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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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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