Expression and biophysical properties of Kv1 channels in supragranular neocortical pyramidal neurones

Dongxu Guan, J. C F Lee, T. Tkatch, D. J. Surmeier, William Armstrong, Robert Foehring

Research output: Contribution to journalArticle

60 Citations (Scopus)

Abstract

Potassium channels are extremely diverse regulators of neuronal excitability. As part of an investigation into how this molecular diversity is utilized by neurones, we examined the expression and biophysical properties of native Kv1 channels in layer II/III pyramidal neurones from somatosensory and motor cortex. Single-cell RT-PCR, immunocytochemistry, and whole cell recordings with specific peptide toxins revealed that individual pyramidal cells express multiple Kv1 α-subunits. The most abundant subunit mRNAs were Kv1.1 > 1.2 > 1.4 > 1.3. All of these subunits were localized to somatodendritic as well as axonal cell compartments. These data suggest variability in the subunit complexion of Kv1 channels in these cells. The α-dendrotoxin (α-DTX)-sensitive current activated more rapidly and at more negative potentials than the α-DTX-insensitive current, was first observed at voltages near action potential threshold, and was relatively insensitive to holding potential. The α-DTX-sensitive current comprised about 10% of outward current at steady-state, in response to steps from -70 mV. From -50 mV, this percentage increased to ∼20%. All cells expressed an α-DTX-sensitive current with slow inactivation kinetics. In some cells a transient component was also present. Deactivation kinetics were voltage dependent, such that deactivation was slow at potentials traversed by interspike intervals during repetitive firing. Because of its kinetics and voltage dependence, the α-DTX-sensitive current should be most important at physiological resting potentials and in response to brief stimuli. Kv1 channels should also be important at voltages near threshold and corresponding to interspike intervals.

Original languageEnglish (US)
Pages (from-to)371-389
Number of pages19
JournalJournal of Physiology
Volume571
Issue number2
DOIs
StatePublished - Mar 1 2006

Fingerprint

Pyramidal Cells
Somatosensory Cortex
Potassium Channels
Motor Cortex
Patch-Clamp Techniques
Membrane Potentials
Action Potentials
Immunohistochemistry
Neurons
Polymerase Chain Reaction
Messenger RNA
Peptides

All Science Journal Classification (ASJC) codes

  • Physiology

Cite this

Expression and biophysical properties of Kv1 channels in supragranular neocortical pyramidal neurones. / Guan, Dongxu; Lee, J. C F; Tkatch, T.; Surmeier, D. J.; Armstrong, William; Foehring, Robert.

In: Journal of Physiology, Vol. 571, No. 2, 01.03.2006, p. 371-389.

Research output: Contribution to journalArticle

@article{93cbc9ac00724bb68910969e30ff4edd,
title = "Expression and biophysical properties of Kv1 channels in supragranular neocortical pyramidal neurones",
abstract = "Potassium channels are extremely diverse regulators of neuronal excitability. As part of an investigation into how this molecular diversity is utilized by neurones, we examined the expression and biophysical properties of native Kv1 channels in layer II/III pyramidal neurones from somatosensory and motor cortex. Single-cell RT-PCR, immunocytochemistry, and whole cell recordings with specific peptide toxins revealed that individual pyramidal cells express multiple Kv1 α-subunits. The most abundant subunit mRNAs were Kv1.1 > 1.2 > 1.4 > 1.3. All of these subunits were localized to somatodendritic as well as axonal cell compartments. These data suggest variability in the subunit complexion of Kv1 channels in these cells. The α-dendrotoxin (α-DTX)-sensitive current activated more rapidly and at more negative potentials than the α-DTX-insensitive current, was first observed at voltages near action potential threshold, and was relatively insensitive to holding potential. The α-DTX-sensitive current comprised about 10{\%} of outward current at steady-state, in response to steps from -70 mV. From -50 mV, this percentage increased to ∼20{\%}. All cells expressed an α-DTX-sensitive current with slow inactivation kinetics. In some cells a transient component was also present. Deactivation kinetics were voltage dependent, such that deactivation was slow at potentials traversed by interspike intervals during repetitive firing. Because of its kinetics and voltage dependence, the α-DTX-sensitive current should be most important at physiological resting potentials and in response to brief stimuli. Kv1 channels should also be important at voltages near threshold and corresponding to interspike intervals.",
author = "Dongxu Guan and Lee, {J. C F} and T. Tkatch and Surmeier, {D. J.} and William Armstrong and Robert Foehring",
year = "2006",
month = "3",
day = "1",
doi = "10.1113/jphysiol.2005.097006",
language = "English (US)",
volume = "571",
pages = "371--389",
journal = "Journal of Physiology",
issn = "0022-3751",
publisher = "Wiley-Blackwell",
number = "2",

