Kv1.1 contributes to a rapid homeostatic plasticity of intrinsic excitability in CA1 pyramidal neurons in vivo

In area CA1 of the hippocampus, the selection of place cells to represent a new environment is biased towards neurons with higher excitability. However, different environments are represented by orthogonal cell ensembles, suggesting that regulatory mechanisms exist. Activity-dependent plasticity of...

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Main Authors: Peter James Morgan, Romain Bourboulou, Caroline Filippi, Julie Koenig-Gambini, Jérôme Epsztein
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2019-11-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/49915
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spelling doaj-aa35872d36244a55a649fb258a250d372021-05-05T18:07:51ZengeLife Sciences Publications LtdeLife2050-084X2019-11-01810.7554/eLife.49915Kv1.1 contributes to a rapid homeostatic plasticity of intrinsic excitability in CA1 pyramidal neurons in vivoPeter James Morgan0Romain Bourboulou1Caroline Filippi2Julie Koenig-Gambini3Jérôme Epsztein4https://orcid.org/0000-0002-5344-3986Institute of Neurobiology of the Mediterranean Sea (INMED), Turing Center for Living Systems (CENTURI), Aix-Marseille University, INSERM, Marseille, FranceInstitute of Neurobiology of the Mediterranean Sea (INMED), Turing Center for Living Systems (CENTURI), Aix-Marseille University, INSERM, Marseille, FranceInstitute of Neurobiology of the Mediterranean Sea (INMED), Turing Center for Living Systems (CENTURI), Aix-Marseille University, INSERM, Marseille, FranceInstitute of Neurobiology of the Mediterranean Sea (INMED), Turing Center for Living Systems (CENTURI), Aix-Marseille University, INSERM, Marseille, France; Institut Universitaire de France, Paris, FranceInstitute of Neurobiology of the Mediterranean Sea (INMED), Turing Center for Living Systems (CENTURI), Aix-Marseille University, INSERM, Marseille, FranceIn area CA1 of the hippocampus, the selection of place cells to represent a new environment is biased towards neurons with higher excitability. However, different environments are represented by orthogonal cell ensembles, suggesting that regulatory mechanisms exist. Activity-dependent plasticity of intrinsic excitability, as observed in vitro, is an attractive candidate. Here, using whole-cell patch-clamp recordings of CA1 pyramidal neurons in anesthetized rats, we have examined how inducing theta-bursts of action potentials affects their intrinsic excitability over time. We observed a long-lasting, homeostatic depression of intrinsic excitability which commenced within minutes, and, in contrast to in vitro observations, was not mediated by dendritic Ih. Instead, it was attenuated by the Kv1.1 channel blocker dendrotoxin K, suggesting an axonal origin. Analysis of place cells’ out-of-field firing in mice navigating in virtual reality further revealed an experience-dependent reduction consistent with decreased excitability. We propose that this mechanism could reduce memory interference.https://elifesciences.org/articles/49915hippocampusCA1 pyramidal cellsintrinsic excitabilitylong-term plasticitymemoryin vivo patch-clamp
collection DOAJ
language English
format Article
sources DOAJ
author Peter James Morgan
Romain Bourboulou
Caroline Filippi
Julie Koenig-Gambini
Jérôme Epsztein
spellingShingle Peter James Morgan
Romain Bourboulou
Caroline Filippi
Julie Koenig-Gambini
Jérôme Epsztein
Kv1.1 contributes to a rapid homeostatic plasticity of intrinsic excitability in CA1 pyramidal neurons in vivo
eLife
hippocampus
CA1 pyramidal cells
intrinsic excitability
long-term plasticity
memory
in vivo patch-clamp
author_facet Peter James Morgan
Romain Bourboulou
Caroline Filippi
Julie Koenig-Gambini
Jérôme Epsztein
author_sort Peter James Morgan
title Kv1.1 contributes to a rapid homeostatic plasticity of intrinsic excitability in CA1 pyramidal neurons in vivo
title_short Kv1.1 contributes to a rapid homeostatic plasticity of intrinsic excitability in CA1 pyramidal neurons in vivo
title_full Kv1.1 contributes to a rapid homeostatic plasticity of intrinsic excitability in CA1 pyramidal neurons in vivo
title_fullStr Kv1.1 contributes to a rapid homeostatic plasticity of intrinsic excitability in CA1 pyramidal neurons in vivo
title_full_unstemmed Kv1.1 contributes to a rapid homeostatic plasticity of intrinsic excitability in CA1 pyramidal neurons in vivo
title_sort kv1.1 contributes to a rapid homeostatic plasticity of intrinsic excitability in ca1 pyramidal neurons in vivo
publisher eLife Sciences Publications Ltd
series eLife
issn 2050-084X
publishDate 2019-11-01
description In area CA1 of the hippocampus, the selection of place cells to represent a new environment is biased towards neurons with higher excitability. However, different environments are represented by orthogonal cell ensembles, suggesting that regulatory mechanisms exist. Activity-dependent plasticity of intrinsic excitability, as observed in vitro, is an attractive candidate. Here, using whole-cell patch-clamp recordings of CA1 pyramidal neurons in anesthetized rats, we have examined how inducing theta-bursts of action potentials affects their intrinsic excitability over time. We observed a long-lasting, homeostatic depression of intrinsic excitability which commenced within minutes, and, in contrast to in vitro observations, was not mediated by dendritic Ih. Instead, it was attenuated by the Kv1.1 channel blocker dendrotoxin K, suggesting an axonal origin. Analysis of place cells’ out-of-field firing in mice navigating in virtual reality further revealed an experience-dependent reduction consistent with decreased excitability. We propose that this mechanism could reduce memory interference.
topic hippocampus
CA1 pyramidal cells
intrinsic excitability
long-term plasticity
memory
in vivo patch-clamp
url https://elifesciences.org/articles/49915
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