Although the newly formed intraneural capillaries grow freely at first among the nervous elements, they too eventually become surrounded by perivascular glial processes. Intraneural capillaries are surrounded by a single basal lamina (formed by the re-fused vascular and the CNS basal laminae) and by a ring of perivascular glia, separating them from other neural elements. The intraneural perivascular glia constitutes also a specific tissue compartment which is anatomically independent from that of the VRC. Therefore, the circulating blood through the intraneural capillaries remains separated from the neuronal elements by a vascularglial (blood-brain) barrier.
As the VRC gradually elongates vertically, its vessels continues to give-off new capillaries which penetrate the CNS substance at different levels (Fig 2.14). The number of penetrating capillaries arriving from the VRC increases in the course of cortical development. These penetrating capillaries establish short-link anastomotic plexuses between contiguous VRCs (Fig 2.14). These anastomotic plexuses also undergo continuous developmental remodelling by capillary angiogenesis and reabsorption. The penetrating capillaries and their anastomotic plexuses constitute the intraneural vascular territory of the CNS vasculature and the only elements to participate in the so-called blood-brain barrier.
Intraneural capillary angiogenesis can best be studied with the rapid Golgi method or with similar procedures (Klosovskii 1963, Chilingarian and Paravian 1971, Press 1977, Marin-Padilla 1985b). This classic method deposits fine silver chromate granules within the membranes of various neural elements, including capillaries, rendering them visible against a transparent background (Figs 2.11, 2.12). Intraneural capillary angiogenesis is extraordinary during the early stages of development of the CNS. Growing endothelial cells produce many long and fine filopodia which advance freely without basal lamina among the neural elements (Fig 2.11). These fine filopodia emanate radially from the original endothelial cell and grow for a considerable distance. Their length ranges between 20 to 40 μm and their diameter between 0.3 to 0.6 μm (Figs 2.11, 2.12). Their size, length, multidirectional growth, and structural variability can be clearly appreciated in Golgi stained preparations (Figs 2.11, 2.12). The fine filopodia of growing capillaries seem to search for developmental clues (angiogenetic factors) which will determine the directional growth of the parent vessel (Marin-Padilla 1985b). They are also capable of perforating through anatomical barriers (CNS surface), and of establishing contacts among them during the formation of anastomotic plexuses (Figs 2.11, 2.12, 2.14).
Intraneural capillaries form short-link anastomotic plexuses throughout the developing CNS (Fig 2.12). It should be emphasized, that although intraneural capillary angiogenesis seems to be a random phenomenon, the formation and location of their anastomotic plexuses is specific, and always associated with actively growing regions of the CNS (Streeter 1918, Bär and Wolff 1972, Marin-Padilla 1985b). In the cerebral cortex, the first recognizable anastomotic plexus is the one formed throughout the paraventricular matrix zone, the first region of the developing CNS to begin differentiation. Anastomotic plexuses are subsequently formed in Layers I and VII following the formation of the cortical plate (Marin-Padilla 1971, 1978). These early anastomotic plexuses undergo continuous modification and remodelling by both capillary angiogenesis and reabsorption. The progressive remodelling of the intraneural plexuses again represents an integrative vascular process continuously adapting to the growing structural and functional needs of each particular region of the developing CNS (Marin-Padilla 1985b). The intraneural anastomotic plexuses evolve by the addition of new links (capillary angiogenesis) throughout growing and differentiating zones and by the removal of other links (capillary reabsorption) throughout zones in which they are no longer needed.
Capillary reabsorption is observed throughout the developing CNS. In Golgi preparations, it is characterized by the progressive reduction in the size and caliber of the regressing capillary and the eventual disappearance of anastomotic links (Fig 2.12). The nature of embryonic capillary regression and reabsorption remains poorly understood and also needs further investigation.
Fig 2.11 Examples of intracortical capillary angiogenesis from rapid Golgi preparations of the cerebral cortex of 13 day hamster embryos. Each illustration represents the tip of a growing intracortical capillary. The leading endothelium of growing capillaries produces numerous radiating filopodia which advance freely, without a recognizable basal lamina, among the neural elements. Their number, size, length, structural variability and multidirectional growth can be readily appreciated in these illustrations. x800.
Fig 2.12A Illustrates the type of short-link anastomotic plexus formed by the growing capillaries of the cerebral cortex of 13 day hamster embryos; from rapid Golgi preparations. In this plexus, some capillaries are growing in some areas (short arrows) while possibly regressing in others (long arrow). These anastomotic plexuses are always formed within differentiating and maturing regions of the developing CNS. B Illustrates the extensive intracortical capillary plexus formed between arterioles (a) and venules (v) of contiguous Virchow-Robin compartments. The intracortical capillary plexus constitutes the intraneural vascular territory of the CNS vasculature. Figure B is reproduced from rapid Golgi preparations of the cerebral cortex of a 32 week gestation infant. Magnifications: upper x800; lower x75.
Fig 2.13 Schematic drawings demonstrating the mature lamellar composition and structural organization of the meningeal, the Virchow-Robin and the perivascular glial compartments of the cerebral cortex. Also illustrated are their corresponding vascular territories, namely: the perineural, the interneural, and the intraneural, respectively. The blood vessels of the perineural (meningeal) and interneural (Virchow-Robin) territories are enclosed within specific perivascular tissue compartments, while those of the intraneural vascular territory are enclosed by perivascular glia. The Virchow-Robin space closes off with the fusion of the vascular and the CNS basal laminae into a single lamina which accompanies the penetrating capillary into the neural tissue proper. The obliteration of the pial (P) space at the entrance of the Virchow-Robin compartment is also illustrated. D = dura mater, NT = neurothelium, EA = external arachnoid lamella, IA = inner arachnoid, lamella, EP = external pia lamella, IP = inner pia lamella, GL = marginal glia, P = pial space, ICR = intercellular compartments. The insert shows the vascular basal lamina and its relationship to the meningeal, Virchow-Robin and perivascular glial compartments, respectively, as well as the location of the various intercellular tissue compartments. (From Krisch, B., H. Leonhardt, A. Oksche: Cell. Tiss. Res. 238: 459, 1984.)
Fig 2.14 Composite figure illustrating the three territories of the vasculature of the human cerebral cortex during embryonic development. 1 External view of the cerebral cortex of a 20 week human fetus illustrating the vasculature of its perineural (meningeal) vascular territory. The numerous anastomoses formed by these vessels throughout the surface of the cerebral cortex are clearly illustrated as well as some of the cortical arteries (A) and veins (V). Between the larger vessels there are many smaller ones which are difficult to