Cortical Cells That Migrate Beyond Area Boundaries: Characterization of an Early Neuronal Population in the Lower Intermediate Zone of Prenatal Rats

Studies of the early development of the mammalian cerebral cortex have revealed that the earliest generated neurons that form the primordial plexiform layer (also called preplate or marginal zone) distribute among layer I and layer VII (subplate). By means of bromodeoxyuridine labelling of cells becoming postmitotic, we have found evidence that, in the rat, an additional group of neurons of the primordial plexiform layer remains in the close vicinity of the ventricular zone. This finding, in line with the proposal by Marín‐Padilla (Z Anat. Entwicklungsgesch., 134, 117‐145, 1971), implies that the primordial plexiform layer suffers a tripartition after the formation of the cortical plate and of the intermediate zone (the latter soon becomes the embryonic white matter). Thus, primordial plexiform layer derivatives are in layer I, layer VII (subplate) and in the lower part of the embryonic white matter. This early generated neuronal population is also revealed with an antibody that recognizes the larger (67 kDa) isoform of glutamic acid decarboxylase (Kaufman et al., Science, 232, 1138‐1140, 1986). This is in accord with the earlier finding of a GABA‐containing cell population showing a similar spatiotemporal distribution. The early generated neurons of the embryonic white matter migrate tangentially and, in early postnatal animals, are found as interstitial cells in the medial regions of the subcortical white matter and at the midline in the corpus callosum. At caudal levels, similar cells invade the subpyramidal strata of the developing hippocampus. This tangential migration might explain the tangential dispersion of neural cell clones described in recent studies of cell lineage in the cerebral cortex.

[1]  L. Garey,et al.  Prenatal development of GABA-immunoreactive neurons in the human striate cortex. , 1992, Brain research. Developmental brain research.

[2]  M. Marín‐Padilla,et al.  Early Ontogenesis of the Human Cerebral Cortex , 1988 .

[3]  A. Fairén,et al.  Transient GABA-like immunoreactive axons in the corpus callosum of perinatal rats , 1988, Neuroscience Letters.

[4]  C. Cepko,et al.  Widespread dispersion of neuronal clones across functional regions of the cerebral cortex. , 1992, Science.

[5]  P. Rakić Neurons in Rhesus Monkey Visual Cortex: Systematic Relation between Time of Origin and Eventual Disposition , 1974, Science.

[6]  R. Reep,et al.  Layer VII of rodent cerebral cortex , 1988, Neuroscience Letters.

[7]  H. Kennedy,et al.  Cortical specification of mice and men. , 1993, Cerebral cortex.

[8]  C. Shatz,et al.  Changing patterns of synaptic input to subplate and cortical plate during development of visual cortex. , 1991, Journal of neurophysiology.

[9]  E Friauf,et al.  Functional synaptic circuits in the subplate during fetal and early postnatal development of cat visual cortex , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[10]  Maria B. Luskin,et al.  Restricted proliferation and migration of postnatally generated neurons derived from the forebrain subventricular zone , 1993, Neuron.

[11]  J. Wolff,et al.  Development of GABAergic neurons in rat visual cortex as identified by glutamate decarboxylase-like immunoreactivity , 1984, Neuroscience Letters.

[12]  M. Schwartz,et al.  Early expression of GABA-containing neurons in the prefrontal and visual cortices of rhesus monkeys. , 1992, Cerebral cortex.

[13]  M. Böswald,et al.  Tracer dose and availability time of thymidine and bromodeoxyuridine: application of bromodeoxyuridine in cell kinetic studies , 1990, Cell and tissue kinetics.

[14]  K. Valentino,et al.  The early formation of the corpus callosum: a light and electron microscopic study in foetal and neonatal rats , 1982, Journal of neurocytology.

[15]  P. Rakić Mode of cell migration to the superficial layers of fetal monkey neocortex , 1972, The Journal of comparative neurology.

[16]  M. Geffard,et al.  Antibodies against gamma-aminobutyric acid: specificity studies and immunocytochemical results. , 1984, Proceedings of the National Academy of Sciences of the United States of America.

[17]  P. Rakic Specification of cerebral cortical areas. , 1988, Science.

[18]  D. O'Leary,et al.  Do cortical areas emerge from a protocortex? , 1989, Trends in Neurosciences.

[19]  J. Katzmann,et al.  A monoclonal antibody reactive with 5-bromo-2-deoxyuridine that does not require DNA denaturation. , 1985, Cytometry.

[20]  C. Cepko,et al.  Cellular migration patterns in the developing mouse cerebral cortex. , 1990, Development.

[21]  R. Sidman,et al.  Autoradiographic Study of Cell Migration during Histogenesis of Cerebral Cortex in the Mouse , 1961, Nature.

