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Cell. 2018 Aug 23;174(5):1264-1276.e15. doi: 10.1016/j.cell.2018.06.036. Epub 2018 Jul 26.

Progenitor Hyperpolarization Regulates the Sequential Generation of Neuronal Subtypes in the Developing Neocortex.

Author information

1
Department of Basic Neurosciences, University of Geneva, 1 Rue Michel Servet, 1211 Geneva, Switzerland.
2
Department of Molecular Genetics and Microbiology, Duke University Medical Center, 224 Carl Building, Durham, NC 27710, USA.
3
Department of Basic Neurosciences, University of Geneva, 1 Rue Michel Servet, 1211 Geneva, Switzerland; Department of Neurology, Geneva University Hospital, 4 Rue Gabrielle-Perret-Gentil, 1205 Geneva, Switzerland. Electronic address: denis.jabaudon@unige.ch.

Abstract

During corticogenesis, ventricular zone progenitors sequentially generate distinct subtypes of neurons, accounting for the diversity of neocortical cells and the circuits they form. While activity-dependent processes are critical for the differentiation and circuit assembly of postmitotic neurons, how bioelectrical processes affect nonexcitable cells, such as progenitors, remains largely unknown. Here, we reveal that, in the developing mouse neocortex, ventricular zone progenitors become more hyperpolarized as they generate successive subtypes of neurons. Experimental in vivo hyperpolarization shifted the transcriptional programs and division modes of these progenitors to a later developmental status, with precocious generation of intermediate progenitors and a forward shift in the laminar, molecular, morphological, and circuit features of their neuronal progeny. These effects occurred through inhibition of the Wnt-beta-catenin signaling pathway by hyperpolarization. Thus, during corticogenesis, bioelectric membrane properties are permissive for specific molecular pathways to coordinate the temporal progression of progenitor developmental programs and thus neocortical neuron diversity.

KEYWORDS:

cortical development; membrane potential; neuronal diversity; progenitors

Comment in

PMID:
30057116
PMCID:
PMC6545245
DOI:
10.1016/j.cell.2018.06.036
[Indexed for MEDLINE]
Free PMC Article

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