Aggregations of granule cells in the basal forebrain (islands of Calleja): Golgi and cytoarchitectonic study in different mammals, including man

Abstract

The granule cell islands in the olfactory tubercle (islands of Calleja) and the insula magna of Calleja are present in all species examined in this study: cat, rat, mouse, rabbit, hedgehog, monkey, man, and dolphin, displaying the same basic morphology. They appear as rather undifferentiated neurons with a poorly developed dendritic tree and a short unramified axon that does not leave the island. The larger islands and the insula magna are associated with medium‐sized neurons often lying in cell‐sparse core regions; they probably represent the efferent component of the islands. The distribution of granule cell islands in the olfactory tubercle varies from species to species: in the cat, they are restricted to the superficial cap regions; in the hedgehog and rabbit, they lie in cap regions and in the deep polymorph layer. In the rat, they are confined mainly to the deep polymorph layer, whereas in the mouse they extend through the three layers. In most species, the lateral islands form part of the cap regions, and they may receive fibers from the lateral olfactory tract. However, the consistent relationship between dwarf cells in the cap regions and granule cells seems to be a merely topographical one. The variable location of granule cell islands indicates that they are not related to specific cell types or cell groups in the olfactory tubercle, except to the large neurons in the hilus zones, which send their dendrites into the islands. Another close and constant relationship exists between granule islands and fibers of the medial forebrain bundle. The medial islands and the insula magna are the largest and most constant aggregations of granule cells. They are present even in the dolphin, which lacks lateral islands. Medial islands and insula magna are continuous in the hedgehog and the newborn kitten and seem to belong to a medial system of granule cells that is independent from the olfactory tubercle and from olfactory fibers. Aggregations of granule cells occur also outside the olfactory tubercle and the insula magna: in the hedgehog and the rabbit, clusters lie scattered in the n. accumbens. Distribution of granule cells outside the olfactory tubercle is related to ontogenetic development: in newborn kittens, granule cells extend from the subependymal layer of the lateral ventricle, where they probably originate, to the medioventral border of the hemisphere, and also distribute throughout the n. accumbens and the ventral pallidum. Thus, the granule cell territory is initially wider, and the original distribution is maintained in some species. It is in man that the aggregations of granule cells reach their maximum extent. In addition to a large insula magna, clusters of granule cells lie in all centers of the substantia perforata anterior; they form extensive islands below the pial surface. The small clusters in the n. accumbens, ventral pallidum, and substantia innominata generally are not associated with medium‐sized neurons. A constant topographical relationship exists between granule cell clusters and the parvicellular sublenticular cell groups, which reach their maximum development in man, and between gran‐ ule cells and the rostra1 extension of the nucleus basalis of Meynert. Despite important individual variations, the most consistent concentration of granule cells in man coincides with the level of maximum entry of blood vessels into the substantia perforata anterior.