Relation Between Putative Transmitter Phenotypes and Connectivity of Subplate Neurons During Cerebral Cortical Development

Antonini, Antonella; Shatz, Carla J.

doi:10.1111/j.1460-9568.1990.tb00465.x

Cited by 111 publications

(65 citation statements)

References 73 publications

(117 reference statements)

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“…Both electrophysiological properties and cell morphology point to a high degree of underlying diversity among subplate neurons (Antonini & Shatz, 1990;Hanganu et al 2001;Hoerder, 2007). There are two basic classes of neuronal phenotypes in the subplate, glutamatergic and c-aminobutyric acid (GABA)ergic (Antonini & Shatz, 1990;Meinecke & Rakic, 1992), with each class expressing heterogeneous molecular markers (Allendoerfer & Shatz, 1994;Hevner & Zecevic, 2006;Hoerder-Suabedissen et al 2009). It is not yet clear whether the same types of subplate neurons possess intracortical and extracortical projections and how the diverse somatodendritic morphologies relate to the equally diverse neurochemical properties and physiological fingerprints.…”

Section: Multiple Functions Of Subplate Neurons During Cortical Develmentioning

confidence: 99%

Subplate in the developing cortex of mouse and human

et al. 2010

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The subplate is a largely transient zone containing precocious neurons involved in several key steps of cortical development. The majority of subplate neurons form a compact layer in mouse, but are dispersed throughout a much larger zone in the human. In rodent, subplate neurons are among the earliest born neocortical cells, whereas in primate, neurons are added to the subplate throughout cortical neurogenesis. Magnetic resonance imaging and histochemical studies show that the human subplate grows in size until the end of the second trimester. Previous microarray experiments in mice have shown several genes that are specifically expressed in the subplate layer of the rodent dorsal cortex. Here we examined the human subplate for some of these markers. In the human dorsal cortex, connective tissue growth factor-positive neurons can be seen in the ventricular zone at 15-22 postconceptional weeks (PCW) (most at 17 PCW) and are present in the subplate at 22 PCW. The nuclear receptor-related 1 protein is mostly expressed in the subplate in the dorsal cortex, but also in lower layer 6 in the lateral and perirhinal cortex, and can be detected from 12 PCW. Our results suggest that connective tissue growth factor-and nuclear receptor-related 1-positive cells are two distinct cell populations of the human subplate. Furthermore, our microarray analysis in rodent suggested that subplate neurons produce plasma proteins. Here we demonstrate that the human subplate also expresses a2zinc-binding globulin and Alpha-2-HeremansSchmid glycoprotein ⁄ human fetuin. In addition, the established subplate neuron marker neuropeptide Y is expressed superficially, whereas potassium ⁄ chloride co-transporter (KCC2)-positive neurons are localized in the deep subplate at 16 PCW. These observations imply that the human subplate shares gene expression patterns with rodent, but is more compartmentalized into superficial and deep sublayers. This increased complexity of the human subplate may contribute to differential vulnerability in response to hypoxia ⁄ ischaemia across the depth of the cortex. Combining knowledge of cell-type specific subplate gene expression with modern imaging methods will enable a better understanding of neuropathologies involving the subplate.

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Section: Multiple Functions Of Subplate Neurons During Cortical Develmentioning

confidence: 99%

Subplate in the developing cortex of mouse and human

et al. 2010

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“…Moreover, recent evidence has shown that certain transient neuronal populations are essential for the formation of neural networks by providing guiding and targeting cues necessary for the establishment of the axon pathway. Striking examples of such a role are the subplate neuronal population of the developing cerebral cortex, which is essential for the formation of appropriate thalamocortical relationships (Shatz, 1992;Antonini and Shatz, 1990;McConnell et al, 1989;Luskin and Shatz, 1985). and the many examples of guidepost cells in invertebrates (Palka et al, 1992).…”

Section: Introductionmentioning

confidence: 99%

Characterization of the phenotype and birthdates of pyknotic dead cells in the nervous system by a combination of DNA staining and immunohistochemistry for 5'-bromodeoxyuridine and neural antigens.

Soriano

Rı́o²,

Auladell³

1993

J Histochem Cytochem.

