Functional and molecular differences between voltage-gated K+ channels of fast-spiking interneurons and pyramidal neurons of rat hippocampus

Marco Martina, Jobst H. Schultz, Heimo Ehmke, Hannah Monyer, Peter Jonas*

*Corresponding author for this work

Research output: Contribution to journalArticle

303 Citations (Scopus)

Abstract

We have examined gating and pharmacological characteristics of somatic K+ channels in fast-spiking interneurons and regularly spiking principal neurons of hippocampal slices. In nucleated patches isolated from basket cells of the dentate gyrus, a fast delayed rectifier K+ current component that was highly sensitive to tetraethylammonium (TEA) and 4-aminopyridine (4- AP) (half-maximal inhibitory concentrations <0.1 mM) predominated, contributing an average of 58% to the total K+ current in these cells. By contrast, in pyramidal neurons of the CA1 region a rapidly inactivating A- type K+ current component that was TEA-resistant prevailed, contributing 61% to the total K+ current. Both types of neurons also showed small amounts of the K+ current component mainly found in the other type of neuron and, in addition, a slow delayed rectifier K+ current component with intermediate properties (sow inactivation, intermediate sensitivity to TEA). Single-cell RT-PCR analysis of mRNA revealed that Kv3 (Kv3.1, Kv3.2) subunit transcripts were expressed in almost all (89%) of the interneurons but only in 17% of the pyramidal neurons. In contrast, Kv4 (Kv4.2, Kv4.3) subunit mRNAs were present in 87% of pyramidal neurons but only in 55% of interneurons. Selective block of fast delayed rectifier K+ channels, presumably assembled from Kv3 subunits, by 4-AP reduced substantially the action potential frequency in interneurons. These results indicate that the differential expression of Kv3 and Kv4 subunits shapes the action potential phenotypes of principal neurons and interneurons in the cortex.

Original languageEnglish (US)
Pages (from-to)8111-8125
Number of pages15
JournalJournal of Neuroscience
Volume18
Issue number20
StatePublished - Oct 15 1998

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Voltage-Gated Potassium Channels
Pyramidal Cells
Interneurons
Hippocampus
Tetraethylammonium
Neurons
Action Potentials
4-Aminopyridine
Messenger RNA
Dentate Gyrus
Pharmacology
Phenotype
Polymerase Chain Reaction

Keywords

  • Hippocampal slices
  • Interneurons
  • Kv1, Kv2, Kv3, Kv4 subunits
  • Nucleated patch
  • Single-cell RT-PCR
  • Voltage-gated K channels

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

@article{0ce9e6a936ce444494e7c1d0eb3afbaa,
title = "Functional and molecular differences between voltage-gated K+ channels of fast-spiking interneurons and pyramidal neurons of rat hippocampus",
abstract = "We have examined gating and pharmacological characteristics of somatic K+ channels in fast-spiking interneurons and regularly spiking principal neurons of hippocampal slices. In nucleated patches isolated from basket cells of the dentate gyrus, a fast delayed rectifier K+ current component that was highly sensitive to tetraethylammonium (TEA) and 4-aminopyridine (4- AP) (half-maximal inhibitory concentrations <0.1 mM) predominated, contributing an average of 58{\%} to the total K+ current in these cells. By contrast, in pyramidal neurons of the CA1 region a rapidly inactivating A- type K+ current component that was TEA-resistant prevailed, contributing 61{\%} to the total K+ current. Both types of neurons also showed small amounts of the K+ current component mainly found in the other type of neuron and, in addition, a slow delayed rectifier K+ current component with intermediate properties (sow inactivation, intermediate sensitivity to TEA). Single-cell RT-PCR analysis of mRNA revealed that Kv3 (Kv3.1, Kv3.2) subunit transcripts were expressed in almost all (89{\%}) of the interneurons but only in 17{\%} of the pyramidal neurons. In contrast, Kv4 (Kv4.2, Kv4.3) subunit mRNAs were present in 87{\%} of pyramidal neurons but only in 55{\%} of interneurons. Selective block of fast delayed rectifier K+ channels, presumably assembled from Kv3 subunits, by 4-AP reduced substantially the action potential frequency in interneurons. These results indicate that the differential expression of Kv3 and Kv4 subunits shapes the action potential phenotypes of principal neurons and interneurons in the cortex.",
keywords = "Hippocampal slices, Interneurons, Kv1, Kv2, Kv3, Kv4 subunits, Nucleated patch, Single-cell RT-PCR, Voltage-gated K channels",
author = "Marco Martina and Schultz, {Jobst H.} and Heimo Ehmke and Hannah Monyer and Peter Jonas",
year = "1998",
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Functional and molecular differences between voltage-gated K+ channels of fast-spiking interneurons and pyramidal neurons of rat hippocampus. / Martina, Marco; Schultz, Jobst H.; Ehmke, Heimo; Monyer, Hannah; Jonas, Peter.

