Modulation of Neocortical Development by Early Neuronal Activity: Physiology and Pathophysiology

Animal and human studies revealed that patterned neuronal activity is an inherent feature of developing nervous systems. This review summarizes our current knowledge about the mechanisms generating early electrical activity patterns and their impact on structural and functional development of the ce...

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Main Authors: Sergei Kirischuk, Anne Sinning, Oriane Blanquie, Jenq-Wei Yang, Heiko J. Luhmann, Werner Kilb
Format: Article
Language:English
Published: Frontiers Media S.A. 2017-11-01
Series:Frontiers in Cellular Neuroscience
Subjects:
Online Access:http://journal.frontiersin.org/article/10.3389/fncel.2017.00379/full
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author Sergei Kirischuk
Anne Sinning
Oriane Blanquie
Jenq-Wei Yang
Heiko J. Luhmann
Werner Kilb
author_facet Sergei Kirischuk
Anne Sinning
Oriane Blanquie
Jenq-Wei Yang
Heiko J. Luhmann
Werner Kilb
author_sort Sergei Kirischuk
collection DOAJ
description Animal and human studies revealed that patterned neuronal activity is an inherent feature of developing nervous systems. This review summarizes our current knowledge about the mechanisms generating early electrical activity patterns and their impact on structural and functional development of the cerebral cortex. All neocortical areas display distinct spontaneous and sensory-driven neuronal activity patterns already at early phases of development. At embryonic stages, intermittent spontaneous activity is synchronized within small neuronal networks, becoming more complex with further development. This transition is accompanied by a gradual shift from electrical to chemical synaptic transmission, with a particular role of non-synaptic tonic currents before the onset of phasic synaptic activity. In this review article we first describe functional impacts of classical neurotransmitters (GABA, glutamate) and modulatory systems (e.g., acetylcholine, ACh) on early neuronal activities in the neocortex with special emphasis on electrical synapses, nonsynaptic and synaptic currents. Early neuronal activity influences probably all developmental processes and is crucial for the proper formation of neuronal circuits. In the second part of our review, we illustrate how specific activity patterns might interfere with distinct neurodevelopmental processes like proliferation, migration, axonal and dendritic sprouting, synapse formation and neurotransmitter specification. Finally, we present evidence that transient alterations in neuronal activity during restricted perinatal periods can lead to persistent changes in functional connectivity and therefore might underlie the manifestation of neurological and neuropsychiatric diseases.
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spelling doaj.art-a19cc43f860c4eecb44bf6b78fe004492022-12-21T18:12:13ZengFrontiers Media S.A.Frontiers in Cellular Neuroscience1662-51022017-11-011110.3389/fncel.2017.00379305458Modulation of Neocortical Development by Early Neuronal Activity: Physiology and PathophysiologySergei Kirischuk0Anne Sinning1Oriane Blanquie2Jenq-Wei Yang3Heiko J. Luhmann4Werner Kilb5nstitute of Physiology, University Medical Center of the Johannes Gutenberg University Mainz, Mainz, Germanynstitute of Physiology, University Medical Center of the Johannes Gutenberg University Mainz, Mainz, Germanynstitute of Physiology, University Medical Center of the Johannes Gutenberg University Mainz, Mainz, Germanynstitute of Physiology, University Medical Center of the Johannes Gutenberg University Mainz, Mainz, Germanynstitute of Physiology, University Medical Center of the Johannes Gutenberg University Mainz, Mainz, Germanynstitute of Physiology, University Medical Center of the Johannes Gutenberg University Mainz, Mainz, GermanyAnimal and human studies revealed that patterned neuronal activity is an inherent feature of developing nervous systems. This review summarizes our current knowledge about the mechanisms generating early electrical activity patterns and their impact on structural and functional development of the cerebral cortex. All neocortical areas display distinct spontaneous and sensory-driven neuronal activity patterns already at early phases of development. At embryonic stages, intermittent spontaneous activity is synchronized within small neuronal networks, becoming more complex with further development. This transition is accompanied by a gradual shift from electrical to chemical synaptic transmission, with a particular role of non-synaptic tonic currents before the onset of phasic synaptic activity. In this review article we first describe functional impacts of classical neurotransmitters (GABA, glutamate) and modulatory systems (e.g., acetylcholine, ACh) on early neuronal activities in the neocortex with special emphasis on electrical synapses, nonsynaptic and synaptic currents. Early neuronal activity influences probably all developmental processes and is crucial for the proper formation of neuronal circuits. In the second part of our review, we illustrate how specific activity patterns might interfere with distinct neurodevelopmental processes like proliferation, migration, axonal and dendritic sprouting, synapse formation and neurotransmitter specification. Finally, we present evidence that transient alterations in neuronal activity during restricted perinatal periods can lead to persistent changes in functional connectivity and therefore might underlie the manifestation of neurological and neuropsychiatric diseases.http://journal.frontiersin.org/article/10.3389/fncel.2017.00379/fulldevelopmentcerebral cortexsubplatespontaneous activitysomatosensory cortexrodent
spellingShingle Sergei Kirischuk
Anne Sinning
Oriane Blanquie
Jenq-Wei Yang
Heiko J. Luhmann
Werner Kilb
Modulation of Neocortical Development by Early Neuronal Activity: Physiology and Pathophysiology
Frontiers in Cellular Neuroscience
development
cerebral cortex
subplate
spontaneous activity
somatosensory cortex
rodent
title Modulation of Neocortical Development by Early Neuronal Activity: Physiology and Pathophysiology
title_full Modulation of Neocortical Development by Early Neuronal Activity: Physiology and Pathophysiology
title_fullStr Modulation of Neocortical Development by Early Neuronal Activity: Physiology and Pathophysiology
title_full_unstemmed Modulation of Neocortical Development by Early Neuronal Activity: Physiology and Pathophysiology
title_short Modulation of Neocortical Development by Early Neuronal Activity: Physiology and Pathophysiology
title_sort modulation of neocortical development by early neuronal activity physiology and pathophysiology
topic development
cerebral cortex
subplate
spontaneous activity
somatosensory cortex
rodent
url http://journal.frontiersin.org/article/10.3389/fncel.2017.00379/full
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AT annesinning modulationofneocorticaldevelopmentbyearlyneuronalactivityphysiologyandpathophysiology
AT orianeblanquie modulationofneocorticaldevelopmentbyearlyneuronalactivityphysiologyandpathophysiology
AT jenqweiyang modulationofneocorticaldevelopmentbyearlyneuronalactivityphysiologyandpathophysiology
AT heikojluhmann modulationofneocorticaldevelopmentbyearlyneuronalactivityphysiologyandpathophysiology
AT wernerkilb modulationofneocorticaldevelopmentbyearlyneuronalactivityphysiologyandpathophysiology