Compartmentalization of the embryonic striatum after intraocular transplantation

doi:10.1016/0165-3806(87)90166-0

Developmental Brain Research

Volume 33, Issue 2, June 1987, Pages 310-314

https://doi.org/10.1016/0165-3806(87)90166-0 Get rights and content

Abstract

In order to assess the intrinsic potential of the isolated embryonic striatum to develop its adult patch and matrix compartments, embryonic day 16 striata were transplanted into the anterior eye chamber of adult host rats. After 2–12 weeks of survival the transplants showed heterogeneous and in the majority of cases complementary distributions of opiate receptor binding and acetylcholinesterase staining, which mark the patch and matrix compartments of the adult striatum, respectively. The complementarity of patch and matrix markers in the transplants shows that the transplants do compartmentalize. However, the density of the markers in the transplants did not reach the levels seen in the adult striatum. The results suggest that the commitment of cells to a striatal compartment is a very early event in the embryonic development of the forebrain.

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Cited by (14)

Mosaic distribution of chondroitin and keratan sulphate in the developing rat striatum: Possible involvement of proteoglycans in the organization of the nigrostriatal system
1998, Developmental Brain Research
The striatum of the mammalian basal ganglia is composed of two neurochemically distinct compartments termed patches and matrix that contribute overall to a mosaic organization. Glycosaminoglycans (GAGs), the sugar moieties of proteoglycans, provide specific spatio-temporal guidance cues during the development of several functional neural systems. However, their distribution within the nigrostriatal system has not been investigated yet. Here, the immunohistochemical distributions of unsulphated (C0S), 4-sulphated (C4S) and 6-sulphated chondroitin (C6S) and keratan sulphate (KS) were examined in the developing neostriatum of rat and compared with the distribution of dopaminergic terminals. All the chondroitin sulphate (CS) isomers are homogeneously expressed in the embryonic striatum. After birth, C0S and C6S reveal the striatal mosaic in being preferentially expressed within the matrix compartment and in boundaries around patches whereas the C4S epitope is present in both compartments, with a slight patchy distribution. KS expression is detected first in the patches during the early postnatal period and subsequently only in the matrix compartment. All these GAG expressions disappear as the brain matures except for C4S which remains high throughout adult life. Furthermore, studies within the developing medial forebrain bundle reveal that CS isomers, but not KS, are expressed in and around the dopamine axonal tract but show similar developmental patterns of distribution which do not appear to be specifically associated with the nigrostriatal pathway. These results suggest a possible implication of proteoglycans during the development of the striatum and may be useful for understanding the complex cellular and molecular interactions in degeneration and plasticity of the nigrostriatal circuit in Parkinson's disease.
Transient compartmental expression of a family of protein tyrosine phosphatases in the developing striatum
1996, Developmental Brain Research
The expression of a family of intracellular protein tyrosine phosphatases (STEP) was studied in the striatum of rats during ontogeny. Links between the formation of dopamine islands and STEP immunoreactive patches in the striatum were examined since previous work had suggested that STEP isoforms were selectively expressed in dopaminoceptive brain regions. STEP protein and mRNAs were distributed in a patchy manner during the first postnatal week. By 2 weeks, STEP immunoreactivity was homogeneous, indicating that both patch and matrix neurons express STEP by maturity. Two-color immunofluorescent staining was also performed to compare STEP with specific markers for patch and matrix. Tyrosine hydroxylase immunoreactive fibers from the substantia nigra form distinctive dopamine islands in the striatum during late embryonic development, and occupy the sites of future patches [23,37,38,54]. These fiber islands align with STEP immunoreactive neuronal patches during the first two postnatal weeks, suggesting that STEP is a marker for patch neurons in early postnatal development. When STEP's distribution was compared with other markers for patch (substance P) or matrix (calbindin), STEP co-localized with substance P in most striatal neurons on postnatal days 1 through 7. However, STEP was also expressed within a subset of calbindin-positive neurons in the lateral striatum, but not with these neurons elsewhere in the striatum. By adulthood, STEP colocalized with both markers. These results suggest that STEP is expressed first within patch neurons but not matrix, and subsequently within both. The expression of STEP may be triggered by the arrival of striatal afferents or other regulatory factors.
Compartmental organization of the peptide network in the human caudate nucleus
1994, Journal of Chemical Neuroanatomy
