DIFFERENT ORIGINS AND DEVELOPMENTAL HISTORIES OF TRANSIENT NEURONS INTHE MARGINAL ZONE OF THE FETAL AND NEONATAL RAT CORTEX

Two major classes of early-born neurons are distinguished during early corticogenesis in the rat. The first class is formed by the cortical pioneer neurons, which are born in the ventricular neuroepithelium all over the cortical primordium. They appear at embryonic day (E) 11.5 i n the lateral aspect of the telencephalic vesicle and cover its whole surface on E12. These cells, which show intense immunoreactivity for c albindin and calretinin, are characterized by their large size and axo nal projection. They remain in the marginal zone after the formation o f the cortical plate; they project first into the ventricular zone, an d then into the subplate and the internal capsule. Therefore, these ce lls are the origin of the earliest efferent pathway of the developing cortex. Pioneer neurons are only present in prenatal brains. The secon d class is formed by subpial granule neurons, which form the subpial g ranular layer (SGL), previously considered to be found exclusively in the human cortex. SGL neurons are smaller than pioneer neurons. They a re generated in a transient compartment of the retrobulbar ventricle b etween E12 and E14, and we propose the hypothesis that they invade the marginal zone, through tangential subpial migration, at different mom ents of fetal life. SGL neurons contain calbindin, calretinin, and gam ma-aminobutyric acid (GABA), but the GABA-immunoreactive group becomes inconspicuous before birth. The extracellular matrixlike glycoprotein reelin, a molecule crucial for cortical lamination, is prenatally exp ressed by SGL neurons; postnatally, it is present in both Cajal-Retziu s cells and subpial pyriform cells, both derivatives of SGL cells. In the rat, Cajal-Retzius cells are horizontal neurons that remain only u ntil the end of the first postnatal week. They are located in layer I at a critical distance of approximately 20 mu m from the pial surface and express reelin and, only occasionally, calretinin. Subpial pyrifor m cells coexpress reelin and calretinin and remain in layer I longer t han Cajal-Retzius cells. Both pioneer neurons and subpial granule neur ons are specific to the cortex. They mark the limit between the rudime ntary cerebral cortex and olfactory bulb in the rat during early corti cogenesis. J. Comp. Neurol. 397:493-518, 1998. (C) 1998 Wiley-Liss, In c.