Behavior-iEEG-Spectral-Power-Correlation: Defining Neural Substrates of Naturalistic Behavior.

Abstract

Intracranial language localization with electrical stimulation mapping (ESM) and high-gamma modulation (HGM) mapping relies on artificial, repetitive tasks, requiring sustained cooperation from patients. Herein, we tested the validity of unstructured, interpersonal, naturalistic conversation for language localization, using a novel methodology: Behavior-iEEG-Spectral-Power correlation (BESPoC). We first validated BESPoC against ESM, HGM, and neuropsychological outcomes using well-established language tasks, then demonstrated the validity of naturalistic conversation. We included 134 patients (59 females), aged 2-29 years, undergoing standard-of-care stereo-electroencephalography monitoring who engaged in picture naming, auditory naming, story listening, and conversed with a family member. ESM and HGM analysis were performed using established methods. BESPoC methodology quantified correlation between stereo-electroencephalography spectral power from task recordings, obviating the need for any trial-based epochs, and behavioral markers. The large sample size allowed mixed-effects modeling to compare BESPoC with HGM and ESM. BESPoC showed high specificity (0.79-0.83) and sensitivity (0.64-0.86) for localizing HGM language sites across the tasks. BESPoC also compared well with HGM across all language tasks for localizing ESM speech/language sites. With conventional tasks, BESPoC was superior to HGM for modeling neuropsychological deficits seen, despite preserving ESM speech/language sites. Naturalistic conversation compared well with standard tasks for localization of HGM and ESM language sites, and determined neuropsychological outcomes better than conventional tasks. Using BESPoC methodology naturalistic conversation is shown to produce valid cortical language maps of both expressive and receptive language, and determine neuropsychological outcomes after epilepsy surgery. ANN NEUROL 2025;98:1096-1110.