Ictal networks of temporal lobe epilepsy: views from high-frequency oscillations in stereoelectroencephalography

Restricted access

OBJECTIVE

In this study, the authors investigated high-frequency oscillation (HFO) networks during seizures in order to determine how HFOs spread from the focal cerebral cortex and become synchronized across various areas of the brain.

METHODS

All data were obtained from stereoelectroencephalography (SEEG) signals in patients with drug-resistant temporal lobe epilepsy (TLE). The authors calculated intercontact cross-coefficients between all pairs of contacts to construct HFO networks in 20 seizures that occurred in 5 patients. They then calculated HFO network topology metrics (i.e., network density and component size) after normalizing seizure duration data by dividing each seizure into 10 intervals of equal length (labeled I1–I10).

RESULTS

From the perspective of the dynamic topologies of cortical and subcortical HFO networks, the authors observed a significant increase in network density during intervals I5–I10. A significant increase was also observed in overall energy during intervals I3–I8. The results of subnetwork analysis revealed that the number of components continuously decreased following the onset of seizures, and those results were statistically significant during intervals I3–I10. Furthermore, the majority of nodes were connected to a single dominant component during the propagation of seizures, and the percentage of nodes within the largest component grew significantly until seizure termination.

CONCLUSIONS

The consistent topological changes that the authors observed suggest that TLE is affected by common epileptogenic patterns. Indeed, the findings help to elucidate the epileptogenic network that characterizes TLE, which may be of interest to researchers and physicians working to improve treatment modalities for epilepsy, including resection, cortical stimulation, and neuromodulation treatments that are responsive to network topologies.

ABBREVIATIONS EEG = electroencephalography; EZ = epileptogenic zone; iEEG = invasive EEG; HFO = high-frequency oscillation; SEEG = stereoelectroencephalography; TLE = temporal lobe epilepsy.
Article Information

Contributor Notes

Correspondence Cheng-Chia Lee: Neurological Institute, Taipei Veterans General Hospital, Taipei, Taiwan. yfnaughty@gmail.com.INCLUDE WHEN CITING Published online November 30, 2018; DOI: 10.3171/2018.6.JNS172844.Disclosures The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

© AANS, except where prohibited by US copyright law.

Headings
References
  • 1

    Bartolomei FChauvel PWendling F: Epileptogenicity of brain structures in human temporal lobe epilepsy: a quantified study from intracerebral EEG. Brain 131:181818302008

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2

    Bartolomei FLagarde SWendling FMcGonigal AJirsa VGuye M: Defining epileptogenic networks: Contribution of SEEG and signal analysis. Epilepsia 58:113111472017

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3

    Bartolomei FWendling FBellanger JJRégis JChauvel P: Neural networks involving the medial temporal structures in temporal lobe epilepsy. Clin Neurophysiol 112:174617602001

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4

    Bikson MFox JEJefferys JG: Neuronal aggregate formation underlies spatiotemporal dynamics of nonsynaptic seizure initiation. J Neurophysiol 89:233023332003

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5

    Bragin AEngel J JrWilson CLFried IBuzsáki G: High-frequency oscillations in human brain. Hippocampus 9:1371421999

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6

    Cossu MCardinale FCastana LCitterio AFrancione STassi L: Stereoelectroencephalography in the presurgical evaluation of focal epilepsy: a retrospective analysis of 215 procedures. Neurosurgery 57:7067182005

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7

    Cotic MZalay OCChinvarun Ydel Campo MCarlen PLBardakjian BL: Mapping the coherence of ictal high frequency oscillations in human extratemporal lobe epilepsy. Epilepsia 56:3934022015

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8

    Dale AMFischl BSereno MI: Cortical surface-based analysis. I. Segmentation and surface reconstruction. Neuroimage 9:1791941999

  • 9

    Gnatkovsky VFrancione SCardinale FMai RTassi LLo Russo G: Identification of reproducible ictal patterns based on quantified frequency analysis of intracranial EEG signals. Epilepsia 52:4774882011

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10

    Gonzalez-Martinez JA: The stereo-electroencephalography: the epileptogenic zone. J Clin Neurophysiol 33:5225292016

  • 11

    Gotman JLevtova V: Amygdala-hippocampus relationships in temporal lobe seizures: a phase-coherence study. Epilepsy Res 25:51571996

  • 12

    Jacobs JLeVan PChander RHall JDubeau FGotman J: Interictal high-frequency oscillations (80-500 Hz) are an indicator of seizure onset areas independent of spikes in the human epileptic brain. Epilepsia 49:189319072008

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13

    Jacobs JZijlmans MZelmann RChatillon CEHall JOlivier A: High-frequency electroencephalographic oscillations correlate with outcome of epilepsy surgery. Ann Neurol 67:2092202010

