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Evidence of an inhibitory restraint of seizure activity in humans

Author

Listed:
  • Catherine A. Schevon

    (Columbia University)

  • Shennan A. Weiss

    (Columbia University)

  • Guy McKhann

    (Columbia University)

  • Robert R. Goodman

    (Columbia University)

  • Rafael Yuste

    (Howard Hughes Medical Institute, Columbia University)

  • Ronald G. Emerson

    (Columbia University
    Hospital for Special Surgery, Cornell University)

  • Andrew J. Trevelyan

    (Institutes of Neuroscience/Aging and Health, Newcastle University, Medical School)

Abstract

The location and trajectory of seizure activity is of great importance, yet our ability to map such activity remains primitive. Recently, the development of multi-electrode arrays for use in humans has provided new levels of temporal and spatial resolution for recording seizures. Here, we show that there is a sharp delineation between areas showing intense, hypersynchronous firing indicative of recruitment to the seizure, and adjacent territories where there is only low-level, unstructured firing. Thus, there is a core territory of recruited neurons and a surrounding 'ictal penumbra'. The defining feature of the 'ictal penumbra' is the contrast between the large amplitude EEG signals and the low-level firing there. Our human recordings bear striking similarities with animal studies of an inhibitory restraint, indicating that they can be readily understood in terms of this mechanism. These findings have important implications for how we localize seizure activity and map its spread.

Suggested Citation

  • Catherine A. Schevon & Shennan A. Weiss & Guy McKhann & Robert R. Goodman & Rafael Yuste & Ronald G. Emerson & Andrew J. Trevelyan, 2012. "Evidence of an inhibitory restraint of seizure activity in humans," Nature Communications, Nature, vol. 3(1), pages 1-11, January.
  • Handle: RePEc:nat:natcom:v:3:y:2012:i:1:d:10.1038_ncomms2056
    DOI: 10.1038/ncomms2056
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    Citations

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    Cited by:

    1. Laura R González-Ramírez & Omar J Ahmed & Sydney S Cash & C Eugene Wayne & Mark A Kramer, 2015. "A Biologically Constrained, Mathematical Model of Cortical Wave Propagation Preceding Seizure Termination," PLOS Computational Biology, Public Library of Science, vol. 11(2), pages 1-34, February.
    2. Joshua M. Diamond & Julio I. Chapeton & Weizhen Xie & Samantha N. Jackson & Sara K. Inati & Kareem A. Zaghloul, 2024. "Focal seizures induce spatiotemporally organized spiking activity in the human cortex," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    3. Suseendrakumar Duraivel & Shervin Rahimpour & Chia-Han Chiang & Michael Trumpis & Charles Wang & Katrina Barth & Stephen C. Harward & Shivanand P. Lad & Allan H. Friedman & Derek G. Southwell & Saurab, 2023. "High-resolution neural recordings improve the accuracy of speech decoding," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    4. Enrico Pracucci & Robert T. Graham & Laura Alberio & Gabriele Nardi & Olga Cozzolino & Vinoshene Pillai & Giacomo Pasquini & Luciano Saieva & Darren Walsh & Silvia Landi & Jinwei Zhang & Andrew J. Tre, 2023. "Daily rhythm in cortical chloride homeostasis underpins functional changes in visual cortex excitability," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    5. Pierre Bourdillon & Liankun Ren & Mila Halgren & Angelique C. Paulk & Pariya Salami & István Ulbert & Dániel Fabó & Jean-Rémi King & Kane M. Sjoberg & Emad N. Eskandar & Joseph R. Madsen & Eric Halgre, 2024. "Differential cortical layer engagement during seizure initiation and spread in humans," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    6. John-Sebastian Mueller & Fabio C. Tescarollo & Trong Huynh & Daniel A. Brenner & Daniel J. Valdivia & Kanyin Olagbegi & Sahana Sangappa & Spencer C. Chen & Hai Sun, 2023. "Ictogenesis proceeds through discrete phases in hippocampal CA1 seizures in mice," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    7. Yuki Bando & Michael Wenzel & Rafael Yuste, 2021. "Simultaneous two-photon imaging of action potentials and subthreshold inputs in vivo," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
    8. Annika Hagemann & Jens Wilting & Bita Samimizad & Florian Mormann & Viola Priesemann, 2021. "Assessing criticality in pre-seizure single-neuron activity of human epileptic cortex," PLOS Computational Biology, Public Library of Science, vol. 17(3), pages 1-18, March.
    9. Laurent Sheybani & Umesh Vivekananda & Roman Rodionov & Beate Diehl & Fahmida A. Chowdhury & Andrew W. McEvoy & Anna Miserocchi & James A. Bisby & Daniel Bush & Neil Burgess & Matthew C. Walker, 2023. "Wake slow waves in focal human epilepsy impact network activity and cognition," Nature Communications, Nature, vol. 14(1), pages 1-14, December.

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