Spatiotemporal Dynamics in Pre-speech Semantic Category Decoding: An intracranial EEG Study.

Despite major advances in brain-computer interfaces (BCIs), decoding high-level language representations prior to speech remains challenging. While prior efforts have primarily focused on acoustic or articulatory features, how semantic categories are decoded in time and space remains unclear. Here, we investigated how semantic representations unfold over time by analyzing high-gamma (HG, 70–170 Hz) electrocorticography (ECoG) signals from twenty subjects (7 females and 13 males) performing a word-reading task involving body- and non-body-related words. HG activity was examined from word presentation to 500 ms, capturing the pre-speech window. Group-level time-resolved decoding, pooling features across subjects within each Brodmann area (BA), revealed significant classification accuracy above chance in both hemispheres (p<0.05, FDR-corrected). In the left hemisphere, peak-performing BAs followed a frontal–temporal–occipital–parietal cascade: dorsolateral prefrontal cortex (dlPFC) (50 ms), inferior temporal and fusiform gyri (350–400 ms), and supramarginal gyrus (SMG) (500 ms). In contrast, the right hemisphere exhibited an occipital–temporal–frontal–temporal–parietal sequence: visual and temporal pole (TP) regions (50–100 ms), dlPFC (200 ms), fusiform gyrus (FG) (400 ms), and angular gyrus (450 ms). This progression contrasts with the frontal-initiated cascade of the left hemisphere, underscoring hemispheric differences in the timing of peak decoding loci. Cross-temporal regression revealed predictive interregional engagement. In the left hemisphere, early dlPFC activity (0–150 ms) predicted later SMG responses (300–350 ms). In the right, a strong but brief predictive link emerged from the TP to the angular gyrus (200–300 ms; peak R² ≈ 0.70). These findings demonstrate that semantic category decoding relies on temporally structured interregional interactions, revealing distinct hemispheric patterns. Significance statement This study investigates spatiotemporal dynamics in decoding semantic categories during the pre-speech interval using high-resolution intracranial EEG. We reveal a left-hemisphere cascade beginning in frontal areas and extending to temporal, occipital, and parietal regions, and a distinct right-hemisphere cascade involving early occipital and temporal pole activity. Cross-temporal regression reveals sustained left-lateral predictive temporal pattern and a brief but high-precision right-hemisphere link. These findings advance our understanding of how semantic categories are constructed in the brain over time and may inform future efforts to develop neural decoding frameworks that operate before speech output.