IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-51338-1.html
   My bibliography  Save this article

Focal seizures induce spatiotemporally organized spiking activity in the human cortex

Author

Listed:
  • Joshua M. Diamond

    (NINDS, National Institutes of Health)

  • Julio I. Chapeton

    (NINDS, National Institutes of Health)

  • Weizhen Xie

    (NINDS, National Institutes of Health
    University of Maryland)

  • Samantha N. Jackson

    (NINDS, National Institutes of Health)

  • Sara K. Inati

    (NINDS, National Institutes of Health)

  • Kareem A. Zaghloul

    (NINDS, National Institutes of Health)

Abstract

Epileptic seizures are debilitating because of the clinical symptoms they produce. These symptoms, in turn, may stem directly from disruptions in neural coding. Recent evidence has suggested that the specific temporal order, or sequence, of spiking across a population of cortical neurons may encode information. Here, we investigate how seizures disrupt neuronal spiking sequences in the human brain by recording multi-unit activity from the cerebral cortex in five male participants undergoing monitoring for seizures. We find that pathological discharges during seizures are associated with bursts of spiking activity across a population of cortical neurons. These bursts are organized into highly consistent and stereotyped temporal sequences. As the seizure evolves, spiking sequences diverge from the sequences observed at baseline and become more spatially organized. The direction of this spatial organization matches the direction of the ictal discharges, which spread over the cortex as traveling waves. Our data therefore suggest that seizures can entrain cortical spiking sequences by changing the spatial organization of neuronal firing, providing a possible mechanism by which seizures create symptoms.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-51338-1
    DOI: 10.1038/s41467-024-51338-1
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-51338-1
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-024-51338-1?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Berens, Philipp, 2009. "CircStat: A MATLAB Toolbox for Circular Statistics," Journal of Statistical Software, Foundation for Open Access Statistics, vol. 31(i10).
    2. Uma R. Mohan & Honghui Zhang & Bard Ermentrout & Joshua Jacobs, 2024. "The direction of theta and alpha travelling waves modulates human memory processing," Nature Human Behaviour, Nature, vol. 8(6), pages 1124-1135, June.
    3. L. Federico Rossi & Robert C. Wykes & Dimitri M. Kullmann & Matteo Carandini, 2017. "Focal cortical seizures start as standing waves and propagate respecting homotopic connectivity," Nature Communications, Nature, vol. 8(1), pages 1-11, December.
    4. L-E Martinet & G. Fiddyment & J. R. Madsen & E. N. Eskandar & W. Truccolo & U. T. Eden & S. S. Cash & M. A. Kramer, 2017. "Human seizures couple across spatial scales through travelling wave dynamics," Nature Communications, Nature, vol. 8(1), pages 1-13, April.
    5. 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.
    6. 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.
    7. Kwabena Boahen, 2022. "Dendrocentric learning for synthetic intelligence," Nature, Nature, vol. 612(7938), pages 43-50, December.
    8. Timothée Proix & Viktor K. Jirsa & Fabrice Bartolomei & Maxime Guye & Wilson Truccolo, 2018. "Predicting the spatiotemporal diversity of seizure propagation and termination in human focal epilepsy," Nature Communications, Nature, vol. 9(1), pages 1-15, December.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. 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.
    2. 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.
    3. Michael E Rule & David Schnoerr & Matthias H Hennig & Guido Sanguinetti, 2019. "Neural field models for latent state inference: Application to large-scale neuronal recordings," PLOS Computational Biology, Public Library of Science, vol. 15(11), pages 1-23, November.
    4. 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.
    5. 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.
    6. 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.
    7. Kyerl Park & Yoonsoo Yeo & Kisung Shin & Jeehyun Kwag, 2024. "Egocentric neural representation of geometric vertex in the retrosplenial cortex," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    8. Jennifer B Tennessen & Marla M Holt & Brianna M Wright & M Bradley Hanson & Candice K Emmons & Deborah A Giles & Jeffrey T Hogan & Sheila J Thornton & Volker B Deecke, 2023. "Divergent foraging strategies between populations of sympatric matrilineal killer whales," Behavioral Ecology, International Society for Behavioral Ecology, vol. 34(3), pages 373-386.
    9. Thomas Schreiner & Marit Petzka & Tobias Staudigl & Bernhard P. Staresina, 2023. "Respiration modulates sleep oscillations and memory reactivation in humans," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    10. Simone D’Agostino & Filippo Moro & Tristan Torchet & Yiğit Demirağ & Laurent Grenouillet & Niccolò Castellani & Giacomo Indiveri & Elisa Vianello & Melika Payvand, 2024. "DenRAM: neuromorphic dendritic architecture with RRAM for efficient temporal processing with delays," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    11. Thomas Schreiner & Elisabeth Kaufmann & Soheyl Noachtar & Jan-Hinnerk Mehrkens & Tobias Staudigl, 2022. "The human thalamus orchestrates neocortical oscillations during NREM sleep," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    12. 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.
    13. Celia M. Gagliardi & Marc E. Normandin & Alexandra T. Keinath & Joshua B. Julian & Matthew R. Lopez & Manuel-Miguel Ramos-Alvarez & Russell A. Epstein & Isabel A. Muzzio, 2024. "Distinct neural mechanisms for heading retrieval and context recognition in the hippocampus during spatial reorientation," Nature Communications, Nature, vol. 15(1), pages 1-22, December.
    14. Alireza Saeedi & Kun Wang & Ghazaleh Nikpourian & Andreas Bartels & Nikos K. Logothetis & Nelson K. Totah & Masataka Watanabe, 2024. "Brightness illusions drive a neuronal response in the primary visual cortex under top-down modulation," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    15. Arthur Pewsey & Eduardo García-Portugués, 2021. "Recent advances in directional statistics," TEST: An Official Journal of the Spanish Society of Statistics and Operations Research, Springer;Sociedad de Estadística e Investigación Operativa, vol. 30(1), pages 1-58, March.
    16. Thomas Schreiner & Benjamin J. Griffiths & Merve Kutlu & Christian Vollmar & Elisabeth Kaufmann & Stefanie Quach & Jan Remi & Soheyl Noachtar & Tobias Staudigl, 2024. "Spindle-locked ripples mediate memory reactivation during human NREM sleep," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    17. César Henrique Mattos Pires & Felipe M. Pimenta & Carla A. D'Aquino & Osvaldo R. Saavedra & Xuerui Mao & Arcilan T. Assireu, 2020. "Coastal Wind Power in Southern Santa Catarina, Brazil," Energies, MDPI, vol. 13(19), pages 1-23, October.
    18. Alexis T Baria & Brian Maniscalco & Biyu J He, 2017. "Initial-state-dependent, robust, transient neural dynamics encode conscious visual perception," PLOS Computational Biology, Public Library of Science, vol. 13(11), pages 1-29, November.
    19. Matthijs J. Warrens & Bunga C. Pratiwi, 2016. "Kappa Coefficients for Circular Classifications," Journal of Classification, Springer;The Classification Society, vol. 33(3), pages 507-522, October.
    20. Lombard, F. & Hawkins, Douglas M. & Potgieter, Cornelis J., 2017. "Sequential rank CUSUM charts for angular data," Computational Statistics & Data Analysis, Elsevier, vol. 105(C), pages 268-279.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-51338-1. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.