The developing neostriatum of the rabbit: Correlation of fluorescence histochemistry, electron microscopy, endogenous dopamine levels, and [3H]dopamine uptake

Tennyson, Virginia M.; Barrett, Robert E.; Cohen, Gerald; Côté, Lucien J.; Heikkila, Richard E.; Mytilineou, Catherine

doi:10.1016/0006-8993(72)90019-4

Cited by 227 publications

(61 citation statements)

References 35 publications

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“…As shown in Figure lC, patches of intense TH-like immunoreactivity were distributed through the cultured neonatal striatum in a pattern similar to that of the so-called dopamine islands, which are known to correspond to developing striosomes (Olson et al, 1972;Tennyson et al, 1972;Graybiel, 1984;Moon Edley and Herkenham, 1984;Murrin and Ferrer, 1984;van der Kooy, 1984). The THlike immunostaining of the islands was most intense dorsally and laterally, and there was a rim of strong immunostaining along the lateral edge of the caudoputamen.…”

Section: Resultsmentioning

confidence: 80%

Dopaminergic regulation of transcription factor expression in organotypic cultures of developing striatum

et al. 1995

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Dopamine is a major neurotransmitter in neural systems innervating the striatum, and dopamine receptors are expressed during early pattern formation in the developing striatum. To test for the functional responsiveness of developing striatal neurons to dopaminergic stimulation, we established an organotypic slice culture of newborn rat striatum. We analyzed the effects of dopamine receptor agonists and of adenylate cyclase and protein kinase activation on striatal neurons by measuring the induction of Fos-like and Fra-like proteins in the cultured striatum. Fos-like and Fra-like proteins were induced in striatal neurons by activation of D1-like dopamine receptors but not by activation of D2-like receptors. The induction of Fos-like protein was mainly in striosomes and a medial compartment next to the ventricular zone, whereas Fra-like protein was induced in the striatal matrix as well. cAMP analogs and forskolin induced widespread expression of both Fos-like and Fra-like proteins. Our findings thus suggest that neurons of developing striosome and matrix compartments not only have different functional coupling of D1-like receptors to adenylate cyclase, but also have distinct maturational programs for dopaminergic regulation of individual transcription factors. Finally, despite evidence that protein kinase was involved in the induction of Fos-like protein, experiments with kinase inhibitors suggested that the induction of Fos- like protein had unusual pharmacological characteristics and raised the possibility that a novel protein kinase A-like molecule may have been involved in the induction. The cultured striatal slice preparation should provide a valuable tool for analyzing the molecular determinants of striatal development and function.

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Section: Resultsmentioning

confidence: 80%

Dopaminergic regulation of transcription factor expression in organotypic cultures of developing striatum

et al. 1995

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“…Anatomical evidence indicates that striatal afferent fibers originating in the thalamus and neocortex terminate in the caudoputamen in a complex array of clusters (8)(9)(10)(11). At least part of the dopaminergic nigrostriatal connection appears also to terminate in clusters, because islands of fluorescence have been found in the striatum of the neonatal rabbit (6) and in the caudoputamen of adult rats pretreated with a tyrosine hydroxylase inhibitor (5). Diprenorphine binding studies in the rat (17) have shown that one set of putative receptors in the striatum, the opiate receptors, occur in patches.…”

Section: Discussionmentioning

confidence: 99%

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

Graybiel¹,

Ragsdale²

1978

Proc. Natl. Acad. Sci. U.S.A.

719

404

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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 ...

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“…Patch-and matrix-directed mesostriatal systems develop asynchronously, with the dopaminergic inputs to the patches developing prior to those in the matrix (Olson et al, 1972;Tennyson et al, 1972;Butcher and Hodge, 1976;Graybiel et al, 198 1;Graybiel, 1984;Moon-Edley and Herkenham, 1984;van der Kooy, 1984). This developmental sequence was examined in the present study by making injections of the neurotoxin 6-hydroxydopamine (6-OHDA) into the striatum of newborn rats at a time when the patch-directed system was in place, and prior to the ingrowth of the bulk of the input to the matrix.…”

mentioning

confidence: 99%

The neostriatal mosaic: III. Biochemical and developmental dissociation of patch-matrix mesostriatal systems

1987

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In the previous paper (Gerfen et al., 1987) mesostriatal dopaminergic neurons were shown to be subdivided into dorsal and ventral tiers that project to the striatal matrix and patch compartments, respectively. The present study provides experimental evidence that these patch- matrix mesostriatal dopaminergic systems are biochemically and developmentally distinct. A 28 kDa calcium-binding protein (CaBP, or calbindin-D28 kDa) is expressed in dorsal tier mesostriatal dopaminergic neurons. The distribution of such neurons, located in the ventral tegmental area, dorsal tier of the substantia nigra pars compacta, and retrorubral area, matches that of dopaminergic neurons that project to the striatal matrix. Dopaminergic neurons that do not express CaBP--those in the ventral tier of the pars compacta and in the pars reticulata--are distributed in a pattern that matches the origin of the dopaminergic projection to the striatal patches. During development, dopaminergic afferents to the striatal patch compartment are in place prior to the development of those to the matrix. Injections of the neurotoxin 6-hydroxydopamine (6-OHDA) into the striatum of newborn rats result in a selective and long-lasting depletion of dopaminergic afferents in the striatal patches. The later- developing matrix projection is relatively spared by such lesions. The distribution of surviving dopaminergic neurons, labeled with tyrosine hydroxylase (TH) immunoreactivity, matches the pattern of dorsal tier neurons previously shown to provide inputs to the matrix. Surviving neurons also express CaBP immunoreactivity and have dendrites that spread mediolaterally, in the plane of the pars compacta. On the other hand, those neurons that project to the patches are selectively lesioned by the neonatal 6-OHDA striatal injections, do not express CaBP, and have dendrites that are directed ventrally into the pars reticulata.

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The developing neostriatum of the rabbit: Correlation of fluorescence histochemistry, electron microscopy, endogenous dopamine levels, and [3H]dopamine uptake

Cited by 227 publications

References 35 publications

Dopaminergic regulation of transcription factor expression in organotypic cultures of developing striatum

Dopaminergic regulation of transcription factor expression in organotypic cultures of developing striatum

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

The neostriatal mosaic: III. Biochemical and developmental dissociation of patch-matrix mesostriatal systems

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