The mammalian striatum may be divided into a striosomal compartment and a surrounding matrix region. We have examined the distribution of leucine enkephalin (LENK) and substance P (SP) immunoreactivity in relation to striosomes defined by calbindin-D (CABD) staining in alternate 70 μm serial sections from the human caudate nucleus. The distribution of LENK immunoreactivity showed a transition from dorsal to ventral striatum: dorsally, LENK-rich patches were present in a lightly stained matrix; mid-ventrally, annular patches of LENK staining with a lighter core were seen. These patches corresponded to striosomal regions defined by CABD-poor zones. In contrast, in the ventral caudate and nucleus accumbens, LENK-poor zones matched CABD-defined striosomes. CABD staining in the matrix was intense in the dorsal caudate, diminishing ventrally. SP-rich zones in dorsal caudate and SP-poor areas in the mid-ventral region overlapped striosomes. In the ventromedial sector, the SP staining pattern was complex and did not consistently correlate with striosomes. Computer-assisted three-dimensional reconstruction of the striosomal system in the human, based on regions of either high LENK or low CABD immunoreactivity, revealed the existence of considerable long-range order. Patches appeared aligned over several millimeters to form long, horizontal structures in the caudate nucleus, with occasional orthogonal interconnecting crossbridges. Our results are in accord with previous work in the human and in other species. These three-dimensional networks are strikingly similar across individuals and may relate to the segregation of and interactions between striatal circuits.
Spatially localized neuronal cell lineages in the developing mammalian forebrain
1993, Neuroscience
The role of cell lineage in the organization of the cerebral cortex and striatum of the developing rat forebrain was analysed using retroviral-mediated gene transfer to mark the progeny of individual progenitors. Injections around the onset of neurogenesis (embryonic day 14) produced neuronal- and glial-specific clones in the striatum and cortex. The majority of the neuronal clones were restricted to either the deep or superficial layers of the cortex and to either the striatal patch or matrix compartments of the striatum. Moreover, modeling the distributions of the neuronal clones in various ways revealed that grouping the clones into deep vs superficial cortical compartments and patch vs matrix striatal compartments best accounted for the clone distributions.
These results suggest that at the onset of neurogenesis there is a heterogeneity of neuronal progenitors within the proliferative ventricular zone.
Embryonic lesions of the substantia nigra prevent the patchy expression of opiate receptors, but not the segregation of patch and matrix compartment neurons, in the developing rat striatum
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Unilateral lesions of the substantia nigra on embryonic day 19 prevent the development of the normal patchy distribution of opiate receptors in the ipsilateral rat striatum. Independent, early and permanent labelling of patch compartment neurons in the same brains on embryonic day 14 with [³H]thymidine revealed that the substantia nigra lesions did not prevent the aggregation of early born neurons into patches, but rather blocked the normal expression of one phenotype (dense opiate receptor binding) of these patches. Thus, early nigrostriatal connections may not be critical for the fundamental patch/matrix compartmentation of the striatum, but may be important in the maturation of phenotypic markers of these compartments.
Mechanisms of striatal pattern formation: conservation of mammalian compartmentalization
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The striatum is composed of two neuroanatomically and neurochemically defined compartments, termed the patches and matrix. We compared this compartmentalization of the striatum in sections from the rat, rhesus monkey and human, in terms of (1) total striatal area, (2) the ratio of patch to matrix areas, (3) the number of patches and (4) the cross-sectional area of individual patches. Dense μ-opiate receptor binding and immunohistochemical staining for enkephalin were used as histochemical markers for the patch compartment and heavy immunostaining for calcium binding protein was used as a matrix marker. Analysis of coronal sections revealed that a relatively constant ratio of 15% patch to 85% matrix area is maintained in each species. The numbers of patches also remain relatively constant across species, despite a 19-fold increase in total striatal area from rat to human. The constant ratio of patch to matrix areas is maintained by an increase in the size of the individual patches. We hypothesize that the maintenance of a 15% patch to 85% matrix ratio in the striata of different mammalian species occurs through proportionate changes in the length of striatal neurogenesis and the numbers of striatal precursors in the ventricular zone, whereas the maintenance of average patch number is proposed to be a function of reciprocal connections with the substantia nigra and adhesive factors that are specific to patch cells.

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^☆: Supported by the Medical Research Council of Canada. Thanks to Dr. Jose Nobrega For his assistance with densitometry.

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Short communicationCompartmentalization of the embryonic striatum after intraocular transplantation☆

Abstract

Brain Res.

J. Neurosci. Meth.

Neuroscience

Neuroscience

Neurosci. Lett.

Dev. Brain Res.

Dev. Brain Res.

Brain Res.

Short communication
Compartmentalization of the embryonic striatum after intraocular transplantation☆