Patterns of cell lineage in the cerebral cortex reveal evidence for developmental boundaries

doi:10.1016/S0014-4886(05)80014-7

Experimental Neurology

Volume 109, Issue 1, July 1990, Pages 131-139

https://doi.org/10.1016/S0014-4886(05)80014-7 Get rights and content

Experimental aggregation chimeric mice offer a perspective on cell lineage relationships that is complementary to that of prospective tracing methods such as dye injections or recombinant retroviruses. To create a lineage map of cerebral cortex, the position and genotype of cortical neurons in three-dimensional space were reconstructed with the aid of a computer-assisted mapping system. Chi-square statistical analyses indicate that the spatial distribution of cell lineages in the cerebral cortex is highly nonrandom. When individual dimensions are analyzed separately, a high degree of order is found in the spatial distribution of neuronal genotype ratios in the anterior-posterior dimension but not in the medial-lateral dimension. This suggests an arrangement of lineage-related neurons into “slabs” or “stripes” of cells that are organized in the plane perpendicular to the neuraxis. Additionally, a highly significant variation in genotype ratios was found in the radial dimension (i.e., among cortical cell layers). These data suggest the hypothesis that separate sets of progenitor cells give rise to the superficial and deep layers of cortex. Taken together, our data are consistent with a picture of the developing nervous system in which early developmental restrictions to cell mixing set up boundaries that may be of considerable developmental genetic importance.

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Latexin is expressed in a subset of glutamatergic projection neurons located in the lateral but not the dorsomedial neocortex in rat. In the present study, we performed clonal analysis of embryonic cortical neurons in vitro using latexin as a subtype-specific molecular marker of glutamatergic neurons to address whether certain precursors in early cortical anlage are already committed to a single molecular phenotype. Dissociated cells from lateral cortex at embryonic day 12 were labelled with a replication-deficient retroviral vector containing the bacterial lacZ gene, and cultured in a monolayer for 3 weeks. Double-immunofluorescence staining was used to simultaneously visualize latexin- and β-galactosidase-immunopositive neurons. Out of 572 β-galactosidase-immunopositive clones examined, 27 clones contained latexin-expressing neuron(s). Of these 27 clones, 25 clones that contained three or more neurons were mixed clones containing both latexin-immunopositive and -immunonegative neurons. These results suggest that committed precursors to producing solely latexin-expressing neurons are not exist in the early cerebral cortical anlage.
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To analyze cell lineage in the rhesus monkey neocortex, we used recombinant retroviruses to label individual progenitor cells in the ventricular zone (VZ), then determined histochemically the distribution of their progeny during and after the period of cortical neurogenesis. Distribution patterns of labeled cells in the VZ suggested the coexistence of asymmetrically and symmetrically dividing progenitor cells, indicating that both postmitotic and mitotic progeny are produced during cortical neurogenesis. In the cortex, several distinct patterns of clonal distribution were observed and interpreted as follows: clones aligned radially suggested that asymmetrically dividing progenitors generate sequential “siblings” that migrate, in tandem, along a common radial path to the cortex. In contrast, clones oriented horizontally within a single lamina suggested that symmetric divisions produce multiple, laterally displaced progenitors which, in turn, simultaneously generate “cousin” cells that migrate, in concert, to the same cortical layer. Thus, we propose that different mitotic lineages, which coexist in the monkey VZ, produce distinct radial or laminar patterns of clone deployment that foreshadow the cytological organization of the adult neocortex.
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Regular ArticlePatterns of cell lineage in the cerebral cortex reveal evidence for developmental boundaries

Exp. Neurol.

Exp. Neurol.

Dev. Brain Res.

Dev. Biol.

Dev. Brain Res.

Neuron

Neuron

Dev. Biol.

Trends Neurosci.

Brain Res.

Dev. Brain Res.

Dev. Biol.

Brain Res.

Autoradiographic study of cell migration during histogenesis of cerebral cortex in mice

Nature (London)

Application of the quail-chick chimera system to the study of brain development and behavior

Science.

Architectonic map of neocortex of the normal mouse

J. Comp. Neurol.

Neuronal lineages in chimeric forebrain are compartmentally segregated

Neurosic. Abstr.

Radial arrangement of clonally related cells in the chicken optic tectum: Lineage analysis with a recombinant retrovirus

A new approach to the development of the cerebellum provided by the quail-chick marker system

Development

Cell lineage relationships in mammalian cerebellar cortex suggest early established migration boundaries

Receptive fields, binocular interaction and functional architecture in the cat's visual cortex

J. Physiol.

Functional architecture of macaque monkey visual cortex

Regular Article
Patterns of cell lineage in the cerebral cortex reveal evidence for developmental boundaries