Cortical stimulation predicts language decline following SEEG radiofrequency thermocoagulation

Stereo-EEG (SEEG) cortical stimulation enables individualized mapping of language networks. Regions associated with induced language deficits are marked as 'language-positive' and considered important in supporting function. It remains unclear, however, whether small lesions in 'language-positive' sites created by radiofrequency thermocoagulation are sufficient to cause language deficits. Thirty-six consecutive SEEG patients with drug-resistant focal epilepsy were prospectively recruited from two Australian epilepsy centres. Formal language assessment was undertaken before and 3 months after radiofrequency thermocoagulation [mean = 106.92 days, standard deviation (SD) = 27.83], which included the Boston Naming Test, Auditory Naming Test and semantic fluency task. During high-frequency (50 Hz) cortical stimulation, language was assessed in vivo using visual and auditory naming, reading, spontaneous speech and/or counting tasks. To evaluate group changes post radiofrequency thermocoagulation, paired sample t-tests were undertaken. Reliable change indices were calculated to classify language decline, and independent samples t-tests or χ2 tests were then used to compare groups on selected clinical and demographic variables. Of the 36 patients (mean = 36.19 years old, SD = 9.22 years, range = 17-56 years, 56% female), 14 (39%) had a language-dominant epileptogenic zone (EZ), 18 (50%) a non-dominant EZ and 4 (11%) a bilateral EZ. A mean of 12.28 (SD = 6.84, range = 2-29) coagulation sites were undertaken per patient. Language decline was associated with radiofrequency thermocoagulation of a language-positive site [χ12 = 6.94, P = 0.008, moderate effect size odds ratio = 10.00, 95% confidence interval (1.68, 59.31)]; specifically, 63% (5/8) of patients with radiofrequency thermocoagulation of a language-positive site experienced a language decline, compared with only 11% (3/28) who declined following radiofrequency thermocoagulation of language-negative sites. The likelihood of language decline was increased by 10-fold when radiofrequency thermocoagulation included a language-positive site/s compared with patients in whom no language-positive sites were coagulated. In contrast, decline was not associated with age at radiofrequency thermocoagulation, age at epilepsy diagnosis, premorbid intellectual function, number of coagulation sites or radiofrequency thermocoagulation within the dominant hemisphere. This study shows that small nodes within language networks can be essential to support function. Moreover, the premorbid integrity or 'functional adequacy' of cognitive networks might determine the capacity to compensate effectively for radiofrequency thermocoagulation of language-positive sites. These findings reveal new intricacies to network organization of cognitive functions in epilepsy and highlight the clinical advantages of language mapping for identifying patients at risk of decline following radiofrequency thermocoagulation.