A period of structural plasticity at the axon initial segment in developing visual cortex

Cortical networks are shaped by sensory experience and are most susceptible to modifications during critical periods characterized by enhanced plasticity at the structural and functional level. A system particularly well-studied in this context is the mammalian visual system. Plasticity has been doc...

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Main Authors: Annika eGutzmann, Nursah eErguel, Rebecca eGrossmann, Christian eSchultz, Petra eWahle, Maren eEngelhardt
Format: Article
Language:English
Published: Frontiers Media S.A. 2014-03-01
Series:Frontiers in Neuroanatomy
Subjects:
Online Access:http://journal.frontiersin.org/Journal/10.3389/fnana.2014.00011/full
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author Annika eGutzmann
Nursah eErguel
Nursah eErguel
Rebecca eGrossmann
Christian eSchultz
Christian eSchultz
Petra eWahle
Maren eEngelhardt
Maren eEngelhardt
author_facet Annika eGutzmann
Nursah eErguel
Nursah eErguel
Rebecca eGrossmann
Christian eSchultz
Christian eSchultz
Petra eWahle
Maren eEngelhardt
Maren eEngelhardt
author_sort Annika eGutzmann
collection DOAJ
description Cortical networks are shaped by sensory experience and are most susceptible to modifications during critical periods characterized by enhanced plasticity at the structural and functional level. A system particularly well-studied in this context is the mammalian visual system. Plasticity has been documented for the somatodendritic compartment of neurons in detail. A neuronal microdomain not yet studied in this context is the axon initial segment (AIS) located at the proximal axon segment. It is a specific electrogenic axonal domain and the site of action potential generation. Recent studies showed that structure and function of the AIS can be dynamically regulated. Here we hypothesize that the AIS shows a dynamic regulation during maturation of the visual cortex. We therefore analyzed AIS length development from embryonic day (E) 12.5 to adulthood in mice. A tri-phasic time course of AIS length remodeling during development was observed. AIS first appeared at E14.5 and increased in length throughout the postnatal period to a peak between postnatal day (P) 10 to P15 (eyes open P13-14). Then, AIS length was reduced significantly around the beginning of the critical period for ocular dominance plasticity (CP, P21). Shortest AIS were observed at the peak of the CP (P28), followed by a moderate elongation towards the end of the CP (P35). To test if the dynamic maturation of the AIS is influenced by eye opening (onset of activity), animals were deprived of visual input before and during the CP. Deprivation for 1 week prior to eye opening did not affect AIS length development. However, deprivation from P0-P28 and P14-P28 resulted in AIS length distribution similar to the peak at P15. In other words, deprivation from birth prevents the transient shortening of the AIS and maintains an immature AIS length. These results are the first to suggest a dynamic maturation of the AIS in cortical neurons and point to novel mechanisms in the development of neuronal excitability.
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spelling doaj.art-8aa02438ba85439bac67c0808290f7622022-12-21T20:19:21ZengFrontiers Media S.A.Frontiers in Neuroanatomy1662-51292014-03-01810.3389/fnana.2014.0001176969A period of structural plasticity at the axon initial segment in developing visual cortexAnnika eGutzmann0Nursah eErguel1Nursah eErguel2Rebecca eGrossmann3Christian eSchultz4Christian eSchultz5Petra eWahle6Maren eEngelhardt7Maren eEngelhardt8Heidelberg University, Medical Faculty Mannheim, CBTMHeidelberg University, Medical Faculty Mannheim, CBTMHeidelberg UniversityHeidelberg University, Medical Faculty Mannheim, CBTMHeidelberg University, Medical Faculty Mannheim, CBTMHeidelberg UniversityRuhr-University BochumHeidelberg University, Medical Faculty Mannheim, CBTMHeidelberg UniversityCortical networks are shaped by sensory experience and are most susceptible to modifications during critical periods characterized by enhanced plasticity at the structural and functional level. A system particularly well-studied in this context is the mammalian visual system. Plasticity has been documented for the somatodendritic compartment of neurons in detail. A neuronal microdomain not yet studied in this context is the axon initial segment (AIS) located at the proximal axon segment. It is a specific electrogenic axonal domain and the site of action potential generation. Recent studies showed that structure and function of the AIS can be dynamically regulated. Here we hypothesize that the AIS shows a dynamic regulation during maturation of the visual cortex. We therefore analyzed AIS length development from embryonic day (E) 12.5 to adulthood in mice. A tri-phasic time course of AIS length remodeling during development was observed. AIS first appeared at E14.5 and increased in length throughout the postnatal period to a peak between postnatal day (P) 10 to P15 (eyes open P13-14). Then, AIS length was reduced significantly around the beginning of the critical period for ocular dominance plasticity (CP, P21). Shortest AIS were observed at the peak of the CP (P28), followed by a moderate elongation towards the end of the CP (P35). To test if the dynamic maturation of the AIS is influenced by eye opening (onset of activity), animals were deprived of visual input before and during the CP. Deprivation for 1 week prior to eye opening did not affect AIS length development. However, deprivation from P0-P28 and P14-P28 resulted in AIS length distribution similar to the peak at P15. In other words, deprivation from birth prevents the transient shortening of the AIS and maintains an immature AIS length. These results are the first to suggest a dynamic maturation of the AIS in cortical neurons and point to novel mechanisms in the development of neuronal excitability.http://journal.frontiersin.org/Journal/10.3389/fnana.2014.00011/fullVisual Cortexplasticityaxon initial segmentDark Rearingankyrin-G
spellingShingle Annika eGutzmann
Nursah eErguel
Nursah eErguel
Rebecca eGrossmann
Christian eSchultz
Christian eSchultz
Petra eWahle
Maren eEngelhardt
Maren eEngelhardt
A period of structural plasticity at the axon initial segment in developing visual cortex
Frontiers in Neuroanatomy
Visual Cortex
plasticity
axon initial segment
Dark Rearing
ankyrin-G
title A period of structural plasticity at the axon initial segment in developing visual cortex
title_full A period of structural plasticity at the axon initial segment in developing visual cortex
title_fullStr A period of structural plasticity at the axon initial segment in developing visual cortex
title_full_unstemmed A period of structural plasticity at the axon initial segment in developing visual cortex
title_short A period of structural plasticity at the axon initial segment in developing visual cortex
title_sort period of structural plasticity at the axon initial segment in developing visual cortex
topic Visual Cortex
plasticity
axon initial segment
Dark Rearing
ankyrin-G
url http://journal.frontiersin.org/Journal/10.3389/fnana.2014.00011/full
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