[22]  V. Caviness,et al.  The alignment of migrating neural cells in relation to the murine neopallial radial glial fiber system. , 1991, Cerebral cortex.

[23]  H. Uylings,et al.  Prenatal development of GABA‐ergic neurons in the neocortex of the rat , 1989, The Journal of comparative neurology.

[24]  M. Chesselet,et al.  Distribution of glutamic acid decarboxylase (Mr 67 000) in the basal ganglia of the rat: an immunohistochemical study with a selective cDNA-generated polyclonal antibody , 1991, Journal of neurocytology.

[25]  I. Ferrer,et al.  Development of GABA‐immunoreactivity in the neocortex of the mouse , 1992, The Journal of comparative neurology.

[26]  T. Kirkwood,et al.  Neuronal precursor cells in the rat hippocampal formation contribute to more than one cytoarchitectonic area , 1992, Neuron.

[27]  D. I. Vaney Photochromic intensification of diaminobenzidine reaction product in the presence of tetrazolium salts: applications for intracellular labelling and immunohistochemistry , 1992, Journal of Neuroscience Methods.

[28]  L. Puelles,et al.  Tangential neuronal migration in the avian tectum: cell type identification and mapping of regional differences with quail/chick homotopic transplants. , 1992, Brain research. Developmental brain research.

[29]  F. Valverde,et al.  Development and differentiation of early generated cells of sublayer VIb in the somatosensory cortex of the rat: A correlated Golgi and autoradiographic study , 1989, The Journal of comparative neurology.

[30]  C. Shatz,et al.  Studies of the earliest generated cells of the cat's visual cortex: cogeneration of subplate and marginal zones , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[31]  R Berezney,et al.  Mapping replicational sites in the eucaryotic cell nucleus , 1989, The Journal of cell biology.

[32]  C. Shatz,et al.  Transient cells of the developing mammalian telencephalon are peptide-immunoreactive neurons , 1987, Nature.

[33]  A. Tobin,et al.  Brain glutamate decarboxylase cloned in lambda gt-11: fusion protein produces gamma-aminobutyric acid. , 1986, Science.

[34]  S. Breen,et al.  Radial mosaicism and tangential cell dispersion both contribute to mouse neocortical development , 1993, Nature.

[35]  L. Thurlow,et al.  Cell lineage in the rat cerebral cortex: a study using retroviral-mediated gene transfer. , 1988, Development.

[36]  I. Smart,et al.  Growth patterns in the lateral wall of the mouse telencephalon: I. Autoradiographic studies of the histogenesis of the isocortex and adjacent areas. , 1982, Journal of anatomy.

[37]  C. Shatz,et al.  Neurogenesis of the cat's primary visual cortex , 1985, The Journal of comparative neurology.

[38]  A. Cobas,et al.  Prenatal development of the intrinsic neurons of the rat neocortex: A comparative study of the distribution of GABA-immunoreactive cells and the GABAA receptor , 1991, Neuroscience.

[39]  T. Verdoorn,et al.  Prenatal ontogeny of the gabaergic system in the rat brain: An immunocytochemical study , 1986, Neuroscience.

[40]  W. Oertel,et al.  Production of a specific antiserum to rat brain glutamic acid decar☐ylase by injection of an antigen-antibody complex , 1981, Neuroscience.

[41]  C. Cepko,et al.  Clonal dispersion in proliferative layers of developing cerebral cortex , 1993, Nature.

[42]  J. Sanes,et al.  Migratory paths and phenotypic choices of clonally related cells in the avian optic tectum , 1991, Neuron.

[43]  S. Mcconnell,et al.  Diverse migratory pathways in the developing cerebral cortex. , 1992, Science.

[44]  B. Chronwall,et al.  Prenatal and postnatal development of GABA‐accumulating cells in the occipital neocortex of rat , 1980, The Journal of comparative neurology.

[45]  P. Levitt,et al.  A unique membrane protein is expressed on early developing limbic system axons and cortical targets , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[46]  M. Jacobson,et al.  Embryonic vertebrate central nervous system: Revised terminology , 1970 .

[47]  K. Kishi Golgi studies on the development of granule cells of the rat olfactory bulb with reference to migration in the subependymal layer , 1987, The Journal of comparative neurology.

[48]  C. Houser,et al.  Two Forms of the γ‐Aminobutyric Acid Synthetic Enzyme Glutamate Decarboxylase Have Distinct Intraneuronal Distributions and Cofactor Interactions , 1991, Journal of neurochemistry.

[49]  M. Vitale,et al.  High-resolution detection of newly synthesized DNA by anti-bromodeoxyuridine antibodies identifies specific chromatin domains. , 1990, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.