The Origin of Neocortex: Lessons from Comparative Embryology

The mammalian neocortex is the great achievement of cortical development and evolution. Its basic structure and parameters are remarkably uniform. With the exception of the primate primary visual cortex, all cortical areas in all mammals have a six-layered dorsal cortex with similar cell numbers within a unit column. This constant feature of the cortex is surprising considering the differences in the elaboration and proportions of infragranular and supragranular cell layers between species and between cortical areas. In contrast with mammals, avian and reptilian dorsal cortex contains only a fraction of the cell types found in mammals, mostly corresponding to infragranular layers (subplate, layers 5 and 6). We shall speculate on the possible evolutionary changes in the mammalian developmental program that may have delivered the additional neural complexity of the cerebral cortex. In this article we compare recent data on cell proliferation patterns, modes of radial and tangential neuronal migration, and construction sequence of the cortical plate in various species (turtle, chick, mouse, rat, macaque, and human). Work in macaque and mouse revealed that the infragranular (lower) and supragranular (upper) cell layers are produced in different mitotic compartments. The infragranular cells mostly originate from divisions of radial glia in the ventricular zone (VZ), while the supragranular cells are derived from symmetrical divisions of intermediate progenitor cells in the subventricular zone (SVZ). Comparisons of the germinal zones at different stages of cortical neurogenesis in macaque and mouse also revealed that macaque has a larger SVZ germinal area, which is correlated to the more elaborate supragranular layers. In chick and turtle, where the neuronal equivalents to the supragranular layers are absent, there is no defined SVZ in their dorsal cortex. This suggests that the SVZ in dorsal cortex is a specific mammalian trait. The elaboration of the dorsal cortical mitotic compartments with distinct gene expression patterns producing different classes of cortical neurons might have been a major driving force behind the increasing complexity of the mammalian cortex.