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Cofilin1 Controls Transcolumnar Plasticity in Dendritic Spines in Adult Barrel Cortex

During sensory deprivation, the barrel cortex undergoes expansion of a functional column representing spared inputs (spared column), into the neighboring deprived columns (representing deprived inputs) which are in turn shrunk. As a result, the neurons in a deprived column simultaneously increase an...

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Autores principales: Tsubota, Tadashi, Okubo-Suzuki, Reiko, Ohashi, Yohei, Tamura, Keita, Ogata, Koshin, Yaguchi, Masae, Matsuyama, Makoto, Inokuchi, Kaoru, Miyashita, Yasushi
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4344332/
https://www.ncbi.nlm.nih.gov/pubmed/25723479
http://dx.doi.org/10.1371/journal.pbio.1002070
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author Tsubota, Tadashi
Okubo-Suzuki, Reiko
Ohashi, Yohei
Tamura, Keita
Ogata, Koshin
Yaguchi, Masae
Matsuyama, Makoto
Inokuchi, Kaoru
Miyashita, Yasushi
author_facet Tsubota, Tadashi
Okubo-Suzuki, Reiko
Ohashi, Yohei
Tamura, Keita
Ogata, Koshin
Yaguchi, Masae
Matsuyama, Makoto
Inokuchi, Kaoru
Miyashita, Yasushi
author_sort Tsubota, Tadashi
collection PubMed
description During sensory deprivation, the barrel cortex undergoes expansion of a functional column representing spared inputs (spared column), into the neighboring deprived columns (representing deprived inputs) which are in turn shrunk. As a result, the neurons in a deprived column simultaneously increase and decrease their responses to spared and deprived inputs, respectively. Previous studies revealed that dendritic spines are remodeled during this barrel map plasticity. Because cofilin1, a predominant regulator of actin filament turnover, governs both the expansion and shrinkage of the dendritic spine structure in vitro, it hypothetically regulates both responses in barrel map plasticity. However, this hypothesis remains untested. Using lentiviral vectors, we knocked down cofilin1 locally within layer 2/3 neurons in a deprived column. Cofilin1-knocked-down neurons were optogenetically labeled using channelrhodopsin-2, and electrophysiological recordings were targeted to these knocked-down neurons. We showed that cofilin1 knockdown impaired response increases to spared inputs but preserved response decreases to deprived inputs, indicating that cofilin1 dependency is dissociated in these two types of barrel map plasticity. To explore the structural basis of this dissociation, we then analyzed spine densities on deprived column dendritic branches, which were supposed to receive dense horizontal transcolumnar projections from the spared column. We found that spine number increased in a cofilin1-dependent manner selectively in the distal part of the supragranular layer, where most of the transcolumnar projections existed. Our findings suggest that cofilin1-mediated actin dynamics regulate functional map plasticity in an input-specific manner through the dendritic spine remodeling that occurs in the horizontal transcolumnar circuits. These new mechanistic insights into transcolumnar plasticity in adult rats may have a general significance for understanding reorganization of neocortical circuits that have more sophisticated columnar organization than the rodent neocortex, such as the primate neocortex.
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spelling pubmed-43443322015-03-04 Cofilin1 Controls Transcolumnar Plasticity in Dendritic Spines in Adult Barrel Cortex Tsubota, Tadashi Okubo-Suzuki, Reiko Ohashi, Yohei Tamura, Keita Ogata, Koshin Yaguchi, Masae Matsuyama, Makoto Inokuchi, Kaoru Miyashita, Yasushi PLoS Biol Research Article During sensory deprivation, the barrel cortex undergoes expansion of a functional column representing spared inputs (spared column), into the neighboring deprived columns (representing deprived inputs) which are in turn shrunk. As a result, the neurons in a deprived column simultaneously increase and decrease their responses to spared and deprived inputs, respectively. Previous studies revealed that dendritic spines are remodeled during this barrel map plasticity. Because cofilin1, a predominant regulator of actin filament turnover, governs both the expansion and shrinkage of the dendritic spine structure in vitro, it hypothetically regulates both responses in barrel map plasticity. However, this hypothesis remains untested. Using lentiviral vectors, we knocked down cofilin1 locally within layer 2/3 neurons in a deprived column. Cofilin1-knocked-down neurons were optogenetically labeled using channelrhodopsin-2, and electrophysiological recordings were targeted to these knocked-down neurons. We showed that cofilin1 knockdown impaired response increases to spared inputs but preserved response decreases to deprived inputs, indicating that cofilin1 dependency is dissociated in these two types of barrel map plasticity. To explore the structural basis of this dissociation, we then analyzed spine densities on deprived column dendritic branches, which were supposed to receive dense horizontal transcolumnar projections from the spared column. We found that spine number increased in a cofilin1-dependent manner selectively in the distal part of the supragranular layer, where most of the transcolumnar projections existed. Our findings suggest that cofilin1-mediated actin dynamics regulate functional map plasticity in an input-specific manner through the dendritic spine remodeling that occurs in the horizontal transcolumnar circuits. These new mechanistic insights into transcolumnar plasticity in adult rats may have a general significance for understanding reorganization of neocortical circuits that have more sophisticated columnar organization than the rodent neocortex, such as the primate neocortex. Public Library of Science 2015-02-27 /pmc/articles/PMC4344332/ /pubmed/25723479 http://dx.doi.org/10.1371/journal.pbio.1002070 Text en © 2015 Tsubota et al http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Tsubota, Tadashi
Okubo-Suzuki, Reiko
Ohashi, Yohei
Tamura, Keita
Ogata, Koshin
Yaguchi, Masae
Matsuyama, Makoto
Inokuchi, Kaoru
Miyashita, Yasushi
Cofilin1 Controls Transcolumnar Plasticity in Dendritic Spines in Adult Barrel Cortex
title Cofilin1 Controls Transcolumnar Plasticity in Dendritic Spines in Adult Barrel Cortex
title_full Cofilin1 Controls Transcolumnar Plasticity in Dendritic Spines in Adult Barrel Cortex
title_fullStr Cofilin1 Controls Transcolumnar Plasticity in Dendritic Spines in Adult Barrel Cortex
title_full_unstemmed Cofilin1 Controls Transcolumnar Plasticity in Dendritic Spines in Adult Barrel Cortex
title_short Cofilin1 Controls Transcolumnar Plasticity in Dendritic Spines in Adult Barrel Cortex
title_sort cofilin1 controls transcolumnar plasticity in dendritic spines in adult barrel cortex
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4344332/
https://www.ncbi.nlm.nih.gov/pubmed/25723479
http://dx.doi.org/10.1371/journal.pbio.1002070
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