Abstract
The human neocortex is undoubtedly considered a supreme accomplishment in mammalian evolution. It features a prenatally established six-layered structure which remains plastic to the myriad of changes throughout an organism’s lifetime. A fundamental feature of neocortical evolution and development is the abundance and diversity of the progenitor cell population and their neuronal and glial progeny. These evolutionary upgrades are partially enabled due to the progenitors’ higher proliferative capacity, compartmentalization of proliferative regions, and specification of neuronal temporal identities. The driving force of these processes may be explained by temporal molecular patterning, by which progenitors have intrinsic capacity to change their competence as neocortical neurogenesis proceeds. Thus, neurogenesis can be conceptualized along two timescales of progenitors’ capacity to (1) self-renew or differentiate into basal progenitors (BPs) or neurons or (2) specify their fate into distinct neuronal and glial subtypes which participate in the formation of six-layers. Neocortical development then proceeds through sequential phases of proliferation, differentiation, neuronal migration, and maturation. Temporal molecular patterning, therefore, relies on the precise regulation of spatiotemporal gene expression. An extensive transcriptional regulatory network is accompanied by post-transcriptional regulation that is frequently mediated by the regulatory interplay between RNA-binding proteins (RBPs). RBPs exhibit important roles in every step of mRNA life cycle in any system, from splicing, polyadenylation, editing, transport, stability, localization, to translation (protein synthesis). Here, we underscore the importance of RBP functions at multiple time-restricted steps of early neurogenesis, starting from the cell fate transition of transcriptionally primed cortical progenitors. A particular emphasis will be placed on RBPs with mostly conserved but also divergent evolutionary functions in neural progenitors across different species. RBPs, when considered in the context of the fascinating process of neocortical development, deserve to be main protagonists in the story of the evolution and development of the neocortex.
Highlights
One of the greatest innovations during the evolution of the mammalian brain is the cerebral cortex, which has arisen from the selective expansion of the dorsal telencephalon in the rostral part of the forebrain (Rakic, 2009) and manifests area-specific lamination patterns (Cadwell et al, 2019)
Insulinomaassociated protein 1 (Insm1) and Elavl4 have opposite protein expression patterns early in mouse and human neocortical development: Insm1 is highly expressed in basal progenitors (BPs)-genic apical radial glia (aRG) and newly generated BP, but becomes downregulated in newborn neurons (Farkas et al, 2008), whereas Elavl4 is mostly present in the cortical plate (CP) and is absent from the ventricular zone (VZ)
The progression of cortical neurogenesis can be succinctly understood via the concept of progenitor temporal patterning (Bayraktar and Doe, 2013)
Summary
One of the greatest innovations during the evolution of the mammalian brain is the cerebral cortex, which has arisen from the selective expansion of the dorsal telencephalon in the rostral part of the forebrain (Rakic, 2009) and manifests area-specific lamination patterns (Cadwell et al, 2019). Another single-cell sequencing study showed that Elavl4 mRNA levels are upregulated in human intermediate progenitors that have a high capacity to differentiate into early neurons during neurogenesis (Pollen et al, 2015).
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