New theories on the origin of cerebral cortical convolutions

Since evolution is the evolution of embryonic forms, the study of embryonic development is currently the most powerful tool for biologists to understand the evolutionary process. When addressing the question of the origins of the human brain, scientists stumble over the frustrating lack of similarities between the surfaces of brains among mammalian and other vertebrate species. All living mammals present a six layered neocortex, whereas no homologous structure is found in any other vertebrate species. The human neocortex would appear to be the greatest achievement during our evolutionary history and the origins of its intrinsic features, such as its huge size and dense convolution (showing complicated gyri and sulci), must be studied among the deepest roots of the mammalian lineage.

HFSP Long-Term Fellow Fernando Garcia-Moreno and colleagues
authored on Tue, 28 February 2012

The surface of the cerebral cortex, just like that of nuts, can vary substantially. Some nuts and brains have a smooth surface, others have a few folds, while some have much more prominent convolutions.  Understanding cortical folding patterns has very general clinical implications since numerous developmental disorders are associated with changes in brain folding, for example, intractable epilepsy and learning disabilities.  Folding ("gyrencephaly") is present in primates and rodents but examples of smooth surfaced brains ("lissencephaly") can also be found.  

 

 Figure: Representation of folds in the brain

 

The origin of the cerebral cortical convolutions has been linked to the increase of a particular subtype of progenitor cells (intermediate outer radial glia (oRG) - or outer subventricular zone (oSVZ) radial progenitors).  These oSVZ radial progenitors have been found in much larger numbers in developing human and ferret cortex than in the mouse cortex, which is smooth.  In order to address the developmental origins of the enlargement of the neocortical surface and the appearance of neocortical gyri, we selected two key mammalian species: a near-lissencephalic primate, the common marmoset (Callithrix jacchus), and a near-gyrencephalic rodent, the agouti (Dasyprocta agouti).  Our recent study published in the journal Cerebral Cortex examined the proportions of various progenitors and demonstrated that the oSVZ radial progenitors are abundant and proliferate in inner as well as oSVZ in both species.  Our data shows evidence that the appearance of convoluted or large brains is not related to this secondary mitotic domain. Both agouti and marmoset presented a thick well-organized oSVZ, cytoarchitectonically distinct from the rest of the subventricular zone as shown through a study of specific mitotic markers and transcription factors associated to the oSVZ. We also provide evidence that oRGs didn’t only populate the oSVZ, but other subdivisions of the SVZ as well.  Differential regulation of oSVZ radial and other progenitor types may enhance the adaptability and diversity of cortical morphogenesis.

Together all these new data suggest that cytoarchitectonic subdivisions of SVZ are an evolutionary trend and not a primate- or a gyrencephalic brain-specific feature. Our study warns that it is premature to generalize based on the comparative analysis of only a handful of species.  The study of the proliferative domains in several mammalian species reveals a surprisingly similar developmental process that was initially believed to be primate-specific, subsequently alleged to be associated with brain folding. We need to examine more models to fully understand how the mammalian neocortex evolved and how primate neocortex bloomed to make us human. Comparative evolutionary developmental biology excluded some possibilities for the explanation of brain folding, but is hasn’t been able to give us the answer, so far.

Reference

(1) Compartmentalization of cerebral cortical germinal zones in a lissencephalic primate and gyrencephalic rodent. García-Moreno F, Vasistha NA, Trevia N, Bourne JA, Molnár Z.Cereb Cortex. 2012 Feb;22(2):482-92.

Other References

(2) The (not necessarily) convoluted role of basal radial glia in cortical neurogenesis.Hevner RF, Haydar TF.Cereb Cortex. 2012 Feb;22(2):465-8.

(3) Abundant occurrence of basal radial glia in the subventricular zone of embryonic neocortex of a lissencephalic primate, the common marmoset Callithrix jacchus. Kelava I, Reillo I, Murayama AY, Kalinka AT, Stenzel D, Tomancak P, Matsuzaki F, Lebrand C, Sasaki E, Schwamborn JC, Okano H, Huttner WB, Borrell V. Cereb Cortex. 2012 Feb;22(2):469-81.

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Pubmed link ref (2)

Pubmed link (3)