}

TY - JOUR

T1 - Expression and biophysical properties of Kv1 channels in supragranular neocortical pyramidal neurones

AU - Guan, Dongxu

AU - Lee, J. C F

AU - Tkatch, T.

AU - Surmeier, D. J.

AU - Armstrong, William

AU - Foehring, Robert

PY - 2006/3/1

Y1 - 2006/3/1

N2 - Potassium channels are extremely diverse regulators of neuronal excitability. As part of an investigation into how this molecular diversity is utilized by neurones, we examined the expression and biophysical properties of native Kv1 channels in layer II/III pyramidal neurones from somatosensory and motor cortex. Single-cell RT-PCR, immunocytochemistry, and whole cell recordings with specific peptide toxins revealed that individual pyramidal cells express multiple Kv1 α-subunits. The most abundant subunit mRNAs were Kv1.1 > 1.2 > 1.4 > 1.3. All of these subunits were localized to somatodendritic as well as axonal cell compartments. These data suggest variability in the subunit complexion of Kv1 channels in these cells. The α-dendrotoxin (α-DTX)-sensitive current activated more rapidly and at more negative potentials than the α-DTX-insensitive current, was first observed at voltages near action potential threshold, and was relatively insensitive to holding potential. The α-DTX-sensitive current comprised about 10% of outward current at steady-state, in response to steps from -70 mV. From -50 mV, this percentage increased to ∼20%. All cells expressed an α-DTX-sensitive current with slow inactivation kinetics. In some cells a transient component was also present. Deactivation kinetics were voltage dependent, such that deactivation was slow at potentials traversed by interspike intervals during repetitive firing. Because of its kinetics and voltage dependence, the α-DTX-sensitive current should be most important at physiological resting potentials and in response to brief stimuli. Kv1 channels should also be important at voltages near threshold and corresponding to interspike intervals.

AB - Potassium channels are extremely diverse regulators of neuronal excitability. As part of an investigation into how this molecular diversity is utilized by neurones, we examined the expression and biophysical properties of native Kv1 channels in layer II/III pyramidal neurones from somatosensory and motor cortex. Single-cell RT-PCR, immunocytochemistry, and whole cell recordings with specific peptide toxins revealed that individual pyramidal cells express multiple Kv1 α-subunits. The most abundant subunit mRNAs were Kv1.1 > 1.2 > 1.4 > 1.3. All of these subunits were localized to somatodendritic as well as axonal cell compartments. These data suggest variability in the subunit complexion of Kv1 channels in these cells. The α-dendrotoxin (α-DTX)-sensitive current activated more rapidly and at more negative potentials than the α-DTX-insensitive current, was first observed at voltages near action potential threshold, and was relatively insensitive to holding potential. The α-DTX-sensitive current comprised about 10% of outward current at steady-state, in response to steps from -70 mV. From -50 mV, this percentage increased to ∼20%. All cells expressed an α-DTX-sensitive current with slow inactivation kinetics. In some cells a transient component was also present. Deactivation kinetics were voltage dependent, such that deactivation was slow at potentials traversed by interspike intervals during repetitive firing. Because of its kinetics and voltage dependence, the α-DTX-sensitive current should be most important at physiological resting potentials and in response to brief stimuli. Kv1 channels should also be important at voltages near threshold and corresponding to interspike intervals.

UR - http://www.scopus.com/inward/record.url?scp=33645277654&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=33645277654&partnerID=8YFLogxK

U2 - 10.1113/jphysiol.2005.097006

DO - 10.1113/jphysiol.2005.097006

M3 - Article

VL - 571

SP - 371

EP - 389

JO - Journal of Physiology

JF - Journal of Physiology

SN - 0022-3751

IS - 2

ER -