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14

    Jirsch JDUrrestarazu ELeVan POlivier ADubeau FGotman J: High-frequency oscillations during human focal seizures. Brain 129:159316082006

  • 15

    Jiruska PAlvarado-Rojas CSchevon CAStaba RStacey WWendling F: Update on the mechanisms and roles of high-frequency oscillations in seizures and epileptic disorders. Epilepsia 58:133013392017

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16

    Jiruska PCsicsvari JPowell ADFox JEChang WCVreugdenhil M: High-frequency network activity, global increase in neuronal activity, and synchrony expansion precede epileptic seizures in vitro. J Neurosci 30:569057012010

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17

    Jiruska PPowell ADChang WCJefferys JG: Electrographic high-frequency activity and epilepsy. Epilepsy Res 89:60652010

  • 18

    Kolaczyk ED: Statistical Analysis of Network Data: Methods and Models. New York: Springer2009

    • PubMed
    • Export Citation
  • 19

    Kramer MAEden UTCash SSKolaczyk ED: Network inference with confidence from multivariate time series. Phys Rev E Stat Nonlin Soft Matter Phys 79:0619162009

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20

    Kramer MAEden UTKolaczyk EDZepeda REskandar ENCash SS: Coalescence and fragmentation of cortical networks during focal seizures. J Neurosci 30:10076100852010

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21

    Lévesque MSalami PGotman JAvoli M: Two seizure-onset types reveal specific patterns of high-frequency oscillations in a model of temporal lobe epilepsy. J Neurosci 32:13264132722012

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 22

    Molaee-Ardekani BBenquet PBartolomei FWendling F: Computational modeling of high-frequency oscillations at the onset of neocortical partial seizures: from ‘altered structure’ to ‘dysfunction’. Neuroimage 52:110911222010

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23

    Morimoto KFahnestock MRacine RJ: Kindling and status epilepticus models of epilepsy: rewiring the brain. Prog Neurobiol 73:1602004

  • 24

    Morrell M: Brain stimulation for epilepsy: can scheduled or responsive neurostimulation stop seizures? Curr Opin Neurol 19:1641682006

  • 25

    Newman M: The structure and function of complex networks. SIAM Rev 45:1672562003

  • 26

    Pail MŘehulka PCimbálník JDoležalová IChrastina JBrázdil M: Frequency-independent characteristics of high-frequency oscillations in epileptic and non-epileptic regions. Clin Neurophysiol 128:1061142017

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27

    Perucca PDubeau FGotman J: Intracranial electroencephalographic seizure-onset patterns: effect of underlying pathology. Brain 137:1831962014

  • 28

    Schiff SJColella DJacyna GMHughes ECreekmore JWMarshall A: Brain chirps: spectrographic signatures of epileptic seizures. Clin Neurophysiol 111:9539582000

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29

    Talairach JBancaud JSzikla GBonis AGeier SVedrenne C: [New approach to the neurosurgery of epilepsy. Stereotaxic methodology and therapeutic results. 1. Introduction and history.] Neurochirurgie 20 (Suppl 1):12401974 (Fr)

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30

    Wasserman SFaust K: Social Network Analysis: Methods and Applications. Cambridge, UK: Cambridge University Press1994

    • Export Citation
  • 31

    Weiss SAAlvarado-Rojas CBragin ABehnke EFields TFried I: Ictal onset patterns of local field potentials, high frequency oscillations, and unit activity in human mesial temporal lobe epilepsy. Epilepsia 57:1111212016

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32

    Wendling FBartolomei FBellanger JJBourien JChauvel P: Epileptic fast intracerebral EEG activity: evidence for spatial decorrelation at seizure onset. Brain 126:144914592003

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33

    Worrell GAParish LCranstoun SDJonas RBaltuch GLitt B: High-frequency oscillations and seizure generation in neocortical epilepsy. Brain 127:149615062004

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 34

    Wu JYSankar RLerner JTMatsumoto JHVinters HVMathern GW: Removing interictal fast ripples on electrocorticography linked with seizure freedom in children. Neurology 75:168616942010

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 35

    Zijlmans MJiruska PZelmann RLeijten FSJefferys JGGotman J: High-frequency oscillations as a new biomarker in epilepsy. Ann Neurol 71:1691782012

  • 36

    Zweiphenning WJvan ’t Klooster MAvan Diessen Evan Klink NEHuiskamp GJGebbink TA: High frequency oscillations and high frequency functional network characteristics in the intraoperative electrocorticogram in epilepsy. Neuroimage Clin 12:9289392016

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
TrendMD
Metrics

Metrics

All Time Past Year Past 30 Days
Abstract Views 82 82 82
Full Text Views 182 182 182
PDF Downloads 47 47 47
EPUB Downloads 0 0 0
PubMed
Google Scholar