Variations of telencephalic development that paved the way for neocortical evolution

Charles Darwin stated, “community in embryonic structure reveals community of descent”. Thus, to understand how the neocortex emerged during mammalian evolution we need to understand the evolution of the development of the pallium, the source of the neocortex. In this article, we review the variations in the development of the pallium that enabled the production of the six-layered neocortex. We propose that an accumulation of subtle modifications from very early brain development accounted for the diversification of vertebrate pallia and the origin of the neocortex. Initially, faint differences of expression of secretable morphogens promote a wide variety in the proportions and organization of sectors of the early pallium in different vertebrates. It prompted different sectors to host varied progenitors and distinct germinative zones. These cells and germinative compartments generate diverse neuronal populations that migrate and mix with each other through radial and tangential migrations in a taxon-specific fashion. Together, these early variations had a profound influence on neurogenetic gradients, lamination, positioning, and connectivity. Gene expression, hodology, and physiological properties of pallial neurons are important features to suggest homologies, but the origin of cells and their developmental trajectory are fundamental to understand evolutionary changes. Our review compares the development of the homologous pallial sectors in sauropsids and mammals, with a particular focus on cell lineage, in search of the key changes that led to the appearance of the mammalian neocortex.