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This paper proposes an evolutionary hypothesis for the origin of (i) the inside-out pattern of mammalian corticogenesis in which late-generated cells become located more superficially than early-generated cells, and (ii) the predominantly radial organization of isocortical inputs in mammals. It is suggested that an outside-in neurogenetic gradient (in which early-generated cells are located more superficially than late-generated cells), as occurs in reptilian cortex, would have positioned the late-produced, associative neurons (destined to supragranular layers in modern isocortex) below the early-produced output neurons. This may have limited the possibilities of synaptic contacts between the younger cells and the afferent terminals which were located in the more superficial layer I. There was probably an adaptive benefit in those individuals in which late-produced cells were capable of passing through the layers of already migrated cells, thus making contacts with superficial afferents and generating corticocortical and local circuits that processed the information before producing an output. Reelin, an extracellular glycoprotein found in layer I, and a cyclin-dependent kinase (cdk5) and its neuronal-specific activator (p35) may have played key roles in the generation of the inside-out gradient. Additionally, by serving as a waiting compartment for thalamic axons while the cortical plate develops, the subplate zone may have participated in the change from an emphasis in a tangential arrangement of thalamic terminals that is characteristic of reptilian cortex to the predominantly radial mode of termination that is observed in mammalian isocortex.

Feature Article: Evolution of Isocortical Organization. A Tentative Scenario Including Roles of Reelin, p35/cdk5 and the Subplate Zone