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Decreased but diverse activity of cortical and thalamic neurons in consciousness-impairing rodent absence seizures

Absence seizures are brief episodes of impaired consciousness, behavioral arrest, and unresponsiveness, with yet-unknown neuronal mechanisms. Here we report that an awake female rat model recapitulates the behavioral, electroencephalographic, and cortical functional magnetic resonance imaging charac...

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Autores principales: McCafferty, Cian, Gruenbaum, Benjamin F., Tung, Renee, Li, Jing-Jing, Zheng, Xinyuan, Salvino, Peter, Vincent, Peter, Kratochvil, Zachary, Ryu, Jun Hwan, Khalaf, Aya, Swift, Kohl, Akbari, Rashid, Islam, Wasif, Antwi, Prince, Johnson, Emily A., Vitkovskiy, Petr, Sampognaro, James, Freedman, Isaac G., Kundishora, Adam, Depaulis, Antoine, David, François, Crunelli, Vincenzo, Sanganahalli, Basavaraju G., Herman, Peter, Hyder, Fahmeed, Blumenfeld, Hal
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9832004/
https://www.ncbi.nlm.nih.gov/pubmed/36627270
http://dx.doi.org/10.1038/s41467-022-35535-4
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author McCafferty, Cian
Gruenbaum, Benjamin F.
Tung, Renee
Li, Jing-Jing
Zheng, Xinyuan
Salvino, Peter
Vincent, Peter
Kratochvil, Zachary
Ryu, Jun Hwan
Khalaf, Aya
Swift, Kohl
Akbari, Rashid
Islam, Wasif
Antwi, Prince
Johnson, Emily A.
Vitkovskiy, Petr
Sampognaro, James
Freedman, Isaac G.
Kundishora, Adam
Depaulis, Antoine
David, François
Crunelli, Vincenzo
Sanganahalli, Basavaraju G.
Herman, Peter
Hyder, Fahmeed
Blumenfeld, Hal
author_facet McCafferty, Cian
Gruenbaum, Benjamin F.
Tung, Renee
Li, Jing-Jing
Zheng, Xinyuan
Salvino, Peter
Vincent, Peter
Kratochvil, Zachary
Ryu, Jun Hwan
Khalaf, Aya
Swift, Kohl
Akbari, Rashid
Islam, Wasif
Antwi, Prince
Johnson, Emily A.
Vitkovskiy, Petr
Sampognaro, James
Freedman, Isaac G.
Kundishora, Adam
Depaulis, Antoine
David, François
Crunelli, Vincenzo
Sanganahalli, Basavaraju G.
Herman, Peter
Hyder, Fahmeed
Blumenfeld, Hal
author_sort McCafferty, Cian
collection PubMed
description Absence seizures are brief episodes of impaired consciousness, behavioral arrest, and unresponsiveness, with yet-unknown neuronal mechanisms. Here we report that an awake female rat model recapitulates the behavioral, electroencephalographic, and cortical functional magnetic resonance imaging characteristics of human absence seizures. Neuronally, seizures feature overall decreased but rhythmic firing of neurons in cortex and thalamus. Individual cortical and thalamic neurons express one of four distinct patterns of seizure-associated activity, one of which causes a transient initial peak in overall firing at seizure onset, and another which drives sustained decreases in overall firing. 40–60 s before seizure onset there begins a decline in low frequency electroencephalographic activity, neuronal firing, and behavior, but an increase in higher frequency electroencephalography and rhythmicity of neuronal firing. Our findings demonstrate that prolonged brain state changes precede consciousness-impairing seizures, and that during seizures distinct functional groups of cortical and thalamic neurons produce an overall transient firing increase followed by a sustained firing decrease, and increased rhythmicity.
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spelling pubmed-98320042023-01-12 Decreased but diverse activity of cortical and thalamic neurons in consciousness-impairing rodent absence seizures McCafferty, Cian Gruenbaum, Benjamin F. Tung, Renee Li, Jing-Jing Zheng, Xinyuan Salvino, Peter Vincent, Peter Kratochvil, Zachary Ryu, Jun Hwan Khalaf, Aya Swift, Kohl Akbari, Rashid Islam, Wasif Antwi, Prince Johnson, Emily A. Vitkovskiy, Petr Sampognaro, James Freedman, Isaac G. Kundishora, Adam Depaulis, Antoine David, François Crunelli, Vincenzo Sanganahalli, Basavaraju G. Herman, Peter Hyder, Fahmeed Blumenfeld, Hal Nat Commun Article Absence seizures are brief episodes of impaired consciousness, behavioral arrest, and unresponsiveness, with yet-unknown neuronal mechanisms. Here we report that an awake female rat model recapitulates the behavioral, electroencephalographic, and cortical functional magnetic resonance imaging characteristics of human absence seizures. Neuronally, seizures feature overall decreased but rhythmic firing of neurons in cortex and thalamus. Individual cortical and thalamic neurons express one of four distinct patterns of seizure-associated activity, one of which causes a transient initial peak in overall firing at seizure onset, and another which drives sustained decreases in overall firing. 40–60 s before seizure onset there begins a decline in low frequency electroencephalographic activity, neuronal firing, and behavior, but an increase in higher frequency electroencephalography and rhythmicity of neuronal firing. Our findings demonstrate that prolonged brain state changes precede consciousness-impairing seizures, and that during seizures distinct functional groups of cortical and thalamic neurons produce an overall transient firing increase followed by a sustained firing decrease, and increased rhythmicity. Nature Publishing Group UK 2023-01-10 /pmc/articles/PMC9832004/ /pubmed/36627270 http://dx.doi.org/10.1038/s41467-022-35535-4 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
McCafferty, Cian
Gruenbaum, Benjamin F.
Tung, Renee
Li, Jing-Jing
Zheng, Xinyuan
Salvino, Peter
Vincent, Peter
Kratochvil, Zachary
Ryu, Jun Hwan
Khalaf, Aya
Swift, Kohl
Akbari, Rashid
Islam, Wasif
Antwi, Prince
Johnson, Emily A.
Vitkovskiy, Petr
Sampognaro, James
Freedman, Isaac G.
Kundishora, Adam
Depaulis, Antoine
David, François
Crunelli, Vincenzo
Sanganahalli, Basavaraju G.
Herman, Peter
Hyder, Fahmeed
Blumenfeld, Hal
Decreased but diverse activity of cortical and thalamic neurons in consciousness-impairing rodent absence seizures
title Decreased but diverse activity of cortical and thalamic neurons in consciousness-impairing rodent absence seizures
title_full Decreased but diverse activity of cortical and thalamic neurons in consciousness-impairing rodent absence seizures
title_fullStr Decreased but diverse activity of cortical and thalamic neurons in consciousness-impairing rodent absence seizures
title_full_unstemmed Decreased but diverse activity of cortical and thalamic neurons in consciousness-impairing rodent absence seizures
title_short Decreased but diverse activity of cortical and thalamic neurons in consciousness-impairing rodent absence seizures
title_sort decreased but diverse activity of cortical and thalamic neurons in consciousness-impairing rodent absence seizures
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9832004/
https://www.ncbi.nlm.nih.gov/pubmed/36627270
http://dx.doi.org/10.1038/s41467-022-35535-4
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