Distinct nigrostriatal projection systems innervate striosomes and matrix in the primate striatum

Abstract

Mesostriatal projections were labeled in 11 squirrel monkeys by injecting the anterograde tracer, [35S]methionine, into different parts of the dopamine-containing A8-A9-A10 cell complex of the midbrain. Two strikingly different compartmental patterns of mesostriatal projection were found. Fields of dense labeling in both the caudate nucleus and the putamen, interrupted by pockets of sparse labeling, were observed with deposits involving cell group A8, cell group A10 and/or the dorsally situated 'pars mixta' of the substantia nigra. Where striosomes could be identified as such in adjoining histochemically stained sections, the sparsely labeled zones were aligned with them. By contrast, a pattern of focally dense labeling in the caudate nucleus and putamen, with much weaker labeling surrounding the densely labeled zones, was found with injection sites centered in the horizontal band and associated ventrally extending fingers of the substantia nigra pars compacta. Many of the pockets of heightened labeling could be shown to correspond to histochemically defined striosomes. These compartmental patterns were identified both in the caudate nucleus and in the putamen. We conclude that the A8-A9-A10 cell complex of the primate contains spatially distinct subdivisions with preferential projections directed, respectively, toward the striosome and matrix compartments of the striatum.