Patterns of muscarinic cholinergic binding in the striatum and their relation to dopamine islands and striosomes

Abstract

The distribution of muscarinic cholinergic binding sites in the striatum was studied in relation to the locations of other neurochemical markers in the developing rat, cat, ferret, and human. In addition, patterns of striatal muscarinic binding were studied in the adult cat. Receptor binding autoradiography was carried out with tritiated propylbenzilylcholine mustard [( 3H]-PrBCM), an irreversible muscarinic antagonist, and subsequent serial section analyses involved comparisons among patterns of muscarinic binding, catecholamine histofluorescence, acetylcholinesterase (AChE) staining, Nissl staining, and cell labeling with [3H]-thymidine. Muscarinic binding in the immature striatum was characterized by local patchiness as well as regional density gradients in all species, with the most complex patterns appearing in the human. Patches of dense muscarinic binding were shown to lie in register with fluorescent dopamine islands (rat, cat, ferret), with AChE-positive patches (all species), and with clusters of neurons pulse-labeled by exposure to [3H]-thymidine on embryonic day 27 (ferret). At the developmental stages examined, the [3H]-PrBCM-positive patches were roughly aligned with regions of weak Nissl staining (cat, human). Striatal [3H]-PrBCM binding in the adult cat was dense, and though it usually appeared nearly homogeneous, in some sections patches of elevated binding were present. These had as counterparts, in neighboring sections, AChE-poor striosomes. We conclude that during development muscarinic cholinergic function is compartmentalized in the striatum in association with dopamine-containing afferents, and that this compartmentalization may persist to some degree in the adult.

Muscarinic m1 and m2 receptor proteins in local circuit and projection neurons of the primate striatum: Anatomical evidence for cholinergic modulation of glutamatergic prefronto‐striatal pathways

“…The striosomal-matrix compartmentalization of m1 receptor expression delineated in this study is in accord with findings of muscarinic binding patterns in young rats, cats, and ferrets and in adult cats (Nastuk and Graybiel, 1985) and is also in register with m1 and m2 receptor binding in adult cats, monkeys, and humans (Nastuk and Graybiel, 1988) and in developing cats (Nastuk and Graybiel, 1989). In juvenile monkeys, m1 was more intense in matrix zones compared with striosomes.…”

“…Acetylcholinesterase (AChE) histochemistry was used (by using the modified Lewis method; Krnjevic and Silver, 1966), because it delineates striosomes as AChE-poor areas and matrix regions as AChE-rich areas (Nastuk and Graybiel, 1985). Adjacent sections stained with m1 and m2 receptor proteins were compared with AChE-stained tissue with the aid of camera lucida drawings.…”

Fine structural features of the acetylcholine innervation in the developing neostriatum of rat

“…A transient patchy distribution has been reported for other cholinergic markers in the developing neostriatum of several mammalian species, including rat (Graybiel, 1984;Nastuk and Graybiel, 1989). It could be related to other aspects of the cytoarchitectural compartmentation in immature neostriatum, and particularly to the early presence of dopamine and opiate receptor rich islands (Graybiel et al, 1981;Moon Edley and Herkenham, 1984;Nastuk and Graybiel, 1985). This might in turn account for some interactions between these systems, as suggested by the observation that ACh regulates DA release as early as P3 in rat brain slices (Nomura et al, 1981).…”

Temporal regulation of ephrin/Eph signalling is required for the spatial patterning of the mammalian striatum

“…The matrix and the striosomes can be distinguished on the basis of various neurochemical markers selectively enriched in one of the compartments, such as calbindin in the matrix and μ-opioid receptor in the striosomes (Gerfen et al, 1987;Herkenham and Pert, 1981;Liu and Graybiel, 1992;Nastuk and Graybiel, 1985). Importantly, the striatal compartmentalization is also related to the organization of cortical inputs to the striatum, with matrix and striosome neurons receiving preferential inputs from distinct cortical layers and areas (Gerfen, 1989;Gerfen, 1992;Kincaid and Wilson, 1996).…”