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

Cian McCafferty, Benjamin F. Gruenbaum, Renee Tung, Jing-Jing Li, Xinyuan Zheng, Peter Salvino, Peter Vincent, Zachary Kratochvil, Jun Hwan Ryu, Aya Khalaf, Kohl Swift, Rashid Akbari, Wasif Islam, Prince Antwi, Emily A. Johnson, Petr Vitkovskiy, James Sampognaro, Isaac G. Freedman, Adam Kundishora, Antoine Depaulis, François David, Vincenzo Crunelli, Basavaraju G. Sanganahalli, Peter Herman, Fahmeed Hyder and Hal Blumenfeld ()
Additional contact information
Cian McCafferty: Yale School of Medicine
Benjamin F. Gruenbaum: Yale School of Medicine
Renee Tung: Yale School of Medicine
Jing-Jing Li: Yale School of Medicine
Xinyuan Zheng: Yale School of Medicine
Peter Salvino: Yale School of Medicine
Peter Vincent: Yale School of Medicine
Zachary Kratochvil: Yale School of Medicine
Jun Hwan Ryu: Yale School of Medicine
Aya Khalaf: Yale School of Medicine
Kohl Swift: Yale School of Medicine
Rashid Akbari: Yale School of Medicine
Wasif Islam: Yale School of Medicine
Prince Antwi: Yale School of Medicine
Emily A. Johnson: Yale School of Medicine
Petr Vitkovskiy: Yale School of Medicine
James Sampognaro: Yale School of Medicine
Isaac G. Freedman: Yale School of Medicine
Adam Kundishora: Yale School of Medicine
Antoine Depaulis: Grenoble Institut Neurosciences
François David: Cardiff University
Vincenzo Crunelli: Cardiff University
Basavaraju G. Sanganahalli: Yale University
Peter Herman: Yale University
Fahmeed Hyder: Yale University
Hal Blumenfeld: Yale School of Medicine

Nature Communications, 2023, vol. 14, issue 1, 1-19

Abstract: Abstract 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.

Date: 2023
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DOI: 10.1038/s41467-022-35535-4

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