In: Journal of Neuroscience, Vol. 18, No. 20, 15.10.1998, p. 8111-8125.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Functional and molecular differences between voltage-gated K+ channels of fast-spiking interneurons and pyramidal neurons of rat hippocampus

AU - Martina, Marco

AU - Schultz, Jobst H.

AU - Ehmke, Heimo

AU - Monyer, Hannah

AU - Jonas, Peter

PY - 1998/10/15

Y1 - 1998/10/15

N2 - We have examined gating and pharmacological characteristics of somatic K+ channels in fast-spiking interneurons and regularly spiking principal neurons of hippocampal slices. In nucleated patches isolated from basket cells of the dentate gyrus, a fast delayed rectifier K+ current component that was highly sensitive to tetraethylammonium (TEA) and 4-aminopyridine (4- AP) (half-maximal inhibitory concentrations <0.1 mM) predominated, contributing an average of 58% to the total K+ current in these cells. By contrast, in pyramidal neurons of the CA1 region a rapidly inactivating A- type K+ current component that was TEA-resistant prevailed, contributing 61% to the total K+ current. Both types of neurons also showed small amounts of the K+ current component mainly found in the other type of neuron and, in addition, a slow delayed rectifier K+ current component with intermediate properties (sow inactivation, intermediate sensitivity to TEA). Single-cell RT-PCR analysis of mRNA revealed that Kv3 (Kv3.1, Kv3.2) subunit transcripts were expressed in almost all (89%) of the interneurons but only in 17% of the pyramidal neurons. In contrast, Kv4 (Kv4.2, Kv4.3) subunit mRNAs were present in 87% of pyramidal neurons but only in 55% of interneurons. Selective block of fast delayed rectifier K+ channels, presumably assembled from Kv3 subunits, by 4-AP reduced substantially the action potential frequency in interneurons. These results indicate that the differential expression of Kv3 and Kv4 subunits shapes the action potential phenotypes of principal neurons and interneurons in the cortex.

AB - We have examined gating and pharmacological characteristics of somatic K+ channels in fast-spiking interneurons and regularly spiking principal neurons of hippocampal slices. In nucleated patches isolated from basket cells of the dentate gyrus, a fast delayed rectifier K+ current component that was highly sensitive to tetraethylammonium (TEA) and 4-aminopyridine (4- AP) (half-maximal inhibitory concentrations <0.1 mM) predominated, contributing an average of 58% to the total K+ current in these cells. By contrast, in pyramidal neurons of the CA1 region a rapidly inactivating A- type K+ current component that was TEA-resistant prevailed, contributing 61% to the total K+ current. Both types of neurons also showed small amounts of the K+ current component mainly found in the other type of neuron and, in addition, a slow delayed rectifier K+ current component with intermediate properties (sow inactivation, intermediate sensitivity to TEA). Single-cell RT-PCR analysis of mRNA revealed that Kv3 (Kv3.1, Kv3.2) subunit transcripts were expressed in almost all (89%) of the interneurons but only in 17% of the pyramidal neurons. In contrast, Kv4 (Kv4.2, Kv4.3) subunit mRNAs were present in 87% of pyramidal neurons but only in 55% of interneurons. Selective block of fast delayed rectifier K+ channels, presumably assembled from Kv3 subunits, by 4-AP reduced substantially the action potential frequency in interneurons. These results indicate that the differential expression of Kv3 and Kv4 subunits shapes the action potential phenotypes of principal neurons and interneurons in the cortex.

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KW - Interneurons

KW - Kv1, Kv2, Kv3, Kv4 subunits

KW - Nucleated patch

KW - Single-cell RT-PCR

KW - Voltage-gated K channels

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