Radial organization of the hippocampal dentate gyrus: a Golgi, ultrastructural, and immunocytochemical analysis in the developing rhesus monkey

Abstract

The cytoarchitectonic organization of the dentate gyrus was analyzed in the rhesus monkey at various embryonic (E) and postnatal (P) ages with the rapid Golgi method, transmission electron microscopy (EM), and immunocytochemical localization of glial fibrillary acidic protein (GFAP). From the earliest ages (stage I, E38-E83), immature granule cells were arranged radially along elongated fibers that extend from the ventricular zone to the pial surface. The glial nature of these radial fibers was confirmed by the presence of GFAP antigen in their cytoplasm detected clearly by E70. EM analysis at this age showed that granule cells situated within the dentate plate, as well as many neurons still migrating from the ventricular zone, were closely apposed to fascicles of radial glial fibers. The radial organization of the dentate plate was even more evident during stage II (E83-E165). Thus, in E97 and E125 specimens, radially oriented immunoreactive glial processes emerged from somas situated either in the ventricular or subgranular zones, penetrated between columns of neurons in the granular layer, branched upon entering the molecular layer, and finally terminated at the pial surface. Palisades of glial processes delineated ontogenetic radial units which consisted of stacks of granule cell bodies in different stages of maturation. In a given radial unit, more mature cells were located superficially (closer to the pial surface) and less mature cells were located at progressively deeper levels. This radial organization of the dentate gyrus was maintained during stage III (P0-P60) and stage IV (2 months-adult). Furthermore, the number of GFAP-positive proliferating cells in the subgranular zone increased from 1 to 5 months. In the mature brain, the radial organization of the dentate gyrus was less apparent although many glial fibers still penetrated the granule cell layer. The present results indicate that the developing dentate gyrus in primates consists of a series of ontogenetic radial units that resemble those described in the fetal neocortex (Rakic, '72). They further suggest that the development and maintenance of this radial columnar organization may be imposed by the orientation of glial scaffolding during development.