Lengthening Neurogenic Period during Neocortical Development Causes a Hallmark of Neocortex Expansion.
A hallmark of the evolutionary expansion of the neocortex is a specific increase in the number of neurons generated for the upper neocortical layers during development. The cause underlying this increase is unknown. Here, we show that lengthening the neurogenic period during neocortical development is sufficient to specifically increase upper-layer neuron generation. Thus, embryos of mouse strains with longer gestation exhibited a longer neurogenic period and generated more upper-layer, but not more deep-layer, neurons than embryos with shorter gestation. Accordingly, long-gestation embryos showed a greater abundance of neurogenic progenitors in the subventricular zone than short-gestation embryos at late stages of cortical neurogenesis. Analysis of a mouse-rat chimeric embryo, developing inside a rat mother, pointed to factors in the rat environment that influenced the upper-layer neuron generation by the mouse progenitors. Exploring a potential maternal source of such factors, short-gestation strain mouse embryos transferred to long-gestation strain mothers exhibited an increase in the length of the neurogenic period and upper-layer neuron generation. The opposite was the case for long-gestation strain mouse embryos transferred to short-gestation strain mothers, indicating a dominant maternal influence on the length of the neurogenic period and hence upper-layer neuron generation. In summary, our study uncovers a hitherto unknown link between embryonic cortical neurogenesis and the maternal gestational environment and provides experimental evidence that lengthening the neurogenic period during neocortical development underlies a key aspect of neocortical expansion.
['Stepien|Barbara K|BK|', 'Naumann|Ronald|R|', 'Holtz|Anja|A|', 'Helppi|Jussi|J|', 'Huttner|Wieland B|WB|', 'Vaid|Samir|S|']
D000818:Animals D000831:Animals, Newborn D005075:Biological Evolution D002460:Cell Line D049109:Cell Proliferation D004624:Embryo Transfer D004622:Embryo, Mammalian D047108:Embryonic Development D005260:Female D008297:Male D051379:Mice D019579:Neocortex D058953:Neural Stem Cells D055495:Neurogenesis D009474:Neurons D011247:Pregnancy D051381:Rats D013997:Time Factors D018183:Transplantation Chimera
neurogenic period upper-layer neurons gestation maternal regulation