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The Journal of Neurophysiology Vol. 82 No. 5 November 1999, pp. 2476-2489
Copyright ©1999 by the American Physiological Society
1Department of Physiology,
Erisir, A.,
D. Lau,
B. Rudy, and
C. S. Leonard.
Function of Specific K+ Channels in Sustained
High-Frequency Firing of Fast-Spiking Neocortical Interneurons. J. Neurophysiol. 82: 2476-2489, 1999. Fast-spiking GABAergic interneurons of the neocortex and hippocampus
fire high-frequency trains of brief action potentials with little
spike-frequency adaptation. How these striking properties arise is
unclear, although recent evidence suggests K+ channels
containing Kv3.1-Kv3.2 proteins play an important role. We investigated
the role of these channels in the firing properties of fast-spiking
neocortical interneurons from mouse somatosensory cortex using a
pharmacological and modeling approach. Low tetraethylammonium (TEA)
concentrations (
1 mM), which block only a few known K+
channels including Kv3.1-Kv3.2, profoundly impaired action potential repolarization and high-frequency firing. Analysis of the spike trains
evoked by steady depolarization revealed that, although TEA had little
effect on the initial firing rate, it strongly reduced firing frequency
later in the trains. These effects appeared to be specific to Kv3.1 and
Kv3.2 channels, because blockade of dendrotoxin-sensitive Kv1 channels
and BK Ca2+-activated K+ channels, which also
have high TEA sensitivity, produced opposite or no effects.
Voltage-clamp experiments confirmed the presence of a Kv3.1-Kv3.2-like
current in fast-spiking neurons, but not in other interneurons.
Analysis of spike shape changes during the spike trains suggested that
Na+ channel inactivation plays a significant role in the
firing-rate slowdown produced by TEA, a conclusion that was supported
by computer simulations. These findings indicate that the unique
properties of Kv3.1-Kv3.2 channels enable sustained high-frequency
firing by facilitating the recovery of Na+ channel
inactivation and by minimizing the duration of the
afterhyperpolarization in neocortical interneurons.
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