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Lengthening Neurogenic Period During Neocortical Development Causes a Hallmark of Neocortex Expansion

45 Pages Posted: 9 Apr 2020 Publication Status: Review Complete

See all articles by Barbara Krystyna Stepien

Barbara Krystyna Stepien

Max Planck Institute of Molecular Cell Biology and Genetics (MPI-CBG)

Ronald Naumann

Max Planck Institute of Molecular Cell Biology and Genetics (MPI-CBG)

Anja Holtz

Max Planck Institute of Molecular Cell Biology and Genetics (MPI-CBG)

Jussi Helppi

Max Planck Institute of Molecular Cell Biology and Genetics (MPI-CBG)

Wieland B. Huttner

Max Planck Institute of Molecular Cell Biology and Genetics (MPI-CBG)

Samir Vaid

Max Planck Institute of Molecular Cell Biology and Genetics (MPI-CBG)

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Abstract

A hallmark of the evolutionary expansion of the neocortex, which is the seat of our higher cognitive abilities, 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 extrinsic factors influencing 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.

Keywords: neurogenic period, upper-layer neurons, gestation, maternal regulation

Suggested Citation

Stepien, Barbara Krystyna and Naumann, Ronald and Holtz, Anja and Helppi, Jussi and Huttner, Wieland B. and Vaid, Samir, Lengthening Neurogenic Period During Neocortical Development Causes a Hallmark of Neocortex Expansion. Available at SSRN: https://ssrn.com/abstract=3565014 or http://dx.doi.org/10.2139/ssrn.3565014
This is a paper under consideration at Cell Press and has not been peer-reviewed.

Barbara Krystyna Stepien

Max Planck Institute of Molecular Cell Biology and Genetics (MPI-CBG) ( email )

Pfotenhauerstr. 108
Dresden, 01307
Germany

Ronald Naumann

Max Planck Institute of Molecular Cell Biology and Genetics (MPI-CBG) ( email )

Pfotenhauerstr. 108
Dresden, 01307
Germany

Anja Holtz

Max Planck Institute of Molecular Cell Biology and Genetics (MPI-CBG)

Pfotenhauerstr. 108
Dresden, 01307
Germany

Jussi Helppi

Max Planck Institute of Molecular Cell Biology and Genetics (MPI-CBG) ( email )

Pfotenhauerstr. 108
Dresden, 01307
Germany

Wieland B. Huttner (Contact Author)

Max Planck Institute of Molecular Cell Biology and Genetics (MPI-CBG) ( email )

Pfotenhauerstr. 108
Dresden, 01307
Germany

Samir Vaid

Max Planck Institute of Molecular Cell Biology and Genetics (MPI-CBG) ( email )

Pfotenhauerstr. 108
Dresden, 01307
Germany

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