Different origins and developmental histories of transient neurons in the marginal zone of the fetal and neonatal rat cortex

Abstract

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 in the lateral aspect of the telencephalic vesicle and cover its whole surface on E12. These cells, which show intense immunoreactivity for calbindin and calretinin, are characterized by their large size and axonal projection. They remain in the marginal zone after the formation of the cortical plate; they project first into the ventricular zone, and then into the subplate and the internal capsule. Therefore, these cells are the origin of the earliest efferent pathway of the developing cortex. Pioneer neurons are only present in prenatal brains. The second class is formed by subpial granule neurons, which form the subpial granular layer (SGL), previously considered to be found exclusively in the human cortex. SGL neurons are smaller than pioneer neurons. They are generated in a transient compartment of the retrobulbar ventricle between E12 and E14, and we propose the hypothesis that they invade the marginal zone, through tangential subpial migration, at different moments of fetal life. SGL neurons contain calbindin, calretinin, and gamma-aminobutyric acid (GABA), but the GABA-immunoreactive group becomes inconspicuous before birth. The extracellular matrix-like glycoprotein reelin, a molecule crucial for cortical lamination, is prenatally expressed by SGL neurons; postnatally, it is present in both Cajal-Retzius cells and subpial pyriform cells, both derivatives of SGL cells. In the rat, Cajal-Retzius cells are horizontal neurons that remain only until the end of the first postnatal week. They are located in layer I at a critical distance of approximately 20 microm from the pial surface and express reelin and, only occasionally, calretinin. Subpial pyriform cells coexpress reelin and calretinin and remain in layer I longer than Cajal-Retzius cells. Both pioneer neurons and subpial granule neurons are specific to the cortex. They mark the limit between the rudimentary cerebral cortex and olfactory bulb in the rat during early corticogenesis.

Na + channel-mediated Ca 2+ entry leads to glutamate secretion in mouse neocortical preplate

“…Radial glial cells could take part in communication between PP and VZ cells as it was demonstrated later in development (31). At E13, some of the PP pioneer cells send processes toward the VZ (32). Cells may also communicate by paracrine means as reported in immature CA1 pyramidal neurons before synapse formation (33).…”

Distinct ontogenic and regional expressions of newly identified Cajal-Retzius cell-specific genes during neocorticogenesis

“…With respect to the CR cell origins, many sources have been proposed, including the pallium (17), the subpallium (18), the retrobulbar area (16), and the cortical hem region (9). The Efb2 gene and the Gdn and p21 genes of the In situ hybridization analysis of CR genes was conducted in neocortical sections at E13.5 and P2, and the results are displayed in Top and Middle, respectively.…”

“…Most of the group 1 CR genes also were detected at the MZ of the caudomedial wall of the telencephalic vesicle (CMWT), including at the cortical hem and at the cortical surface of the pallium (data not shown), where newly generated CR cells from origins are supposed to be transiently accumulated (9,16). Importantly, signals of p21 and Gdn at E13.5 were abundantly seen at the CMWT possessing massive GFP-positive CR cells, whereas the signal of Ebf2 was considerably detected at the MZ adjacent to the ventral pallium (Fig.…”

“…4). These group 2 CR genes are thus distinctly expressed at the regions corresponding to the plausible CR cell origins at the early stage of corticogenesis (9,(16)(17)(18).…”

The N-terminal region of reelin regulates postnatal dendritic maturation of cortical pyramidal neurons

“…Upon completion of the cortical layer formation, the density of Cajal-Retzius cells decreases during the first two postnatal weeks (in rodents) as a consequence of progressive ''dilution,'' apoptosis, or differentiation into an interneuron-like phenotype (12)(13)(14). During that period, neurons expressing reelin remain confined to layer I (9,15).…”