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.(ABSTRACT TRUNCATED AT 400 WORDS)

Evidence for enhancement of gap junctional coupling between rat island of Calleja granule cells in vitro by the activation of dopamine D3 receptors

“…A D1-like receptor is also implicated in reducing transfer of Lucifer Yellow between neurones of the core region of the nucleus accumbens and also in the surrounding shell of that structure (O'Donnell & Grace, 1993). Interestingly O'Donnell & Grace (1993) found that Dµ-like agonists potentiated dye coupling in the shell region, which contains a single large Calleja island (Meyer, Gonzalez-Hernandez, Carrillo-Padilla & Ferres-Torres, 1989) and shares many other similarities (Alheid & Heimer, 1988) with the olfactory tubercle, including a marked presence of D× receptors (Landwehrmeyer et al 1993a;Diaz et al 1995). The contribution of the particular subclass of Dµ-like receptor responsible for potentiated dye coupling could not have been distinguished pharmacologically by the compounds that O'Donnell & Grace (1993) had available and it is possible that these effects were due to activation of D× receptors in the accumbens.…”

“…In spite of this, descriptions of the anatomy of the IC and their counterparts in vertebrate species are detailed (see Meyer et al 1989 for references); granule cell clusters with IC-like morphology are seen in the brain of man (in the anterior perforated substance, the human vestige of the olfactory tubercleventral striatum) where they, too, contain D× receptors (Landwehrmeyer, Mengod & Palacios 1993b;Murray, Ryoo, Gurevich & Joyce, 1994). In all species, the granule cells are associated with large (> 20 ìm diameter) neurones residing in a cell-sparse (hilar) region that forms a dorsal concavity in the overall shape of islands; the large cells possess dendrites which extend only as far as the outer edges of the granule cell clusters and intimate contacts have been described between IC granules and these dendrites at the light microscope level (Fallon, Riley, Sipe & Moore, 1978;Millhouse & Heimer, 1984;Meyer & Wahle, 1986;Millhouse, 1987;Meyer et al 1989). As well as gap junctions, conventional chemical synapses are apparent within the IC complexes (Ribak & Fallon, 1982).…”

The Reward Circuit: Linking Primate Anatomy and Human Imaging

“…The VS has numerous smaller and more densely packed neurons; the dorsal striatum is more homogenous. The VS contains cell islands, including the islands of Calleja, which are thought to contain quiescent immature cells that remain in the adult brain (Bayer, 1985;Chronister et al, 1981;Meyer et al, 1989). The VS also contains many pallidal cells and their dendritic arbors that invade this ventral forebrain territory (see section Ventral pallidum).…”

Basal telencephalic regions connected with the olfactory bulb in a Madagascan hedgehog tenrec

“…As in other species, it is considered a striopallidal structure (Heimer et al, 1995), but there are still uncertainties regarding the particular nature (striatal, pallidal, nonstriopallidal) of certain elements (Millhouse, 1987;Talbot et al, 1988b;Meyer et al, 1989). The possibility of being a nonstriopallidal structure particularly applies to the Callejal islands, the cells around the tubercular islands (TuE), and the rostrolateral tubercular seam region (TuS), which are difficult to understand because of the considerable variability in their location and intrinsic organization.…”

“…It includes 1) the tuberculum olfactorium and the proper ventral pallidum (subcommissural portion of the substantia innominata), 2) the islands of Calleja, 3) the nuclear complex of the diagonal band (cells in and around the globus pallidus, the nuclei of the diagonal band and the medial septum), and 4) the classic and the extended amygdala. The actual subdivision of these cells groups has been obtained predominantly on the basis of histochemical criteria and connectivity (Meyer et al, 1989;Gaykema et al, 1990;Martin et al, 1991;Amaral et al, 1992;McDonald, 1992;Alheid et al, 1995;Heimer et al, 1997;Zaborszky et al, 1997), and may still be subjected to change (see e.g., Swanson and Petrovich, 1998). An obvious handicap to understand the organisation and evolution of the mammalian basal telencephalon is that previous studies have been carried out mainly in rodents and primates but not in lower mammals.…”