The evolutionary origin of the mammalian isocortex: towards an integrated developmental and functional approach.

The isocortex is a distinctive feature of mammalian brains, which has no clear counterpart in the cerebral hemispheres of other amniotes. This paper speculates on the evolutionary processes giving rise to the isocortex. As a first step, we intend to identify what structure may be ancestral to the isocortex in the reptilian brain. Then, it is necessary to account for the transformations (developmental, connectional, and functional) of this ancestral structure, which resulted in the origin of the isocortex. One long-held perspective argues that part of the isocortex derives from the ventral pallium of reptiles, whereas another view proposes that the isocortex originated mostly from the dorsal pallium. We consider that, at this point, evidence tends to favor correspondence of the isocortex with the dorsal cortex of reptiles. In any case, the isocortex may have originated partly as a consequence of an overall "dorsalizing" effect (that is, an expansion of the territories expressing dorsal-specific genes) during pallial development. Furthermore, expansion of the dorsal pallium may have been driven by selective pressures favoring the development of associative networks between the dorsal cortex, the olfactory cortex, and the hippocampus, which participated in spatial or episodic memory in the early mammals. In this context, sensory projections that in reptiles end in the ventral pallium, are observed to terminate in the isocortex (dorsal pallium) of mammals, perhaps owing to their participation in these associative networks.

Evolutionary divergence of the reptilian and the mammalian brains: considerations on connectivity and development.

The isocortex is a distinctive feature of the mammalian brain, with no clear counterpart in other amniotes. There have been long controversies regarding possible homologues of this structure in reptiles and birds. The brains of the latter are characterized by the presence of a structure termed dorsal ventricular ridge (DVR), which receives ascending auditory and visual projections, and has been postulated to be homologous to parts of the mammalian isocortex (i.e., the auditory and the extrastriate visual cortices). Dissenting views, now supported by molecular evidence, claim that the DVR originates from a region termed ventral pallium, while the isocortex may arise mostly from the dorsal pallium (in mammals, the ventral pallium relates to the claustroamygdaloid complex). Although it is possible that in mammals the embryonic ventral pallium contributes cells to the developing isocortex, there is no evidence yet supporting this alternative. The possibility is raised that the expansion of the cerebral cortex in the origin of mammals was product of a generalized dorsalizing influence in pallial development, at the expense of growth in ventral pallial regions. Importantly, the evidence suggests that organization of sensory projections is significantly different between mammals and sauropsids. In reptiles and birds, some sensory pathways project to the ventral pallium and others project to the dorsal pallium, while in mammals sensory projections end mainly in the dorsal pallium. We suggest a scenario for the origin of the mammalian isocortex which relies on the development of associative circuits between the olfactory, the dorsal and the hippocampal cortices in the earliest mammals.