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

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)...

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Main Authors: Oriane Blanquie, Jenq-Wei Yang, Werner Kilb, Salim Sharopov, Anne Sinning, Heiko J Luhmann
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2017-08-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/27696
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spelling doaj-bc08d7aedd0e4d3484a7178db1e8cddf2021-05-05T13:42:17ZengeLife Sciences Publications LtdeLife2050-084X2017-08-01610.7554/eLife.27696Electrical activity controls area-specific expression of neuronal apoptosis in the mouse developing cerebral cortexOriane Blanquie0https://orcid.org/0000-0003-2361-7129Jenq-Wei Yang1Werner Kilb2Salim Sharopov3Anne Sinning4https://orcid.org/0000-0002-1518-7272Heiko J Luhmann5https://orcid.org/0000-0002-7934-8661Institute of Physiology, University Medical Center of the Johannes Gutenberg University Mainz, Mainz, GermanyInstitute of Physiology, University Medical Center of the Johannes Gutenberg University Mainz, Mainz, GermanyInstitute of Physiology, University Medical Center of the Johannes Gutenberg University Mainz, Mainz, GermanyInstitute of Physiology, University Medical Center of the Johannes Gutenberg University Mainz, Mainz, GermanyInstitute of Physiology, University Medical Center of the Johannes Gutenberg University Mainz, Mainz, GermanyInstitute of Physiology, University Medical Center of the Johannes Gutenberg University Mainz, Mainz, GermanyProgrammed 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.https://elifesciences.org/articles/27696cerebral cortexactivity patternsapoptosiscell deathdevelopmentwhisker deafferentation
collection DOAJ
language English
format Article
sources DOAJ
author Oriane Blanquie
Jenq-Wei Yang
Werner Kilb
Salim Sharopov
Anne Sinning
Heiko J Luhmann
spellingShingle Oriane Blanquie
Jenq-Wei Yang
Werner Kilb
Salim Sharopov
Anne Sinning
Heiko J Luhmann
Electrical activity controls area-specific expression of neuronal apoptosis in the mouse developing cerebral cortex
eLife
cerebral cortex
activity patterns
apoptosis
cell death
development
whisker deafferentation
author_facet Oriane Blanquie
Jenq-Wei Yang
Werner Kilb
Salim Sharopov
Anne Sinning
Heiko J Luhmann
author_sort Oriane Blanquie
title Electrical activity controls area-specific expression of neuronal apoptosis in the mouse developing cerebral cortex
title_short Electrical activity controls area-specific expression of neuronal apoptosis in the mouse developing cerebral cortex
title_full Electrical activity controls area-specific expression of neuronal apoptosis in the mouse developing cerebral cortex
title_fullStr Electrical activity controls area-specific expression of neuronal apoptosis in the mouse developing cerebral cortex
title_full_unstemmed Electrical activity controls area-specific expression of neuronal apoptosis in the mouse developing cerebral cortex
title_sort electrical activity controls area-specific expression of neuronal apoptosis in the mouse developing cerebral cortex
publisher eLife Sciences Publications Ltd
series eLife
issn 2050-084X
publishDate 2017-08-01
description 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.
topic cerebral cortex
activity patterns
apoptosis
cell death
development
whisker deafferentation
url https://elifesciences.org/articles/27696
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AT jenqweiyang electricalactivitycontrolsareaspecificexpressionofneuronalapoptosisinthemousedevelopingcerebralcortex
AT wernerkilb electricalactivitycontrolsareaspecificexpressionofneuronalapoptosisinthemousedevelopingcerebralcortex
AT salimsharopov electricalactivitycontrolsareaspecificexpressionofneuronalapoptosisinthemousedevelopingcerebralcortex
AT annesinning electricalactivitycontrolsareaspecificexpressionofneuronalapoptosisinthemousedevelopingcerebralcortex
AT heikojluhmann electricalactivitycontrolsareaspecificexpressionofneuronalapoptosisinthemousedevelopingcerebralcortex
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