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The Journal of Neuroscience, March 15, 2003, 23(6):2058
Kv3 Potassium Conductance is Necessary and Kinetically Optimized
for High-Frequency Action Potential Generation in Hippocampal
Interneurons
Cheng-Chang
Lien and
Peter
Jonas
Institute of Physiology, University of Freiburg, D-79104 Freiburg,
Germany
Kv3 channels are thought to be essential for the fast-spiking (FS)
phenotype in GABAergic interneurons, but how these channels confer the
ability to generate action potentials (APs) at high frequency is
unknown. To address this question, we developed a fast dynamic-clamp
system ( 50 kHz) that allowed us to add a Kv3 model conductance to
CA1 oriens alveus (OA) interneurons in hippocampal slices. Selective
pharmacological block of Kv3 channels by 0.3 mM
4-aminopyridine or 1 mM tetraethylammonium ions led to a
marked broadening of APs during trains of short stimuli and a reduction in AP frequency during 1 sec stimuli. The addition of artificial Kv3
conductance restored the original AP pattern. Subtraction of Kv3
conductance by dynamic clamp mimicked the effects of the blockers.
Application of artificial Kv3 conductance also led to FS in OA
interneurons after complete K+ channel block and
even induced FS in hippocampal pyramidal neurons in the absence of
blockers. Adding artificial Kv3 conductance with altered deactivation
kinetics revealed a nonmonotonic relationship between mean AP frequency
and deactivation rate, with a maximum slightly above the original
value. Insertion of artificial Kv3 conductance with either lowered
activation threshold or inactivation also led to a reduction in the
mean AP frequency. However, the mechanisms were distinct. Shifting the
activation threshold induced adaptation, whereas adding inactivation
caused frequency-dependent AP broadening. In conclusion, Kv3 channels
are necessary for the FS phenotype of OA interneurons, and several of
their gating properties appear to be optimized for high-frequency
repetitive activity.
Key words:
Kv3 channels; dynamic clamp; fast spiking; deactivation kinetics; OA interneurons; hippocampal slices; two
electrode current clamp
Copyright © 2003 Society for Neuroscience 0270-6474/03/2362058-11$05.00/0
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|
|
|
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|
|
|
|
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|
|
|
|
|
|
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|
|
|
|
|
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|
|
|
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[Full Text]
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|
|
|
|
|
|
|
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304(5668):
265 - 270.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Lewis, Z. A. McCrossan, and G. W. Abbott
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279(9):
7884 - 7892.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
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23(22):
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[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
