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

Author

Listed:
  • Cian McCafferty

    (Yale School of Medicine
    University College Cork)

  • 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
    Yale University
    Yale University)

  • Peter Herman

    (Yale University
    Yale University
    Yale University)

  • Fahmeed Hyder

    (Yale University
    Yale University
    Yale University)

  • Hal Blumenfeld

    (Yale School of Medicine
    Yale University
    Yale School of Medicine
    Yale School of Medicine)

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.

Suggested Citation

  • 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 & Wasi, 2023. "Decreased but diverse activity of cortical and thalamic neurons in consciousness-impairing rodent absence seizures," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-022-35535-4
    DOI: 10.1038/s41467-022-35535-4
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    References listed on IDEAS

    as
    1. Nikos K. Logothetis & Jon Pauls & Mark Augath & Torsten Trinath & Axel Oeltermann, 2001. "Neurophysiological investigation of the basis of the fMRI signal," Nature, Nature, vol. 412(6843), pages 150-157, July.
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    Cited by:

    1. Andrea I. Luppi & Lynn Uhrig & Jordy Tasserie & Camilo M. Signorelli & Emmanuel A. Stamatakis & Alain Destexhe & Bechir Jarraya & Rodrigo Cofre, 2024. "Local orchestration of distributed functional patterns supporting loss and restoration of consciousness in the primate brain," Nature Communications, Nature, vol. 15(1), pages 1-22, December.

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