Multiscale Recordings Reveal the Dynamic Spatial Structure of Human Seizures

Overview

Journal Neurobiol Dis

Specialty Neurology

Date 2019 Mar 23

PMID 30898669

Citations 22

Authors

Catherine A Schevon

Steven Tobochnik

Tahra Eissa

Edward Merricks

Brian Gill

R Ryley Parrish

Lisa M Bateman

Guy M McKhann Jr

Ronald G Emerson

Andrew J Trevelyan

Affiliations

Soon will be listed here.

Abstract

The cellular activity underlying human focal seizures, and its relationship to key signatures in the EEG recordings used for therapeutic purposes, has not been well characterized despite many years of investigation both in laboratory and clinical settings. The increasing use of microelectrodes in epilepsy surgery patients has made it possible to apply principles derived from laboratory research to the problem of mapping the spatiotemporal structure of human focal seizures, and characterizing the corresponding EEG signatures. In this review, we describe results from human microelectrode studies, discuss some data interpretation pitfalls, and explain the current understanding of the key mechanisms of ictogenesis and seizure spread.

Citing Articles

A selective small-molecule agonist of G protein-gated inwardly-rectifying potassium channels reduces epileptiform activity in mouse models of tumor-associated and provoked seizures.

Rifkin R, Wu X, Pereira B, Gill B, Merricks E, Michalak A Neuropharmacology. 2024; 265():110259.

PMID: 39662702 PMC: 11726401. DOI: 10.1016/j.neuropharm.2024.110259.

The time-evolving epileptic brain network: concepts, definitions, accomplishments, perspectives.

Brohl T, Rings T, Pukropski J, von Wrede R, Lehnertz K Front Netw Physiol. 2024; 3:1338864.

PMID: 38293249 PMC: 10825060. DOI: 10.3389/fnetp.2023.1338864.

Cell-type specific and multiscale dynamics of human focal seizures in limbic structures.

Agopyan-Miu A, Merricks E, Smith E, McKhann 2nd G, Sheth S, Feldstein N Brain. 2023; 146(12):5209-5223.

PMID: 37536281 PMC: 10689922. DOI: 10.1093/brain/awad262.

Human acute microelectrode array recordings with broad cortical access, single-unit resolution, and parallel behavioral monitoring.

Eisenkolb V, Held L, Utzschmid A, Lin X, Krieg S, Meyer B Cell Rep. 2023; 42(5):112467.

PMID: 37141095 PMC: 10242451. DOI: 10.1016/j.celrep.2023.112467.

Multilayer brain networks can identify the epileptogenic zone and seizure dynamics.

Shahabi H, Nair D, Leahy R Elife. 2023; 12.

PMID: 36929752 PMC: 10065796. DOI: 10.7554/eLife.68531.

References

Powell T, MOUNTCASTLE V . Some aspects of the functional organization of the cortex of the postcentral gyrus of the monkey: a correlation of findings obtained in a single unit analysis with cytoarchitecture. Bull Johns Hopkins Hosp. 1959; 105:133-62. View

Weiss S, Banks G, McKhann Jr G, Goodman R, Emerson R, Trevelyan A . Ictal high frequency oscillations distinguish two types of seizure territories in humans. Brain. 2013; 136(Pt 12):3796-808. PMC: 3859220. DOI: 10.1093/brain/awt276. View

Sloviter R . Decreased hippocampal inhibition and a selective loss of interneurons in experimental epilepsy. Science. 1987; 235(4784):73-6. DOI: 10.1126/science.2879352. View

Zijlmans M, Jacobs J, Kahn Y, Zelmann R, Dubeau F, Gotman J . Ictal and interictal high frequency oscillations in patients with focal epilepsy. Clin Neurophysiol. 2010; 122(4):664-71. PMC: 3771929. DOI: 10.1016/j.clinph.2010.09.021. View

Ziburkus J, Cressman J, Barreto E, Schiff S . Interneuron and pyramidal cell interplay during in vitro seizure-like events. J Neurophysiol. 2006; 95(6):3948-54. PMC: 1469233. DOI: 10.1152/jn.01378.2005. View

