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Impaired Action Potential Initiation in GABAergic Interneurons Causes Hyperexcitable Networks in an Epileptic Mouse Model Carrying a Human NaV1.1 Mutation
Open accessAbstract
Mutations in SCN1A and other ion channel genes can cause different epileptic phenotypes, but the precise mechanisms underlying the development of hyperexcitable networks are largely unknown. Here, we present a multisystem analysis of an SCN1A mouse model carrying the Na V 1.1-R1648H mutation, which causes febrile seizures and epilepsy in humans. We found a ubiquitous hypoexcitability of interneurons in thalamus, cortex, and hippocampus, without detectable changes in excitatory neurons. Interestingly, somatic Na+channels in interneurons and persistent Na+currents were not significantly changed. Instead, the key mechanism of interneuron dysfunction was a deficit of action potential initiation at the axon initial segment that was identified by analyzing action potential firing. This deficit increased with the duration of firing periods, suggesting that increased slow inactivation, as recorded for recombinant mutated channels, could play an important role. The deficit in interneuron firing caused reduced action potential-driven inhibition of excitatory neurons as revealed by less frequent spontaneous but not miniature IPSCs. Multiple approaches indicated increased spontaneous thalamocortical and hippocampal network activity in mutant mice, as follows: (1) more synchronous and higher-frequency firing was recorded in primary neuronal cultures plated on multielectrode arrays; (2) thalamocortical slices examined by field potential recordings revealed spontaneous activities and pathological high-frequency oscillations; and (3) multineuron Ca 2+imaging in hippocampal slices showed increased spontaneous neuronal activity. Thus, an interneuron-specific generalized defect in action potential initiation causes multisystem disinhibition and network hyperexcitability, which can well explain the occurrence of seizures in the studied mouse model and in patients carrying this mutation.
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“Scn1a is a gene that encodes Nav1.1, a sodium channel necessary for PV cell firing (Ogiwara et al., 2007; Hedrich et al., 2014).”
From The Perineuronal ‘Safety’ Net? Perineuronal Net Abnormalities in Neurological Disorders (2018) · cites this paper as Hedrich et al., 2014
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“Recent studies demonstrate that reduced PV cell spike output may contribute to seizures in mice with genetic knock-in of mutated human Scn1a, which results in subtle changes in Nav1.1 functionality (Ogiwara et al., 2007; Hedrich et al., 2014).”
From The Perineuronal ‘Safety’ Net? Perineuronal Net Abnormalities in Neurological Disorders (2018) · cites this paper as Hedrich et al., 2014
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Metadata
- Authors
- Hedrich, U. B. S., Liautard, C., Kirschenbaum, D., Pofahl, M., Lavigne, J., Liu, Y., Theiss, S., Slotta, J., Escayg, A., Dihné, M., Beck, H., Mantegazza, M., & Lerche, H.
- Affiliations
- Hertie Institute for Clinical Brain Research (DE)
- Centre National de la Recherche Scientifique (FR)
- University of Bonn (DE)
- Heinrich Heine University Düsseldorf (DE)
- Emory University (US)
- ORCID
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2014-11-05
- Volume
- 34
- Issue
- 45
- Pages
- 14874-14889
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC4220023
- OpenAlex
- W1964533239
- Cited by
- 164
- References
- 70
- Citations by year
- 2026: 9 · 2025: 10 · 2024: 15 · 2023: 16 · 2022: 19 · 2021: 20 · 2020: 9 · 2019: 21 · 2018: 13 · 2017: 16 · 2016: 9 · 2015: 6 · 2014: 1
- FWCI
- 8.14
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- DZNE Pub (submittedVersion)
- Journal of Neuroscience Nursing
- Funders
- Danish Cancer Society Research Center
- European Commission
- Deutsche Forschungsgemeinschaft (SFB1089)
- National Institutes of Health
- National Institute of Neurological Disorders and Stroke (R01NS072221)
- Topics
- Health Sciences › Medicine › Clinical Neurology › Epilepsy research and treatment
- 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
- Keywords
- SCN1A, Nav1.1, GABAergic interneurons, action potential generation, axon initial segment, slow inactivation, disinhibition, network hyperexcitability, febrile seizures, epilepsy, thalamocortical network, hippocampal network activity, inhibitory postsynaptic currents, sodium channel mutations
- MeSH terms
- Action Potentials, Animals, Axons, Brain, Calcium, Cells, Cultured, Epilepsy, Humans, Interneurons, Mice, Inbred C57BL, Mutation, Nerve Net, Mice, Inhibitory Postsynaptic Potentials, GABAergic Neurons, NAV1.1 Voltage-Gated Sodium Channel
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