Pallio-pallial tangential migrations and growth signaling: new scenario for cortical evolution?

Abstract

Observations accruing in recent years imply that the areal patterning and size dimensioning of the mammalian neocortex are influenced by diverse sets of tangentially migrating glutamatergic neurons that invade the cortical plate and, in so doing, modify the properties of the neopallial proliferative compartments. This developmental scenario sheds new light upon the old issue of how the mammalian neocortex evolved its more complex structure from nonmammalian antecedent forms. In reviewing these novelties, I first point out the topological position of the neopallial island as a central component of the pallium in all gnathostomes, surrounded by a ring of prospective allocortical pallial regions and a more distant set of peripheral neighboring forebrain areas. Early patterning arises from the periphery via passive planar signaling. This process probably establishes the pallium field and its basic island plus allocortical ring organization, as well as a rough prepatterning of some regional subareas. Afterwards, patterning and modulated growth are also actively influenced by the convergence of separate streams of tangentially migrating subpial cells (partly peripheral and partly allocortical in origin) which collectively form the Cajal-Retzius neuronal population in layer I. Effects of these cells include the inside-out stratification of the cortical plate and they may also contribute to the evolutionary emergence of the 6-layered neocortical structure. The most recent addition to our knowledge of pallio-pallial migrations is the existence of a subsequent deep tangential migration of ventropallial cells into the neopallial primordium, whose signaling influence upon local progenitors magnifies the cortex population by 20%. These glutamatergic cells dispersedly invade the entire cortex but largely die postnatally. The crucial implications of these data for comparative thinking on mammalian neocortex evolution and interpretation of potential homologs in sauropsids are explored. Finally, a new conjecture regarding a possible role of the hitherto disregarded lateral pallium is advanced.