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WIREs Dev Biol
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Neural progenitor cells and their role in the development and evolutionary expansion of the neocortex

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The evolutionary expansion of the mammalian brain, notably the neocortex, provides a platform for the higher cognitive abilities that characterize humans. Cortical expansion is accompanied by increased folding of the pial surface, which gives rise to a gyrencephalic (folded) rather than lissencephalic (unfolded) neocortex. This expansion reflects the prolonged and increased proliferation of neural stem and progenitor cells (NPCs). Distinct classes of NPCs can be distinguished based on either cell biological criteria (apical progenitors [APs], basal progenitors [BPs]) or lineage (primary progenitors and secondary progenitors). Cortical expansion in development and evolution is linked to an increased abundance and proliferative capacity of BPs, notably basal radial glial cells, a recently characterized type of secondary progenitor derived from apical radial glial cells, the primary progenitors. To gain insight into the molecular basis underlying the prolonged and increased proliferation of NPCs and in particular BPs, comparative genomic and transcriptomic approaches, mostly for human versus mouse, have been employed and applied to specific NPC types and subpopulations. These have revealed two principal sets of molecular changes. One concerns differences in the expression of common genes between species with different degrees of cortical expansion. The other comprises human‐specific genes or genomic regulatory sequences. Various systems that allow functional testing of these genomic and gene expression differences between species have emerged, including transient and stable transgenesis, genome editing, cerebral organoids, and organotypic slice cultures. These provide future avenues for uncovering the molecular basis of cortical expansion. WIREs Dev Biol 2017, 6:e256. doi: 10.1002/wdev.256 This article is categorized under: Nervous System Development > Vertebrates: Regional Development Comparative Development and Evolution > Organ System Comparisons Between Species Comparative Development and Evolution > Evolutionary Novelties
Principal zones and progenitor cell types of developing neocortex. (a) Neuroepithelial cells (red). Arrows indicate the nuclear migration during the cell cycle. (b) Cell types after the onset of neurogenesis. Primary progenitor cells (apical radial glial cell, aRGC), secondary progenitor cells (apical intermediate progenitor, aIP; basal radial glial cells, bRGs; neurogenic and proliferative basal intermediate progenitor cells, nbIP and pbIP) and postmitotic neurons are indicated in red, green and blue, respectively. (c) Major lineages from primary progenitor cells via secondary progenitor cells to neurons (see (b)) in a lissencephalic rodent. Orange band indicates the SVZ. (d) Major lineages from primary progenitor cells via secondary progenitor cells to neurons (see b) in a gyrencephalic primate. Orange bands indicate the oSVZ and iSVZ. SP, subplate.
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Lissencephalic mouse and gyrencephalic human neocortex. Cartoons of mouse (left) and human (right) brain (top) and of a coronal section (bottom). Blue area indicates the gray matter.
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ARHGAP11B. Cartoon showing key differences between ARHGAP11A and ARHGAP11B. ARHGAP11A contains a complete RhoGAP domain (magenta) and exhibits RhoGAP activity toward RhoA. In contrast, ARHGAP11B, due to a frame shift‐causing mutation, lacks the C‐terminal 26 amino acids of the RhoGAP domain, does not exhibit RhoA‐GAP activity, and contains a unique, human‐specific 47 amino acid‐sequence (green) following residue 220.
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Selected examples of canonical neural progenitor cell lineages to neurons in developing neocortex. Left: direct neurogenesis by asymmetric division of an aRGC. Middle and right: indirect neurogenesis. Middle: in a lissencephalic rodent, an aRGC undergoes asymmetric division to yield an nbIP, which undergoes symmetric consumptive division to yield two neurons (N). Right: in a gyrencephalic primate, an aRGC undergoes asymmetric division to yield a bRGC or pbIP, which undergoes symmetric proliferative division to yield two BPs, bRGCs or bIPs. These then undergo either asymmetric or symmetric division to yield neurons.
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Classification of neural progenitor cells in the developing neocortex (For details, see text).
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Nervous System Development > Vertebrates: Regional Development