Function of Specific K + Channels in Sustained High-Frequency Firing of Fast-Spiking Neocortical Interneurons
Abstract
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 Ca(2+)-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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Delayed rectifier channels assembled from Kv3 subunits are instrumental components in conferring high-frequency action potential firing in numerous hippocampal and cortical interneuron subtypes.
“Delayed rectifier channels assembled from Kv3 subunits are instrumental components in conferring high-frequency action potential firing in numerous hippocampal and cortical interneuron subtypes (304, 967, 1187).”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [304]
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- Authors
- Erisir, A., Lau, D., Rudy, B., & Leonard, C. S.
- Affiliations
- Department of Physiology, New York Medical College, Valhalla 10595; and
- New York University (US)
- New York Medical College (US)
- Venue
- Journal of Neurophysiology
- Publisher
- American Physiological Society
- Published
- 1999-11-01
- Volume
- 82
- Issue
- 5
- Pages
- 2476-2489
- ISSN
- 0022-3077 (ISSN-L)
- 1522-1598
- OpenAlex
- W1747998245
- Cited by
- 458
- References
- 65
- Citations by year
- 2026: 21 · 2025: 11 · 2024: 16 · 2023: 12 · 2022: 20 · 2021: 21 · 2020: 13 · 2019: 16 · 2018: 14 · 2017: 16 · 2016: 15 · 2015: 19 · 2014: 14 · 2013: 13 · 2012: 15
- FWCI
- 4.59
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Neurophysiology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (1r01ns035215-01a1)
- National Institute of Neurological Disorders and Stroke (NS27881, NS-35215)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ion channel regulation and function
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Cardiac electrophysiology and arrhythmias
- Keywords
- Kv3.1, potassium channels, fast-spiking interneurons, neocortical interneurons, high-frequency firing, spike frequency adaptation, tetraethylammonium, action potential repolarization, afterhyperpolarization, somatosensory cortex, GABAergic interneurons
- MeSH terms
- Action Potentials, Animals, Evoked Potentials, Hippocampus, Interneurons, Mice, Inbred C57BL, Neurons, Neuropeptides, Reaction Time, Regression Analysis, Somatosensory Cortex, Potassium Channels, Neocortex, Tetraethylammonium, Potassium Channels, Voltage-Gated, Mice, Shaw Potassium Channels, In Vitro Techniques
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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