The striatal mosaic in primates: patterns of neuropeptide immunoreactivity differentiate the ventral striatum from the dorsal striatum

Abstract

Patterns of immunoreactivity for calcium-binding protein, tyrosine hydroxylase and four neuropeptides in the ventral striatum (nucleus accumbens, olfactory tubercle and ventromedial parts of the caudate nucleus and putamen) were compared to patterns of these markers in the dorsal striatum (the majority of the neostriatum) in rhesus monkey. The striatal mosaic was delineated by calcium-binding protein and tyrosine hydroxylase immunoreactivities. Both markers were found preferentially in the matrix of the dorsal striatum. The mosaic configurations of tyrosine hydroxylase, but not calcium-binding protein immunoreactivity, were similar in dorsal and ventral striatal regions. Substance P and leucine-enkephalin were not distributed homogeneously; distinct types and the prevalence of patches of substance P and leucine-enkephalin immunoreactivity distinguish the dorsal striatum from the ventral striatum and distinguish the caudate nucleus from the putamen. In the dorsal striatum, substance P and leucine-enkephalin patches consist of dense islands of immunoreactive neurons and puncta or clusters of immunoreactive neurons marginated by a dense rim of terminal-like puncta; the matrix was also enriched in leucine-enkephalin-immunoreactive neurons but contained less substance P-immunoreactive neurons. Patches were more prominent in the caudate nucleus than in the putamen. In the caudate, compartments low in tyrosine hydroxylase and calcium-binding protein immunoreactivities corresponded to cytologically identified cell islands and to patches enriched in substance P and leucine-enkephalin. These patches had a discrete infrastructure based on the location of substance P and leucine-enkephalin-immunoreactive neurons and terminals. In the ventral striatum, patches that showed low levels of substance P and leucine-enkephalin immunoreactivities were embedded in a matrix rich in immunoreactive cell bodies, fibers and terminals. In the accumbens, regions showing little tyrosine hydroxylase were in spatial register with patches low in substance P and leucine-enkephalin. Neurotensin- and somatostatin-immunoreactive neurons or processes were also compartmentally organized, particularly in the ventral striatum. Neurotensin-immunoreactive neurons were present predominantly in the nucleus accumbens but not in the dorsal striatum. Some regions enriched in neurotensin immunoreactivity were spatially registered with zones low in tyrosine hydroxylase, substance P and zones enriched in leucine-enkephalin. Areas enriched in somatostatin-immunoreactive processes overlapped with both tyrosine hydroxylase-rich and -poor regions in the ventral striatum. Our results show that the chemoarchitectonic topography of the striatal mosaic is different in the dorsal and ventral striatum of rhesus monkey and that the compartmental organization of some neurotransmitters/neuropeptides in the ventral striatum is variable and not as easily divisible into conventional patch and matrix regions as in the dorsal striatum.(ABSTRACT TRUNCATED AT 400 WORDS)