Electrical activity controls area-specific expression of neuronal apoptosis in the developing mouse cerebral cortex

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Abstract

Programmed cell death widely but heterogeneously affects the developing brain, causing the loss of up to 50% of neurons in rodents. However, whether this heterogeneity originates from neuronal identity and/or network-dependent processes is unknown. Here, we report that the primary motor cortex (M1) and primary somatosensory cortex (S1), two adjacent but functionally distinct areas, display striking differences in density of apoptotic neurons during the early postnatal period. These differences in rate of apoptosis negatively correlate with region-dependent levels of activity. Disrupting this activity either pharmacologically or by electrical stimulation alters the spatial pattern of apoptosis and sensory deprivation leads to exacerbated amounts of apoptotic neurons in the corresponding functional area of the neocortex. Thus, our data demonstrate that spontaneous and periphery-driven activity patterns are important for the structural and functional maturation of the neocortex by refining the final number of cortical neurons in a region-dependent manner.

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Oriane Blanquie

Institute of Physiology, University Medical Center of the Johannes Gutenberg University Mainz, Mainz, Germany

Competing interests
The authors declare that no competing interests exist.
Jenq-Wei Yang

Institute of Physiology, University Medical Center of the Johannes Gutenberg University Mainz, Mainz, Germany

For correspondence
yangj@uni-mainz.de

Competing interests
The authors declare that no competing interests exist.
Werner Kilb

Institute of Physiology, University Medical Center of the Johannes Gutenberg University Mainz, Mainz, Germany

For correspondence
wkilb@uni-mainz.de

Competing interests
The authors declare that no competing interests exist.
Salim Sharopov

Institute of Physiology, University Medical Center of the Johannes Gutenberg University Mainz, Mainz, Germany

For correspondence
shsalim@mail.ru

Competing interests
The authors declare that no competing interests exist.
Anne Sinning

Institute of Physiology, University Medical Center of the Johannes Gutenberg University Mainz, Mainz, Germany

For correspondence
asinning@uni-mainz.de

Competing interests
The authors declare that no competing interests exist.
Heiko J Luhmann

Institute of Physiology, University Medical Center of the Johannes Gutenberg University Mainz, Mainz, Germany

For correspondence
luhmann@uni-mainz.de

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-7934-8661

Funding

German Research Foundation (Collaborative Research Center 1080)

Anne Sinning
Heiko J Luhmann

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: All experiments were conducted in accordance with National and European (86/609/EEC) laws for the use of animals in research and were approved by the local ethical committee (Landesuntersuchungsamt Rheinland-Pfalz 23.177-07/G 10-1-010).

Copyright

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.