Subdivisions of the dopamine-containing A8-A9-A10 complex identified by their differential mesostriatal innervation of striosomes and extrastriosomal matrix

Abstract

The mesostriatal projections from the dopamine-containing cells groups A8, A9 and A10 have been studied in the cat in relation to the histochemical compartments known to exist in the striatum. In order to do this, we made stereotaxic injections in the substantia nigra of either [3H]proline-[3H]leucine, [35S]methionine, wheat germ agglutinin-horseradish peroxidase, or the two last tracers combined, and compared the location of anterograde labeling in the striatum to the locations of striosomes and extrastriosomal matrix identified by their low or high content, respectively, of the enzyme acetylcholinesterase. A discrete innervation of dorsolateral striosomes by a caudal densocellular subdivision of the substantia nigra pars compacta was found. This densocellular zone of the pars compacta was readily identifiable in sections stained for tyrosine hydroxylase-like immunoreactivity and corresponded to the uniquely acetylcholinesterase-poor zone detected in the substantia nigra pars compacta in serially adjacent sections stained for this enzyme. Selective anterograde labeling of the extrastriosomal matrix occurred in cases with injection sites centered in cell group A8. Tracer deposits in cell group A10 also elicited a preferential labeling of the extrastriosomal matrix, but this innervation was sparse compared to the prominent labeling of fibers in the ventral striatum. An almost exclusive innervation of caudal and ventral striosomes of the head of the caudate nucleus occurred after a deposit of tracer in the pars lateralis of the substantia nigra. Mixed labeling of striosomes and matrix occurred with injection sites centered in the rostral, cell-sparse part of the pars compacta of the substantia nigra. Clusters of tyrosine hydroxylase-immunoreactive neurons within this zone, most likely representing finger-like extensions of the caudal densocellular zone of the pars compacta, might have accounted for part of the striosomal labeling in these cases. We conclude that different subdivisions of the A8-A9-A10 dopamine-containing cell complex of the cat's mesencephalon project preferentially to striosomes or to extrastriosomal matrix. On this basis we suggest that there may be different functional channels in the mesostriatal projection, including, from cell group A8, a channel providing dopaminergic modulation of sensorimotor processing in the striatal matrix, and, from the densocellular zone of the substantia nigra pars compacta, a channel leading to limbic-related mechanisms represented in the striosomal system.