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The ictal wavefront is the spatiotemporal source of discharges during spontaneous human seizures

Author

Listed:
  • Elliot H. Smith

    (Columbia University Medical Center)

  • Jyun-you Liou

    (Columbia University)

  • Tyler S. Davis

    (University of Utah)

  • Edward M. Merricks

    (Institute of Neuroscience, Newcastle University)

  • Spencer S. Kellis

    (California Institute of Technology)

  • Shennan A. Weiss

    (UCLA David Geffen School of Medicine)

  • Bradley Greger

    (School of Biological and Health Systems Engineering, Arizona State University)

  • Paul A. House

    (University of Utah)

  • Guy M. McKhann II

    (Columbia University Medical Center)

  • Robert R. Goodman

    (Icahn School of Medicine at Mount Sinai)

  • Ronald G. Emerson

    (Weill Cornell Medical College)

  • Lisa M. Bateman

    (Columbia University Medical Center)

  • Andrew J. Trevelyan

    (Institute of Neuroscience, Newcastle University)

  • Catherine A. Schevon

    (Columbia University Medical Center)

Abstract

The extensive distribution and simultaneous termination of seizures across cortical areas has led to the hypothesis that seizures are caused by large-scale coordinated networks spanning these areas. This view, however, is difficult to reconcile with most proposed mechanisms of seizure spread and termination, which operate on a cellular scale. We hypothesize that seizures evolve into self-organized structures wherein a small seizing territory projects high-intensity electrical signals over a broad cortical area. Here we investigate human seizures on both small and large electrophysiological scales. We show that the migrating edge of the seizing territory is the source of travelling waves of synaptic activity into adjacent cortical areas. As the seizure progresses, slow dynamics in induced activity from these waves indicate a weakening and eventual failure of their source. These observations support a parsimonious theory for how large-scale evolution and termination of seizures are driven from a small, migrating cortical area.

Suggested Citation

  • Elliot H. Smith & Jyun-you Liou & Tyler S. Davis & Edward M. Merricks & Spencer S. Kellis & Shennan A. Weiss & Bradley Greger & Paul A. House & Guy M. McKhann II & Robert R. Goodman & Ronald G. Emerso, 2016. "The ictal wavefront is the spatiotemporal source of discharges during spontaneous human seizures," Nature Communications, Nature, vol. 7(1), pages 1-12, September.
  • Handle: RePEc:nat:natcom:v:7:y:2016:i:1:d:10.1038_ncomms11098
    DOI: 10.1038/ncomms11098
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    Cited by:

    1. 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.
    2. Vasiliki Bougou & Michaël Vanhoyland & Alexander Bertrand & Wim Paesschen & Hans Op De Beeck & Peter Janssen & Tom Theys, 2024. "Neuronal tuning and population representations of shape and category in human visual cortex," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    3. 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.
    4. 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.
    5. Anton V Chizhov & Aleksei E Sanin, 2020. "A simple model of epileptic seizure propagation: Potassium diffusion versus axo-dendritic spread," PLOS ONE, Public Library of Science, vol. 15(4), pages 1-21, April.

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