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Journal of Neuroscience, Vol 13, 1730-1750, Copyright © 1993 by Society for Neuroscience
Neurons, astrocytes, and oligodendrocytes of the rat cerebral cortex originate from separate progenitor cells: an ultrastructural analysis of clonally related cells
MB Luskin, JG Parnavelas and JA Barfield
Department of Anatomy and Cell Biology, Emory University School of Medicine, Atlanta, Georgia 30322.
The diverse array of neurons and glia in the mammalian cerebral cortex
arises from proliferating cells of the ventricular zone that surrounds the
lateral ventricles of the developing brain. A fundamental but unresolved
question is whether the individual cells of the ventricular zone are
committed to producing progeny of only one particular phenotype or whether
they generate progeny of more than one phenotype. We have begun to address
this question by asking if individual cells of the ventricular zone
generate exclusively neurons or glia at the onset of cortical neurogenesis
in the rat. To assess the phenotypes of cells derived from a common
progenitor cell, retroviral-mediated gene transfer was used to introduce
the reporter gene, Escherichia coli beta- galactosidase, into ventricular
zone cells at embryonic day 15 or 16. We used histochemistry to reveal
beta-galactosidase-expressing cells in the mature rat cerebral cortex.
Isolated clusters of beta-galactosidase- expressing cells, presumably
clones, were identified in serial sections. Since the histochemical
reaction product is electron dense, each cell could be examined at the
ultrastructural level and assigned definitively to one of the major classes
of cells in the cerebral cortex on the basis of well-established
morphological criteria. This approach overcomes the problems of cell type
identification encountered with light microscopy, where it is not always
possible to distinguish between different cell phenotypes. We found that
virtually all clones contained cells of exclusively one type: either all
astrocytes, all oligodendrocytes, or all neurons. Furthermore, each
particular cell type exhibited a different pattern and intensity of
staining. The neuronal clones, with one exception, were composed of either
all pyramidal cells (projection neurons), or all nonpyramidal cells
(interneurons). The size and composition of neuronal clones did not seem
related to their position in the cerebral cortex. Collectively, our
observations indicate that separate progenitor cells exist for pyramidal
neurons, nonpyramidal neurons, astrocytes, and oligodendrocytes. The
striking phenotypic homogeneity in the clones arising from individual
progenitor cells suggests that by the onset of cortical neurogenesis, at
least some lineage restrictions have already occurred among the precursor
cell population. Thus, our results suggest that lineage may play a pivotal
role in determining some of the functionally important phenotypic
attributes of cells in the cerebral cortex.
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