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Research ArticleResearch Article: New Research, Disorders of the Nervous System

A Computational Biomarker of Photosensitive Epilepsy from Interictal EEG

Marinho A. Lopes, Sanchita Bhatia, Glen Brimble, Jiaxiang Zhang and Khalid Hamandi
eNeuro 31 May 2022, 9 (3) ENEURO.0486-21.2022; DOI: https://doi.org/10.1523/ENEURO.0486-21.2022
Marinho A. Lopes
1Cardiff University Brain Research Imaging Centre, School of Psychology, Cardiff University, Cardiff CF24 4HQ, United Kingdom
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  • ORCID record for Marinho A. Lopes
Sanchita Bhatia
1Cardiff University Brain Research Imaging Centre, School of Psychology, Cardiff University, Cardiff CF24 4HQ, United Kingdom
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Glen Brimble
2Department of Clinical Neurophysiology, University Hospital of Wales, Cardiff CF14 4XW, United Kingdom
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Jiaxiang Zhang
1Cardiff University Brain Research Imaging Centre, School of Psychology, Cardiff University, Cardiff CF24 4HQ, United Kingdom
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Khalid Hamandi
1Cardiff University Brain Research Imaging Centre, School of Psychology, Cardiff University, Cardiff CF24 4HQ, United Kingdom
3The Welsh Epilepsy Unit, Department of Neurology, University Hospital of Wales, Cardiff CF14 4XW, United Kingdom
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  • Figure 1.
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    Figure 1.

    Summary of our computational method. We used interictal scalp EEG to infer functional networks. Then, to interrogate the networks, we considered a computational model of ictogenicity to simulate seizure-like activity on the functional networks. This allowed us to assess the propensity of a functional network to generate seizures in silico, the BNI. It further enabled us to measure the NI (i.e., the effect of removing a node on the BNI), which represents the local ictogenic propensity.

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    Figure 2.

    Violin plot of BNI comparing the PPR and non-PPR groups. The white dot represents the median, the black box represents the interquartile range, and the other dots within the shaded region correspond to the BNI of each individual. The BNI values are not statistically higher in the PPR group than in the non-PPR group (p = 0.89, one-sided Mann–Whitney U test).

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    Figure 3.

    NI of the occipital lobe nodes in the PPR and non-PPR groups. The NI values in the O2 region are statistically significantly higher in the PPR group than in the non-PPR group. The p-values correspond to one-sided Mann–Whitney U tests corrected with the Bonferroni–Holm procedure.

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    Figure 4.

    NI of all the network nodes in the PPR and non-PPR groups. This figure excludes the nodes corresponding to the occipital lobe nodes (presented in Fig. 3). p-Values, effect sizes, and confidence intervals are presented in Table 3. All these differences in NI are not statistically significant.

Tables

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    Table 1

    Demographics and clinical information of the group of individuals that presented PPR on EEG

    IDAge (years)GenderSyndromeMedication
    PPR124MJMELamotrigine
    PPR216MGTCSONone
    PPR315MGTSOValproate
    PPR413FJAENone
    PPR515FJAELevetiracetam,
    lamotrigine
    PPR613FJMENone
    PPR716FJMELamotrigine
    PPR817FJMELamotrigine
    PPR919FJAEClobazam
    PPR1018MGTCSONone
    PPR1116FGTCSOLevetiracetam
    PPR1217FJMELevetiracetam
    PPR1313FJMENone
    PPR1424FJMEValproate
    PPR1519FGTCSONone
    PPR1622FGTCSONone
    PPR1714FJMENone
    PPR1831FJMENone
    PPR1918MJMENone
    PPR2023FGTCSOLevetiracetam
    PPR2119MGTCSOValproate
    PPR2223FGTCSOSertraline
    PPR2326MJMEValproate, zonisamide
    PPR2413FJMENone
    PPR2514FGTCSONone
    PPR2613FJAENone
    • M, Male; F, female; GTCSO, generalized tonic-clonic seizures only.