Gardner A, Worrell G, Marsh E, Dlugos D, Litt B . Human and automated detection of high-frequency oscillations in clinical intracranial EEG recordings. Clin Neurophysiol. 2007; 118(5):1134-43. PMC: 2020804. DOI: 10.1016/j.clinph.2006.12.019. View

Wilson S, Scheuer M, Plummer C, Young B, Pacia S . Seizure detection: correlation of human experts. Clin Neurophysiol. 2003; 114(11):2156-64. DOI: 10.1016/s1388-2457(03)00212-8. View

Bonini F, McGonigal A, Trebuchon A, Gavaret M, Bartolomei F, Giusiano B . Frontal lobe seizures: from clinical semiology to localization. Epilepsia. 2013; 55(2):264-77. DOI: 10.1111/epi.12490. View

Weiss S, Staba R, Bragin A, Moxon K, Sperling M, Avoli M . "Interneurons and principal cell firing in human limbic areas at focal seizure onset". Neurobiol Dis. 2018; 124:183-188. PMC: 6794098. DOI: 10.1016/j.nbd.2018.11.014. View

10.

van Drongelen W, Koch H, Marcuccilli C, Pena F, Ramirez J . Synchrony levels during evoked seizure-like bursts in mouse neocortical slices. J Neurophysiol. 2003; 90(3):1571-80. DOI: 10.1152/jn.00392.2003. View

11.

Quian Quiroga R, Nadasdy Z, Ben-Shaul Y . Unsupervised spike detection and sorting with wavelets and superparamagnetic clustering. Neural Comput. 2004; 16(8):1661-87. DOI: 10.1162/089976604774201631. View

12.

Dzhala V, Kuchibhotla K, Glykys J, Kahle K, Swiercz W, Feng G . Progressive NKCC1-dependent neuronal chloride accumulation during neonatal seizures. J Neurosci. 2010; 30(35):11745-61. PMC: 3070296. DOI: 10.1523/JNEUROSCI.1769-10.2010. View

13.

Spencer S, Spencer D, Williamson P, Mattson R . The localizing value of depth electroencephalography in 32 patients with refractory epilepsy. Ann Neurol. 1982; 12(3):248-53. DOI: 10.1002/ana.410120306. View

14.

Wilson C, Babb T . Structurally stable burst and synchronized firing in human amygdala neurons: auto- and cross-correlation analyses in temporal lobe epilepsy. Epilepsy Res. 1987; 1(1):17-34. DOI: 10.1016/0920-1211(87)90047-7. View

15.

Schevon C, Weiss S, McKhann Jr G, Goodman R, Yuste R, Emerson R . Evidence of an inhibitory restraint of seizure activity in humans. Nat Commun. 2012; 3:1060. PMC: 3658011. DOI: 10.1038/ncomms2056. View

16.

Alfonsa H, Merricks E, Codadu N, Cunningham M, Deisseroth K, Racca C . The contribution of raised intraneuronal chloride to epileptic network activity. J Neurosci. 2015; 35(20):7715-26. PMC: 4438123. DOI: 10.1523/JNEUROSCI.4105-14.2015. View

17.

Meijer H, Eissa T, Kiewiet B, Neuman J, Schevon C, Emerson R . Modeling focal epileptic activity in the Wilson-cowan model with depolarization block. J Math Neurosci. 2015; 5:7. PMC: 4385301. DOI: 10.1186/s13408-015-0019-4. View

18.

Rosenow F, Luders H . Presurgical evaluation of epilepsy. Brain. 2001; 124(Pt 9):1683-700. DOI: 10.1093/brain/124.9.1683. View

19.

Eissa T, Tryba A, Marcuccilli C, Ben-Mabrouk F, Smith E, Lew S . Multiscale Aspects of Generation of High-Gamma Activity during Seizures in Human Neocortex. eNeuro. 2016; 3(2). PMC: 4876490. DOI: 10.1523/ENEURO.0141-15.2016. View

20.

Ellender T, Raimondo J, Irkle A, Lamsa K, Akerman C . Excitatory effects of parvalbumin-expressing interneurons maintain hippocampal epileptiform activity via synchronous afterdischarges. J Neurosci. 2014; 34(46):15208-22. PMC: 4228130. DOI: 10.1523/JNEUROSCI.1747-14.2014. View