Lateralization and time-course of cortical phonological representations during syllable production.

Spoken language contains information at a broad range of timescales, from phonetic distinctions on the order of milliseconds to semantic contexts which shift over seconds to minutes. It is not well understood how the brain's speech production systems combine features at these timescales into a coherent vocal output. We investigated the spatial and temporal representations in cerebral cortex of three phonological units with different durations: consonants, vowels, and syllables. Electrocorticography recordings were obtained from five participants while speaking single syllables. We developed a novel clustering and Kalman filter-based trend analysis procedure to sort electrodes into temporal response profiles. A linear discriminant classifier was used to determine how strongly each electrode's response encoded phonological features. We found distinct time-courses of encoding phonological units depending on their duration: consonants were represented more during speech preparation, vowels were represented evenly throughout trials, and syllables during production. Locations of strongly speech-encoding electrodes (the top 30% of electrodes) likewise depended on phonological element duration, with consonant-encoding electrodes left-lateralized, vowel-encoding hemispherically balanced, and syllable-encoding right-lateralized. The lateralization of speech-encoding electrodes depended on onset time, with electrodes active before or after speech production favoring left hemisphere and those active during speech favoring the right. Single-electrode speech classification revealed cortical areas with preferential encoding of particular phonemic elements, including consonant encoding in the left precentral and postcentral gyri and syllable encoding in the right middle frontal gyrus. Our findings support neurolinguistic theories of left hemisphere specialization for processing short-timescale linguistic units and right hemisphere processing of longer-duration units. Significance Statement Articulating speech requires control and monitoring of motor outputs that change at timescales ranging from milliseconds to whole sentences. During syllable repetition, we examined how the neural processing of differently-sized speech units is distributed in the brain and across different stages of the task. Using direct electrical recordings from human cerebral cortex, we found that larger linguistic units (syllables) are represented more in the right hemisphere while shorter linguistic units (consonants) are represented more in the left hemisphere. Across time, syllables were represented during vocal output, while consonants were represented during speech preparation and after production. These results indicate a hemispheric specialization for distinct sizes of phonological units and that these units are processed at specific timepoints during speech.