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Cells displaying highly condensed pyknotic nuclei, the most characteristic feature of apoptosis, are considered as dead cells in neural tissue. The present study aimed to devise methods that could allow the neurogenetic and phenotypic characterization of dying pyknotic cells. In the first set of experiments, pregnant mice were labeled at embryonic days E10-El6 with pulses of 5'-bromodeoxyuridine (BrdU). Offspring were processed for the immunocytochemical visualization of BrdU after an immunoperoxidase reaction. In addition to normal, healthy immunopositive nuclei, these preparations displayed a number of pyknotic nuclei that were immunoreactive for BrdU. Both the regional and the temporal distribution of BrdU-positive pyknotic cells were coincidental with the peaks of dead cells in neural tissue. For example, pulses of BrdU at E10-E11 resulted in the visualization of immunoreactive pyknotic cells in the subplate and white matter of the cerebral cortex in early postnatal (P) animals. Thus, the times of generation (birthdates) of cells subjected to degenerative processes can be unequivocally identified. In the second set of experiments, brain sections from unlabeled littermates were immunostained for a variety of neural and glial markers and counterstained with bisbenzimide, to find antigens which, by being present in degener-

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“…A second type of SPi-positive neuron had an inverted pyramidal-shaped cell body and dendritic spines. Similar types of inverted pyramidal subplate neurons project to the thalamus and can be labeled by the retrograde transport of [3H]aspartate (40). In addition, Golgi impregnation or intracellular staining ofkitten cortical subplate neurons with biocytin has revealed some subplate neurons with typical pyramidal or bipolar cell bodies (30).…”

Section: Resultsmentioning

confidence: 99%

Expression of a unique 56-kDa polypeptide by neurons in the subplate zone of the developing cerebral cortex.

Naegele

Barnstable

Wahle

1991

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

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In the mammalian cerebral cortex, neurons destined for layers 2-6 are generated only after the period of genesis for a group of transient neurons that populate the subplate and marginal zones. Although a number of molecular markers for the subplate zone exist, most are also expressed by other cell populations in the cortical plate. To begin to study molecular properties of the subplate, we generated monoclonal antibodies against homogenates of cat cortical subplate zone. One monoclonal antibody, termed subplate 1 (SP1), recognized a polypeptide of 56 kDa. This antigen was strongly expressed within the subplate neurons only during a 3-week period nning at birth and extending until 3 weeks after birth. From postnatal day 1, the number of SPi-immunoreactive neurons below the visual cortex increased until the end of second postnatal week and then declined thereafter. This period coincides with the period when a majority of the subplate neurons undergo naturally occurring cell death. The antigen was not expressed by subplate neurons surviving in the adult white matter. At the peak of antigen expression, 14% or less of the immunoreactive neurons also coexpressed -aminobutyric acid, somatostatin, or neuropeptide Y. Biochemical and immunocytochemical properties of the SP1 antigen were also compared with the Alz-50 antigen (A68), a marker for dying neurons. On Western blots, SP1-and Alz-50-reactive polypeptides were selectively enriched in cytosolic fractions of kitten cerebral cortex, but each marker recognized different molecular weight polypeptides. In tissue sections many subplate, cortical plate, and layer 1 neurons were Alz-50 immunoreactive. In contrast, a rarer subpopulation of neurons restricted to the subplate was labeled by SP1. We propose that the SP1 antigen is a protein expressed within dying cortical subplate neurons, at the commencement of cell death.In mammals, the cerebral cortex initially includes a number of transient zones that do not persist in the mature brain (1). Of particular interest is the subplate zone, whose functions appear to include guiding axons that enter or leave the cortex (2-&). This zone is populated by the earliest-generated cortical neurons and lies between the cortical plate and the future white matter (8)(9)(10) MATERIALS AND METHODS Generation of Monoclonal Antibodies (mAbs). Postnatal mice received subcutaneous immunizations with homogenate obtained from paraformaldehyde-fixed adult rat cortical white matter, optic nerves, and trigeminal nerves to generate tolerance to adult white matter antigens (22, 23). Tolerizing injections were carried out on postnatal day (PND) 0, PND 2, PND 4, PND 6, PND 8, and PND 10. Tolerized mice were then immunized on days 21, 25, and 29 with intraperitoneal and subcutaneous injections of paraformaldehyde-fixed tissue homogenates from the subplate region ofPND 1 and PND 12 kittens emulsified in Freund's complete (first injection only) or Freund's incomplete adjuvant. On PND 33, the mice received a booster injection of subplate antigen into...

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Relation Between Putative Transmitter Phenotypes and Connectivity of Subplate Neurons During Cerebral Cortical Development

Cited by 111 publications

References 73 publications

Subplate in the developing cortex of mouse and human

Subplate in the developing cortex of mouse and human

Characterization of the phenotype and birthdates of pyknotic dead cells in the nervous system by a combination of DNA staining and immunohistochemistry for 5'-bromodeoxyuridine and neural antigens.

Expression of a unique 56-kDa polypeptide by neurons in the subplate zone of the developing cerebral cortex.

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