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

  1. Oriane Blanquie
  2. Jenq-Wei Yang  Is a corresponding author
  3. Werner Kilb  Is a corresponding author
  4. Salim Sharopov  Is a corresponding author
  5. Anne Sinning  Is a corresponding author
  6. Heiko J Luhmann  Is a corresponding author
  1. University Medical Center of the Johannes Gutenberg University Mainz, Germany

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.

Article and author information

Author details

  1. 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.
  2. 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.
  3. 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.
  4. 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.
  5. 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.
  6. 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.
    ORCID icon "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).

Reviewing Editor

  1. John Huguenard, Stanford University School of Medicine, United States

Publication history

  1. Received: April 11, 2017
  2. Accepted: August 18, 2017
  3. Accepted Manuscript published: August 21, 2017 (version 1)
  4. Version of Record published: September 4, 2017 (version 2)

Copyright

© 2017, Blanquie et al.

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.

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  1. Oriane Blanquie
  2. Jenq-Wei Yang
  3. Werner Kilb
  4. Salim Sharopov
  5. Anne Sinning
  6. Heiko J Luhmann
(2017)
Electrical activity controls area-specific expression of neuronal apoptosis in the developing mouse cerebral cortex
eLife 6:e27696.
https://doi.org/10.7554/eLife.27696

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