Origin of the Cortical Layer I in Rodents

Abstract

Using birthdating techniques, we have studied when cells that settle in the marginal zone (future layer 1) of the cortical neuroepithelium are generated in developing rat embryos. The majority of marginal zone cells are generated at embryonic day 12 (E12), E13 and E14, although some cells generated later can incorporate into this stratum after the cortical plate forms. The nature and the origin of the cell populations that colonize the preplate/marginal zone was studied by means of immunohistochemistry using cell markers for γ-amino butyric acid (GABA), reelin and the calcium binding proteins calretinin and calbindin. At early stages of development, the preplate is formed by Cajal-Retzius cells, subplate cells, subpial granular layer cells, some interneurons and some glial cells. With the arrival of the cortical plate cells, the subplate cells descend to occupy the stratum below. Layer 1 cells are of diverse origin as some of them are generated in the ventricular zone of the cortical neuroepithelium, whereas other cell populations come from extracortical regions such as the olfactory placode or the ganglionic eminences of the basal telencephalon. The predominant cell type in the marginal zone is the Cajal-Retzius cell, which expresses reelin and calretinin, and is probably generated in the cortical neuroepithelium. These cells can be readily distinguished from cells that come from the ganglionic eminences as these later populations mainly express GABA and calbindin. Finally, our results suggest that the cells of the subpial granular layer might be generated in the rostral pole of the lateral ganglionic eminences.

The discovery of the subpial granular layer in the human cerebral cortex

“…However, it should be noted that Ranke clearly stated that he observed the SGL in fetal brains of other mammals (sheep, cow, dog and cat), which was subsequently confirmed by Friedrich Sanides and Emilia Sas at least for the paleocortex of various mammals [14]. The SGL is also well developed in the fetal monkey cerebral cortex [15], and it has recently been described even in the developing cortex of rodents [16,17].…”

Massive loss of Cajal-Retzius cells does not disrupt neocortical layer order

“…The MZ contains a variety of cell types (Jimenez et al, 2003). However, CR cells are distinguished by their expression of reelin, calretinin and glutamate (Alcantara et al, 1998;del Rio et al, 1995;Ogawa et al, 1995;Soda et al, 2003).…”

Early history of subplate and interstitial neurons: from Theodor Meynert (1867) to the discovery of the subplate zone (1974)

“…These findings clearly show that an initial description of the subplate as layer VIb in the fetal cat (Marin-Padilla, 1971, 1972, 1978 was overly simplified and that it at best can only be applied to the first (earliest generated) wave of subplate neurons. For a detailed criticism of this original concept of the primordial plexiform layer (or preplate) see a recent review (Bystron et al 2008) as well as a number of recent studies which pointed out a previously unsuspected complexity of the early neocortical anlage in humans (Zecevic et al 1999;Meyer et al 2000;Zecevic & Rakic, 2001;Rakic & Zecevic, 2003;Bystron et al 2005Bystron et al , 2006 as well as in rodents (Rickmann et al 1977;Hevner et al 2003;Jimé nez et al 2003;Bielle et al 2005;García-Moreno et al 2007). …”