical plausibility of these interpretations, we developed finite-element models of the forebrain, including frictionless contact between the SE and OVs. With differential growth included in the OVs, these models were used to simulate each experiment (control, SE removed, no contraction). For each case, the predicted shape of the OV agrees reasonably well with experiments. Our results support this idea that a combination of differential growth in the OV and external pressure exerted by the SE are sufficient to cause the global changes in OV shape observed during the earliest stages of eye development.