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A supercritical density of fast Na(+) channels ensures rapid propagation of action potentials in GABAergic interneuron axons

Fast-spiking, parvalbumin-expressing GABAergic interneurons/basket cells (BCs) play a key role in feedforward and feedback inhibition, gamma oscillations, and complex information processing. For these functions, fast propagation of action potentials (APs) from the soma to the presynaptic terminals i...

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Detalles Bibliográficos
Autores principales: Hu, Hua, Jonas, Peter
Formato: Online Artículo Texto
Lenguaje:English
Publicado: 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4286295/
https://www.ncbi.nlm.nih.gov/pubmed/24657965
http://dx.doi.org/10.1038/nn.3678
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author Hu, Hua
Jonas, Peter
author_facet Hu, Hua
Jonas, Peter
author_sort Hu, Hua
collection PubMed
description Fast-spiking, parvalbumin-expressing GABAergic interneurons/basket cells (BCs) play a key role in feedforward and feedback inhibition, gamma oscillations, and complex information processing. For these functions, fast propagation of action potentials (APs) from the soma to the presynaptic terminals is important. However, the functional properties of interneuron axons remain elusive. Here, we examined interneuron axons by confocally targeted subcellular patch-clamp recording in rat hippocampal slices. APs were initiated in the proximal axon ~20 μm from the soma, and propagated to the distal axon with high reliability and speed. Subcellular mapping revealed a stepwise increase of Na(+) conductance density from the soma to the proximal axon, followed by a further gradual increase in the distal axon. Active cable modeling and experiments with partial channel block indicated that low axonal Na(+) conductance density was sufficient for reliability, but high Na(+) density was necessary for both speed of propagation and fast-spiking AP phenotype. Our results suggest that a supercritical density of Na(+) channels compensates for the morphological properties of interneuron axons (small segmental diameter, extensive branching, and high bouton density), ensuring fast AP propagation and high-frequency repetitive firing.
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spelling pubmed-42862952015-01-07 A supercritical density of fast Na(+) channels ensures rapid propagation of action potentials in GABAergic interneuron axons Hu, Hua Jonas, Peter Nat Neurosci Article Fast-spiking, parvalbumin-expressing GABAergic interneurons/basket cells (BCs) play a key role in feedforward and feedback inhibition, gamma oscillations, and complex information processing. For these functions, fast propagation of action potentials (APs) from the soma to the presynaptic terminals is important. However, the functional properties of interneuron axons remain elusive. Here, we examined interneuron axons by confocally targeted subcellular patch-clamp recording in rat hippocampal slices. APs were initiated in the proximal axon ~20 μm from the soma, and propagated to the distal axon with high reliability and speed. Subcellular mapping revealed a stepwise increase of Na(+) conductance density from the soma to the proximal axon, followed by a further gradual increase in the distal axon. Active cable modeling and experiments with partial channel block indicated that low axonal Na(+) conductance density was sufficient for reliability, but high Na(+) density was necessary for both speed of propagation and fast-spiking AP phenotype. Our results suggest that a supercritical density of Na(+) channels compensates for the morphological properties of interneuron axons (small segmental diameter, extensive branching, and high bouton density), ensuring fast AP propagation and high-frequency repetitive firing. 2014-03-23 2014-05 /pmc/articles/PMC4286295/ /pubmed/24657965 http://dx.doi.org/10.1038/nn.3678 Text en Users may view, print, copy, and download text and data-mine the content in such documents, for the purposes of academic research, subject always to the full Conditions of use:http://www.nature.com/authors/editorial_policies/license.html#terms
spellingShingle Article
Hu, Hua
Jonas, Peter
A supercritical density of fast Na(+) channels ensures rapid propagation of action potentials in GABAergic interneuron axons
title A supercritical density of fast Na(+) channels ensures rapid propagation of action potentials in GABAergic interneuron axons
title_full A supercritical density of fast Na(+) channels ensures rapid propagation of action potentials in GABAergic interneuron axons
title_fullStr A supercritical density of fast Na(+) channels ensures rapid propagation of action potentials in GABAergic interneuron axons
title_full_unstemmed A supercritical density of fast Na(+) channels ensures rapid propagation of action potentials in GABAergic interneuron axons
title_short A supercritical density of fast Na(+) channels ensures rapid propagation of action potentials in GABAergic interneuron axons
title_sort supercritical density of fast na(+) channels ensures rapid propagation of action potentials in gabaergic interneuron axons
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4286295/
https://www.ncbi.nlm.nih.gov/pubmed/24657965
http://dx.doi.org/10.1038/nn.3678
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