MULTIPLE STRIATAL REPRESENTATION IN PRIMATE SUBSTANTIA-NIGRA

The pattern of arborization of the striatonigral fibers in the squirre l monkey (Saimiri sciureus) was studied with Phaseolus vulgaris-leucoa gglutinin (PHA-L) and biocytin as anterograde tracers. Single, small i njections of PHA-L or biocytin in either the caudate nucleus or the pu tamen give rise to at least four distinct, nonoverlapping but intercon nected fiber plexuses that are distributed throughout the rostrocaudal extent of the substantia nigra pars reticulata (SNr) according to a s trikingly precise and constant sequence. These plexuses, which compris e numerous fibers that closely entwine unlabeled dendrites of SNr neur ons (woolly fibers), often lie at the base of dopaminergic cell column s of the substantia nigra pars compacta (SNc). Long and varicose fiber s emerge dorsally from SNr plexuses and climb along the ventrally orie nted dendrites of dopaminergic SNc neurons, as visualized with tyrosin e hydroxylase immunohistochemistry. These fibers appear to contact en passant both dendrites and cell bodies of dopaminergic neurons belongi ng to the ventral tier of SNc. Anterograde double-labeling experiments involving small deposits of PHA-L and biocytin in adjacent areas of t he caudate nucleus and the putamen reveal that neighboring striatonigr al cell populations form two distinct sets of terminal plexuses that r emain well segregated throughout SNr. Plexuses from the two sources in terdigitate in some parts of SNr, but never intermix. Furthermore, the woolly fibers in these plexuses are composed exclusively of either PH A-L- or biocytin-labeled elements; none of them display both types of labeling. These results reveal that the striatonigral projection in pr imates is highly divergent and that the striatum has multiple represen tations at nigral levels. They also indicate that striatal information is conveyed to the substantia nigra in a highly ordered fashion throu gh multiple segregated channels. (C) 1994 Wiley-Liss, Inc.