Studies of the earliest generated cells of the cat's visual cortex: cogeneration of subplate and marginal zones

Abstract

The earliest generated cells of the cat's telencephalon that may play a role in the formation of the primary visual cortex are the subject of this study. Using [3H]thymidine autoradiography, we have found that these cells are generated between embryonic day 24 (E24) and E30 (gestation is 65 days) and that they are present in very low numbers in the white matter of the adult brain. These cells are rarely labeled by injections made after E30, when the cells destined for the cortical layers are generated. Examination of the labeling pattern in the fetal brain 10 days or more after administration of [3H]thymidine between E24 and E30 revealed a bistratified distribution of these early generated cells. Labeled cells were found in large numbers in two embryonic zones flanking the developing cortical plate: above in the marginal zone and below in the subplate. (Some if not all of the marginal zone cells constitute the population of Cajal-Retzius cells of the cat's telencephalon.). These experiments indicate that cells of the subplate and marginal zones are cogenerated in time during the days just preceding the genesis of the cortical plate. We also examined the distribution of the early generated cells shortly after their genesis--on E30, a time when cells of the cortical plate are just being generated at the ventricular zone. In this case, the labeling pattern at the occipital pole was not bistratified. Rather, labeled cells were situated within a single zone extending from the pial surface inward to the border of the ventricular zone. This finding indicates that the cells of the subplate and marginal zones are generated as a contiguous population that is subsequently split apart by the insertion of cells forming the cortical plate. A comparison between the number of early generated cells found in fetal and newborn brains with that found in adult brains suggests that these cells are generated initially in substantial numbers but then largely disappear during early postnatal life, since injections of [3H]thymidine between E24 and E30 yielded large numbers of labeled cells in the white matter and layer 1 at birth, but very few at 2 months postnatal. This significant loss contrasted with the results from injections made just a few days later (E33) that resulted in large numbers of labeled cells in cortical layer 6 not only at birth but also in adulthood.(ABSTRACT TRUNCATED AT 400 WORDS)

Expression of neuron-specific tubulin defines a novel population in the proliferative layers of the developing telencephalon

“…1,2a,b). Later-generated neurons migrate between the preplate cells and form the cortical plate, which over time will give rise to the cellular layers of the cerebral cortex (Luskin and Shatz, 1985). The progressive change ofTuJ1 staining intensity also follows the degree of maturation of these layers: The more mature cells of the marginal zone and subplate layer have a more intense labeling than the cells of the cortical plate, which is composed of younger migrating or postmigratory neurons (Figs.…”

“…Additional clues to the composition of the proliferative zones stem from an examination of the candidate neurotransmitters expressed within them during the development of the cerebral cortex (Parnavelas et al, 1988;Chun and Shatz, 1989;Schambra et al, 1989;Van Eden et al, 1989;Hajos et al, 1990;Cobas et al, 199 1;Del Rio et al, 1992;Schwartz and Meinecke, 1992;Yan et al, 1992). However, it has not been resolved if the cells that express neurotransmitters in the proliferative zones are a subset of the early-generated subplate neurons (Luskin and Shatz, 1985;Chun and Shatz, 1989) or if they represent expression of neurotransmitters by immature neurons that are still undergoing migration. Furthermore, neurotransmitters are not an exclusive marker of neurons.…”

Cellular Strategies of Axonal Pathfinding

“…These early-born neurons are thought to guide both crossed and uncrossed retinal axons past the midline (Sretavan et al 1994). The subplate cells in the developing cortex, a transient cell layer above the subventricular zone and below the emerging cortical layers, serve as a temporary way-station where axons pause before entering the emerging permanent cortical layers (Luskin and Shatz 1985;Ghosh and Shatz 1992). The subplate is crucial for proper guidance and afferent invasion of the cortex (Catalano and Shatz 1998;Kanold et al 2003).…”

Regulation of the POU domain gene SCIP during cerebral cortical development

“…As shown in previous studies of rodent neurogenesis (Angevine and Sidman, 196 1;Berry and Rogers, 1965;Hicks and D'Amato, 1968;Miller, 1985), there is an overall inside-first, outside-last gradient of development. (Note that our injections began too late in embryogenesis to capture the earliest-developing preplate neurons that will reside both in layer 1 and in the subplate (sp) (Luskin and Shatz, 1985b;Bayer and Altman. 1990).…”