Anatomy of the isolated area dentata grown in the rat anterior eye chamber.

Abstract

AbstractWe used the intraocular transplantation technique to test the developmental potential of isolated, fetal area dentata, and to help define the determinants of such critical aspects of brain development as cell arrangements, dendritic arborization, axon growth, synaptogenesis, and connectional specificity. Fetal hippocampal formations were removed from embryos of 19 to 20 days of embryonic age. A region, termed area dentata, was dissected from the hippocampal formation. This region included the anlage of the dentate gyrus, the hilus, and the medial regio inferior. Areae dentatae were transplanted into the anterior eye chamber of isogenic, adult rats. The growth and vascularization of area dentata transplants were monitored over the first 2 months in oculo. From 2 to 7 months after transplantation host animals were killed and the area dentata transplants were examined with a variety of histological techniques. The cytoarchitectonics of a great majority of the transplants were highly reminiscent of area dentata in situ. A typical morphogenetic outcome included tightly packed, continuous, C‐shaped sheets of granule cells with mossy fibers which made contact with the proximal dendrites of a segregated group of dispersed hilar cells and a loosely packed layer of pyramidal cells. The axons of pyramidal and hilar cells, in turn, provided the major innervation of the granule cell dendrites. The granule cell dendritic spine density was nearly normal, and synapses were common in the granule cell neuropil. Very little innervation of the transplant was found to originate from the axons of the ciliary or trigeminal ganglia which innervate the host iris and enter the transplant. Sympathetic fibers from the host iris innervate the transplant in a reproducible and organotypic fashion although the degree of innervation is less than the in situ noradrenergic innervation of area dentata. Few Timm‐positive fibers of the transplant were found to leave the transplant and enter the host iris. Area dentata transplants had several features which were different from their in situ counterparts. These differences included less expansive granule cell dendrites, extensive presence of fibrous astrocytes, pyramidal cells with reduced kainic acid sensitivity, hypervascularized neuropil, and transformation of peripheral adrenergic fiber morphology to one of central characteristics.Thus, pieces of isolated area dentata display a great self‐developing capacity, in terms of cellular and afferent organization, both of which follow “rules” present in situ. A powerful capacity for intrinsic and appropriate innervation of area dentata is apparent in the face of a total lack of normal extrinsic afferents and an availability of extrinsic but inappropriate sources of innervation. This initial description of isolated area dentata organization in oculo is meant to lay the groundwork for experimental investigations into the regulatory mechanisms governing morphogenesis and afferent organization.