Direct demonstration of a correspondence between the dopamine islands and acetylcholinesterase patches in the developing striatum.

Abstract

The distribution of dopamine-containing processes in the striatum of fetal and neonatal cats was studied by immunohistochemical and glyoxylic acid histofluorescence methods and compared to the distribution of acetylcholinesterase (acetylcholine acetylhydrolase, EC 3.1.1.7) observed by thiocholine histochemistry in the same or serially adjoining sections. Both methods for demonstrating the dopamine innervation revealed the characteristic patchwork of dopamine "islands" in the caudoputamen, in which catecholamine histofluorescence or tyrosine hydroxylase [tyrosine 3-monooxygenase; L-tyrosine, tetrahydropteridine: oxygen oxidoreductase (3-hydroxylating), EC 1.14.16.21-like immunoreactivity was concentrated into 0.2-to 0.6-mm-wide patches. Both methods also demonstrated a high degree ofpatterning of the dopamine innervation in the ventral striatum, including the nucleus accumbens septi. A detailed and striking match was found between these configurations and the compartmental distribution of acetylcholinesterase observed in the caudoputamen and ventral striatum of the same brains. The correspondence between the dopamine and acetylcholinesterase figures was most obvious in the fetal brains, in which the background acetylcholinesterase staining was lightest, but matches between the dopamine islands and acetylcholinesterase patches could still be seen in the kittens. There was no clear alignment of striatal cell bodies stained for acetylcholinesterase with either the dopamine or the acetylcholinesterase-positive patches. Nor was there an obvious correspondence between dopamine and acetylcholinesterase in the striatal background matrix. We conclude that, at least during ontogenesis, it is the clustered arrangements of dopamine and acetylcholinesterase that are, in particular, tightly linked, and we suggest that information about the maturation of these clusters may be crucial in assessing the functions of striatal dopamine and acetylcholinesterase in the adult.A surprising outcome ofrecent work on the caudate nucleus and putamen is that these telencephalic nuclei, although subcortical, are divided up into orderly sets ofanatomical compartments with distinct histochemical properties and fiber connections. In the mature striatum, incoming afferents from the neocortex (1, 2) and thalamus (3-5), striatal projection cells (6), and certain neuropeptides (7) form three-dimensional patchworks, and we have shown that these heterogeneous distributions are for the most part aligned with a network of acetylcholinesterase (acetylcholine acetylhydrolase, EC 3.1.1.7)-poor zones called striosomes (8-10). The implications of these correspondences are ofat least two sorts. First, though electrophysiological evidence is still lacking, it is clear from the anatomy that these striosomal units must be functional units because they represent subdivisions in which connections become established between particular sets of striatal inputs and outputs. Second, the findings suggest that there is a compartmentalization of different pharmac...

Compartment-Specific Modulation of GABAergic Synaptic Transmission by μ-Opioid Receptor in the Mouse Striatum with Green Fluorescent Protein-Expressing Dopamine Islands

“…These GFPpositive and TH-immunoreactive "dopamine islands" are composed of axons from dopamine neurons of the substantia nigra and do not contain any intrinsic dopamine cells. It has been established that the dopamine islands correspond to the striosome compartments (Graybiel et al, 1981;Herkenham and Pert, 1981). The striosomes were thus identified as bright GFP-rich areas under a fluorescence microscope (Fig.…”

“…We therefore identified dopamine islands as striosomal compartments. The dopamine islands of the developing striatum correspond to the acetylcholinesterase-poor and MORenriched striosomes/patches (Graybiel et al, 1981;Herkenham and Pert, 1981). In the rat, the striosomal neurons are born at embryonic day 12 (E12) and only become patchy as the matrix neurons generated at E18 -E21 migrate out into the striatum (Edley and Herkenham, 1984;Fishell and van der Kooy, 1987).…”

Retrograde axonal transport of glial cell line-derived neurotrophic factor in the adult nigrostriatal system suggests a trophic role in the adult.

“…Developmentally, these areas are the first to become innervated by dopamine nerve terminals (24,25). This structural subdivision of striatum persists in the adult in the form of striosomes (26)(27)(28)(29).…”

Compartmentalization of excitatory amino acid receptors in human striatum.

“…Recent evidence suggests that the neostriatum is able to maintain segregated information flow due to compartmentalization in mammalian caudate and putamen (1)(2)(3)(4)(5)(6)(7)(8)(9)(10)(11). Distinct regions within caudate and putamen have been defined in several species with histochemical techniques, in situ hybridization, and neurotransmitter receptor binding studies in rat (1,(12)(13)(14)(15), cat (10,14,(16)(17)(18)(19)(20), primate (12,14,(19)(20)(21)(22), and human (20,(23)(24)(25)(26). These compartments, termed striosomes and matrix, exhibit distinct afferent and efferent connections.…”