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    Table 2

    Demographics and clinical information of the group of individuals that did not show a PPR on EEG

    IDAge (years)GenderSyndromeMedication
    Non-PPR116MJMENone
    Non-PPR228FJMEValproate
    Non-PPR330MJMEValproate
    Non-PPR419MJMENone
    Non-PPR524FJMELevetiracetam
    Non-PPR618MJMEEpilim
    Non-PPR719MJMENone
    Non-PPR827FJMEValproate
    Non-PPR920FJMELamotrigine
    Non-PPR1018MJMENone
    Non-PPR1118FJMENone
    Non-PPR1222FJMEDuloxetine
    Non-PPR1322FJMELamotrigine, carbamazepine
    Non-PPR1423MJMENone
    Non-PPR1521FJMETopiramate, levetiracetam, clobazam
    Non-PPR1630MGTCSOCarbamazepine
    Non-PPR1720FJMEEpilim
    Non-PPR1820FJMENone
    Non-PPR1920MJMEValproate
    Non-PPR2031FJMELamotrigine, Sumatriptan
    • M, Male; F, female; GTCSO, generalized tonic-clonic seizures only.

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    Table 3

    Assessment of NI differences between the two groups in each node (as presented in Fig. 4)

    NodeUncorrected p-valueCorrected p-valueU statisticzEffect sizeCI lower limitCI upper limit
    C30.541583−0.6−0.016−0.0480.025
    C40.351568−0.94−0.026−0.0600.011
    CZ0.591586−0.54−0.002−0.0570.046
    F30.651590−0.45−0.019−0.0680.029
    F40.731595−0.34−0.020−0.0720.031
    F70.6316330.480.068−0.0240.124
    F80.5616380.590.038−0.0140.073
    FP10.471578−0.72−0.014−0.0640.050
    FP20.941607−0.080.015−0.0270.058
    FPZ0.7516260.320.045−0.0720.179
    FZ0.791599−0.25−0.006−0.0560.050
    P30.2916591.050.067−0.0010.121
    P40.3516530.920.022−0.0450.106
    PZ0.2916591.050.024−0.0320.096
    T30.6016350.520.010−0.0460.051
    T40.0816891.720.042−0.0020.079
    T50.851602−0.19−0.004−0.0570.057
    T60.261560−1.12−0.015−0.0510.031
    • The p-values, U statistics, and z-scores correspond to two-sided Mann–Whitney U tests assessing whether NI is different between the two groups at a given node. The p-values were corrected using the Bonferroni–Holm procedure, and none is significant. The effect size (median difference of NI) and confidence intervals further show that there are no statistical differences between the groups in any of these nodes.

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    Table 4

    Assessment of relative power and connectivity differences on occipital electrodes between the PPR and non-PPR groups

    MeasureNodeUncorrected p-valueU statisticz-scoreEffect sizeCI lower limitCI upper limit
    Relative low alpha powerO10.79575−0.81−0.028−0.0950.047
    O20.74582−0.65−0.013−0.0890.049
    Relative alpha powerO10.86562−1.10−0.078−0.130.049
    O20.80573−0.85−0.039−0.140.041
    Occipital connectivityO10.94543−1.52−0.76−2.180.48
    O20.76580−0.70−0.34−2.181.17
    • The relative power was computed following the methods of Vaudano et al. (2017). We considered the following two frequency bands: low alpha power (6–9 Hz) as in the main analysis; and alpha power (7.5–12.5 Hz) as in the study by Vaudano et al. (2017). The occipital connectivity corresponds to the connection strength of the electrodes (i.e., sum of in-strength and out-strength; Rubinov and Sporns, 2010). The p-values, U statistics, and z-scores correspond to one-sided Mann–Whitney U tests assessing whether the relative power (or connectivity strength) is higher in the PPR group relative to the non-PPR group at a given occipital electrode. All p-values are not significant. The effect size (median difference) and confidence intervals further show that there are no statistical differences between the groups when using these measures.

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A Computational Biomarker of Photosensitive Epilepsy from Interictal EEG
Marinho A. Lopes, Sanchita Bhatia, Glen Brimble, Jiaxiang Zhang, Khalid Hamandi
eNeuro 31 May 2022, 9 (3) ENEURO.0486-21.2022; DOI: 10.1523/ENEURO.0486-21.2022

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A Computational Biomarker of Photosensitive Epilepsy from Interictal EEG
Marinho A. Lopes, Sanchita Bhatia, Glen Brimble, Jiaxiang Zhang, Khalid Hamandi
eNeuro 31 May 2022, 9 (3) ENEURO.0486-21.2022; DOI: 10.1523/ENEURO.0486-21.2022
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Keywords

  • functional network
  • hyperexcitability
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