Early vascularization of the embryonic cerebral cortex: Golgi and electron microscopic studies

Two developmental aspects in the establishment of the vasculature of the embryonic cerebral cortex have been analyzed: the vascular perforation of the external basal lamina and marginal glia by leptomeningeal capillaries and their early intracortical angiogenesis. Electron microscopic and rapid Golgi preparations have been used in this study. Four phases have been identified in the vascular perforation of the cortex. First, the leptomeningeal capillary approaches and establishes direct contact with the external basal lamina and marginal glia of the cerebral cortex. Second, the leading endothelium of the glia-touching capillary undergoes considerable membrane activity forming many filopodia and pseudopodia. Some filopodia of this activated endothelium perforate the vascular and cortical basal laminae and penetrate into the neural tissue. This filopodial perforation is accompanied by swelling and disintegration of the subadjacent marginal glial endfeet. Third, the original perforation enlarges progressively and allows an entire endothelial cell (or cells) to penetrate into the neural tissue. Fourth, proliferation and progressive canalization of penetrated endothelial cells result in the formation of a new cortical capillary in situ. Its proximal wall becomes surrounded by perivascular glial processes which appear to replace the degenerated ones. Thus a vasculoglial barrier is formed around the growing capillary, isolating it from the neural tissue, while the filopodia at its leading edge are still growing among the neural elements without recognizable basal lamina. The formation of a shallow pial-funnel at the capillary entrance can also be recognized at this time. This funnel contains the fine processes of leptomeningeal cells, a few collagen fibers, and the basal laminae of the penetrating vessel and of the perivascular glia. It represents an early stage in the formation of the Virchow-Robin space. The intracortical embryonic vasculature is characterized by both capillary angiogenesis and regression and by the formation of anastomotic plexuses. While capillary angiogenesis and reabsorption are found everywhere and appear as random phenomena, the location of the anastomotic plexuses is specific and always associated with actively growing cortical regions.