Destruction of meningeal cells over the medial cerebral hemisphere of newborn hamsters prevents the formation of the infrapyramidal blade of the dentate gyrus

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Abstract
Meningeal cells participate in the development of the cerebellum both by stabilizing the extracellular matrix of the pial surface and by organizing the radial glial scaffold and the lamination of the cerebellar cortex. In the present study we investigated possible influences of meningeal cells on the development of the dentate gyrus, whose ontogenesis has many similarities to that of the cerebellum. Meningeal cells were selectively destroyed by injecting newborn hamsters with 25 μg 6-hydroxydopamine (6-OHDA) into the interhemispheric fissure. Twenty-four hours postinjection (p.i.) the meningeal cells over the medial cerebral hemispheres were completely destroyed. Thirty days p.i. the infrapyramidal blade of the dentate gyrus was almost completely missing, while the suprapyramidal blade was hypertrophied, extending with its medial tip almost up to the medial surface of the cortex. In order to ascertain that this maldevelopment was caused by the destruction of meningeal cells, another group of hamsters was pretreated with normetanephrine (NMN) which inhibits the extraneuronal uptake of 6-OHDA into meningeal cells. In this group the meningeal cells were unaffected by the treatment, and the morphology of the dentate gyrus was normal 30 days p.i. of 6-OHDA plus NMN. When the meningeal cells were destroyed in later stages of development (postnatal days 1–5), alterations of the dentate gyrus could be induced only up to the fourth postnatal day; thereafter, 6-OHDA treatment left it unchanged. This indicates a critical period of meningeal cell influence that coincides with the period of existence of the subpial dentate matrix. Analysis of the time course of the defective development revealed that in the first 5 days p.i. (1) meningeal cells over the medial cerebral hemisphere were destroyed and removed, (2) the pial basement membrane over both the dentate anlage and the diencephalon thinned and ruptured, and the adjacent brain parts fused focally, (3) many cells of the subpial dentate matrix disappeared from their subsurface position, (4) the number of “immature” cells increased in the hilus and the subgranular zone of the suprapyramidal blade, (5) the suprapyramidal blade elongated and thickened considerably, while the infrapyramidal blade did not form. Beyond 5 days p.i. those parts of the pial surface of the dentate anlage that had not fused with the diencephalon were repopulated with meningeal cells. This reappearance of meningeal cells was accompanied by (1) the restitution of the normal morphology of the basement membrane, (2) the reappearance of neuronal and glial cells below the pial surface, and (3) the formation of fragments of the infrapyramidal blade which later developed a normal appearing lamination. These findings show that meningeal cells are involved in the development of at least the infrapyramidal blade of the dentate gyrus. The mechanisms of this influence remain speculative at present, but probably include (1) participation of the meningeal cells in the remodelling of the extracellular matrix of the pial surface, and (2) the regulation of the spatial distribution and organization of the neuronal and glial cells in the subpial dentate matrix and the infrapyramidal blade of the dentate gyrus.

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