Supplementary motor area in speech initiation: a large-scale intracranial EEG evaluation of stereotyped word articulation

Abstract

Speech production is known to engage a distributed network. The brain regions responsible for the initiation of articulation are unclear, and they would be expected to coordinate a distributed network. Using direct intracranial recordings in a large cohort, during stereotyped speech production to eliminate confounds of phonological and semantic complexity, we performed a comprehensive analysis of cortical sites engaged in speech initiation. We found that the supplementary motor area (SMA) was the earliest speech motor region to be active prior to speech onset and was active almost exclusively prior to articulation. Broadband gamma activity in the SMA was predictive of the response time of word production, predicting response time from 250 ms after stimulus onset. Neural activity in SMA began at a highly predictable time after stimulus onset and extended until speech onset. SMA activity offset coincided with ventral premotor cortex and primary motor activity onset. This suggests that the SMA may coordinate the concerted activation of motor execution cortex. Our results support the idea that SMA is a key node in the speech initiation network. Significance statementProducing speech requires coordination across multiple brain regions. One cortical region - the supplementary motor area (SMA) - has long been a candidate region to coordinate across other regions to initiate speech production. In this study, we used human intracranial recordings from patients with epilepsy to investigate the role of the SMA in initiating speech. In a picture-naming task, subjects repeated the word "scrambled" scores of times; using this condition to eliminate any linguistic confounds, we found that the SMA was consistently one of the earliest regions to activate during word production. We also uncovered the SMAs temporally precise tuning to speech onset at the single-trial level.