Subpallial origin of a population of projecting pioneer neurons during corticogenesis.
Pyramidal neurons of the mammalian cerebral cortex are generated in the ventricular zone of the pallium whereas the subpallium provides the cortex with inhibitory interneurons. The marginal zone contains a subpial stream of migratory interneurons and two different classes of transient neurons, the pioneer neurons provided with corticofugal axons, and the reelin-expressing Cajal-Retzius cells. We found in cultured slices that the medial ganglionic eminence provides the reelin-negative pioneer neurons of the marginal zone. Pioneer neurons sent long projection axons that went through the cortical plate and reached the subplate and the lateral border of the lateral ganglionic eminence. In the cultured slices, pioneer neurons were functionally mature: they displayed a voltage-gated sodium current, expressed functional alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptors, and showed gamma-aminobutyric acid type A (GABAA) postsynaptic events that were modulated by presynaptic AMPA receptors. Pioneer neurons expressed the adhesion molecules L1 and TAG-1; the latter has been reported to control tangential migrations to the neocortex [Denaxa, M., Chan, C.-H., Schachner, M., Parnavelas, J. & Karagogeos, D. (2001) Development (Cambridge, U.K.) 128, 4635-4644], and we show here that the pioneer neurons of the marginal zone are the cellular substrate of such a function. Finally, we show that, in early corticogenesis, reelin controls both the tangential migration of cortical interneurons toward the cortical plate and the tangential migration of pioneer neurons toward the marginal zone.
Morante-Oria
Javier
J
Laboratory of Perception and Memory, Centre National de la Recherche Scientifique, Unité de Recherche Associée 2182, Pasteur Institute, 25 Rue du Docteur Roux, 75724 Paris, France.
Carleton
Alan
A
Ortino
Barbara
B
Kremer
Eric J
EJ
Fairén
Alfonso
A
Lledo
Pierre-Marie
PM
D000818:Animals; D015816:Cell Adhesion Molecules, Neuronal / Q000378:metabolism / Q000502:physiology; D002454:Cell Differentiation; D002465:Cell Movement / Q000502:physiology; D002540:Cerebral Cortex / Q000166:cytology* / Q000196:embryology* / Q000502:physiology; D058969:Contactin 2; D046508:Culture Techniques; D016326:Extracellular Matrix Proteins / Q000502:physiology; D018398:Homeodomain Proteins / Q000235:genetics / Q000378:metabolism; D051379:Mice; D018345:Mice, Knockout; D008818:Mice, Neurologic Mutants; D009419:Nerve Tissue Proteins; D018408:Patch-Clamp Techniques; D017966:Pyramidal Cells / Q000166:cytology* / Q000502:physiology; D018091:Receptors, AMPA / Q000378:metabolism; D011963:Receptors, GABA-A / Q000378:metabolism; D000091042:Reelin Protein; D012697:Serine Endopeptidases; D015222:Sodium Channels / Q000378:metabolism
D015816:Cell Adhesion Molecules, Neuronal; C548675:Cntn2 protein, mouse; D058969:Contactin 2; D016326:Extracellular Matrix Proteins; D018398:Homeodomain Proteins; D009419:Nerve Tissue Proteins; D018091:Receptors, AMPA; D011963:Receptors, GABA-A; D000091042:Reelin Protein; D015222:Sodium Channels; C000717128:Reln protein, mouse; D012697:Serine Endopeptidases