Histochemically distinct compartments in the striatum of human, monkeys, and cat demonstrated by acetylthiocholinesterase staining.

Abstract

We here report observations on the distribution of acetylcholinesterase (acetylcholine hydrolase, EC 3.1.1.7) in the striatum of the adult human, the rhesus monkey, and the cat. By the histochemical staining methods of Geneser-Jensen and Blackstad and of Karnovsky and Roots, compartments of low cholinesterase activity were identified in parts of the striatum in all three species. In frontal sections, these enzyme-poor zones appeared as a variable number of weakly stained t0.5-mm-wide zones embedded in a darkly stained background. The zones varied in cross-sectional shape from round to elongated and were sometimes branched. They were most prominent in the head of the caudate nucleus. Three-dimensional reconstructions of serial sections through the caudate nucleus in the human and cat suggest that over distances of at least several millimeters, the zones of low enzyme activity form nearly continuous labyrinths.The mammalian striatum is characterized by one of the highest concentrations of acetylcholinesterase (acetylcholine hydrolase, EC 3.1.1.7) in the brain. The presence of this enzyme is not in itself sufficient to establish the existence of cholinergic transmission in the striatum, but the caudoputamen has also been shown to contain cholinergic receptors (1) and the synthetic enzyme of the cholinergic mechanism, choline acetyltransferase (2). The histochemical demonstration of acetylcholinesterase has therefore come to be regarded as a useful indirect indicator of cholinergic activity in the striatum and has further attracted interest because of the remarkable similarity in distribution of dopamine histofluorescence and acetylcholinesterase activity in the caudoputamen and nucleus accumbens. We report here observations on the distribution of striatal acetylcholinesterase in the human, together with parallel observations in cat and monkey. The main finding of this study is that the cholinesterase of the adult striatum in all three species is characterized by a complex intrinsic architecture that can be visualized by the histochemical methods of Karnovsky and Roots (3) and Geneser-Jensen and Blackstad (4). These findings strongly suggest that in the human, as in the cat and monkey, the contrast between an architecturally highly differentiated cerebral cortex on the one hand and a structurally homogeneous striatum on the other' has been overdrawn. When considered in the context of other recent experimental studies of the mature and developing striatum (5-13), the present findings support the concept of a fundamental subdivision of the striatum into a mosaic of at least partially segregated, histochemically distinct units. Figs. 1-4 illustrate this pattern of staining in frontal sections passing through the caudate nucleus of the cat (Fig. 1), monkey (Fig. 2), and human (Figs. 3 and 4). Typically, 6 to 12 distinct regions of low enzyme activity appeared in the caudate nucleus in single sections near the levels illustrated. The average transverse diameter of the zones was 0.3-0.5 mm in the cat and 5723 ...

Changes in Muscle Tone Are Regulated by D1 and D2 Dopamine Receptors in the Ventral Striatum and D1 Receptors in the Substantia Nigra

“…The sulpiride site is also close to the D2 site previously defined by us as mediating dopamine agonist-elicited stereotyped head-down sniffing (Cameron and Crocker 1989). Although it has been demonstrated extensively that the striatum is a heterogeneous structure in terms of its neurochemistry (Graybiel and Ragsdale 1978;Graybiel et al 1979;Herkenham and Pert 1981;Graybiel 1990), functional heterogeneity of this structure has only been documented relatively recently (Cameron and Crocker 1989;Koshikawa et al 1989;Ossowska et al 1990;Crocker and Cameron 1992;Wardas et al 1995). In fact, many clinical and experimental animal studies (including Farde et al 1992;Leysen et al 1993) consider the striatum as a homogeneous structure in terms of the actions of dopamine antagonists producing motor side effects.…”

Nur77 mRNA levels and L-Dopa-induced dyskinesias in MPTP monkeys treated with docosahexaenoic acid

“…In addition to the segregation into direct and indirect pathways, caudate-putamen projection neurons are segregated functionally and biochemically into two major compartments, termed striosome or patch and matrix (Gerfen, 1984;Graybiel and Ragsdale, 1978). Since we observed a strong co-localization between Nur77 and SP after L-Dopa and L-Dopa + DHA treatments and that immunochemistry of DYN and SP are highly prevalent in striosomes, it is not surprising that these treatments predominantly modulated Nur77 mRNA levels in striosomes.…”

Contributions of Dopamine D1, D2, and D3 Receptor Subtypes to the Disruptive Effects of Cocaine on Prepulse Inhibition in Mice

“…Additionally, amphetamine induces immediate early gene c-fos expression mainly in striosomes, whereas cocaine causes an immediate c-fos expression in both the striosome and matrix compartments of the dorsal striatum in the rat . The striosomes and matrix are the major neurotransmitter-specific compartments in the dorsal striatum (Graybiel and Ragsdale, 1978;Graybiel et al, 1990) and have different limbic and sensorimotor affiliations with cortex and subcortex (Donoghue and Herkenham, 1986;Ragsdale and Graybiel, 1990). Amphetamine and cocaine also lead to different c-fos expression patterns in the nucleus accumbens.…”