A novel approach for combining task-dependent gamma with alpha and beta power modulation for enhanced identification of eloquent cortical areas using ECoG in patients with medical-refractory epilepsy

Abstract

AbstractElectrical stimulation mapping (ESM) is the gold standard for identification of “eloquent” areas prior to resection of epileptogenic tissue, however, it is time consuming and may cause side effects, especially stimulation-induced seizures and after-discharges. Broadband gamma activity (55 – 200 Hz) recorded with subdural electrocorticography (ECoG) during cognitive tasks has been proposed as an attractive tool for mapping cortical areas with specific function but until now has not proven definitive clinical value. Fewer studies have addressed whether the alpha (8 – 12 Hz) and beta (15 – 25 Hz) band activity could also be used to improve eloquent cortex identification. We compared alpha, beta and broadband gamma activity, and their combination for the identification of eloquent cortical areas defined by ESM. Ten patients participated in a delayed-match-to-sample task, where syllable sounds were matched to visually presented letters and responses given by keyboard. We used a generalized linear model (GLM) approach to find the optimal weighting of low frequency bands and broadband gamma power to predict the ESM categories. Broadband gamma activity increased more in eloquent areas than in non-eloquent areas and this difference had a diagnostic ability (area under (AU) the receiving operating characteristic curve - AUROC) of ∼70%. Both alpha and beta power decreased more in eloquent areas. Alpha power had lower AUROC than broadband gamma while beta had similar AUROC. AUROC was enhanced by the combination of alpha and broadband gamma (3% improvement) and by the combination of beta and broadband gamma (7% improvement) over the use of broadband gamma alone. Further analysis showed that the relative performance of broadband gamma and low frequency bands depended on multiple factors including the time period of the cognitive task, the location of the electrodes and the patient’s attention to the stimulus. However, the combination of beta band and broadband gamma always gave the best performance. We show how ECoG power modulation from cognitive testing periods can be used to map the probability of eloquence by ESM and how this probability can be used as an aid for optimal ESM planning. We conclude that low frequency power during cognitive testing can contribute to the identification of eloquent areas in patients with focal refractory epilepsy improving its precision but does not replace the need of ESM.HighlightsGamma, alpha and beta band activity has significant diagnostic ability to identify ESM defined eloquent cortical areas.We present a novel method to combine gamma and low frequency activity for enhanced identification.We quantify how identification is dependent on analysis time window, cortical function, and patient’s attentional engagement.With further development, this approach may offer an alternative to ESM mapping with reduced burden for patients.