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. 2023 Jun;64(6):1527-1540.
doi: 10.1111/epi.17575. Epub 2023 Mar 17.

Comparing electrical stimulation functional mapping with subdural electrodes and stereoelectroencephalography

Gewalin Aungaroon  1   2 , Kishore Vedala  1 , Anna W Byars  1   2 , Brian Ervin  1   3 , Leonid Rozhkov  1 , Paul S Horn  1   2 , S K Z Ihnen  1   2 , Katherine D Holland  1   2 , Jeffrey R Tenney  1   2 , Kelly Kremer  1   2 , Susan L Fong  1   2 , Nan Lin  1   2 , Wei Liu  1   2 , Todd M Arthur  1   2 , Hisako Fujiwara  1   2 , Jesse Skoch  2   4 , James L Leach  2   5 , Francesco T Mangano  2   4 , Hansel M Greiner  1   2 , Ravindra Arya  1   2   3
Affiliations

Comparing electrical stimulation functional mapping with subdural electrodes and stereoelectroencephalography

Gewalin Aungaroon et al. Epilepsia. 2023 Jun.

Abstract

Objective: Electrical stimulation mapping (ESM) is the clinical standard for functional localization with subdural electrodes (SDE). As stereoelectroencephalography (SEEG) has emerged as an alternative option, we compared functional responses, afterdischarges (ADs), and unwanted ESM-induced seizures (EISs) between the two electrode types.

Methods: Incidence and current thresholds for functional responses (sensory, motor, speech/language), ADs, and EISs were compared between SDE and SEEG using mixed models incorporating relevant covariates.

Results: We identified 67 SEEG ESM and 106 SDE ESM patients (7207 and 4980 stimulated contacts, respectively). We found similar incidence of language and motor responses between electrode types; however, more SEEG patients reported sensory responses. ADs and EISs occurred less commonly with SEEG than SDE. Current thresholds for language, face motor, and upper extremity (UE) motor responses and EIS significantly decreased with age. However, they were not affected by electrode type, premedication, or dominant hemispheric stimulation. AD thresholds were higher with SEEG than with SDE. For SEEG ESM, language thresholds remained below AD thresholds up to 26 years of age, whereas this relationship was inverse for SDE. Also, face and UE motor thresholds fell below AD thresholds at earlier ages for SEEG than SDE. AD and EIS thresholds were not affected by premedication.

Significance: SEEG and SDE have clinically relevant differences for functional brain mapping with electrical stimulation. Although evaluation of language and motor regions is comparable between SEEG and SDE, SEEG offers a higher likelihood of identifying sensory areas. A lower incidence of ADs and EISs, and a favorable relationship between functional and AD thresholds suggest superior safety and neurophysiologic validity for SEEG ESM than SDE ESM.

Keywords: drug-resistant epilepsy; functional brain mapping intracranial EEG.

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Conflict of interest statement

RA receives research support from NIH NINDS R01 NS115929 and Cincinnati Children’s Research Foundation (Research Innovation Project Grant). None of the other authors have any relevant potential conflicts of interest to report.

Figures

Figure 1.
Figure 1.. Incidence of functional responses.
The proportion of patients (top panel) and stimulated contacts (bottom panel) with different functional responses are shown for SEEG and SDE electrical stimulation. Abbreviations: SDE subdural electrodes, SEEG stereo-electroencephalography
Figure 2.
Figure 2.. Contribution of random effect of each patient in the relationship between language (A) or motor (B) thresholds and age.
Each horizontal line shows the magnitude of random effect (z-score) for an individual patient. Note that SEEG shows high between-subject heterogeneity (non-overlapping error bars) but low within-subject heterogeneity (tighter error bars), whereas SDE has low between-subject heterogeneity but high within-subject heterogeneity. Higher heterogeneity seen in motor thresholds (z-scores on x-axis) is probably partly due to inclusion of disparate motor responses (face, upper extremity, and lower extremity) in this analysis. Abbreviations: SDE subdural electrodes, SEEG stereo-electroencephalography
Figure 3.
Figure 3.. Language, motor, and AD thresholds as functional of age.
Language (blue) thresholds remain below AD (red) thresholds for SEEG ESM for most of the age range whereas the relationship is inverse for SDE ESM. UE motor (dark green) thresholds remain below AD thresholds (red) throughout the age range for SEEG ESM, whereas they fall below AD thresholds (red) at 7.4 years-of-age for SDE ESM. Face motor thresholds (light green) also fall below AD thresholds (red) at an earlier age for SEEG ESM compared to SDE ESM. Although the data was analyzed with mixed models, ordinary least square lines are shown for convenience. For SEEG graph showing language thresholds, the number of data points for age>24 years is small (wide confidence interval band) and should be interpreted with caution. Abbreviations: AD after-discharges, ESM electrical stimulation mapping, SDE subdural electrodes, SEEG stereo-electroencephalography
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