Spike-phase coupling of subthalamic neurons to posterior perisylvian cortex predicts speech sound accuracy

Speech provides a rich context for understanding how cortical interactions with the basal ganglia contribute to unique human behaviors, but opportunities for direct human intracranial recordings across cortical-basal ganglia networks are rare. Here we have recorded electrocorticographic signals in the cortex synchronously with single units in the basal ganglia during awake neurosurgeries where participants spoke syllable repetitions. We have discovered that individual subthalamic nucleus (STN) neurons have transient (200 ms) spike-phase coupling (SPC) events with multiple cortical regions. The spike timing of STN neurons is locked to the phase of theta-alpha oscillations in the supramarginal and posterior superior temporal gyrus during speech planning and production. Speech sound errors occur when this STN-cortical interaction is delayed. Our results suggest that timely interactions between the STN and the posterior perisylvian cortex support auditory-motor coordinate transformation or phonological working memory during speech planning. These findings establish a framework for understanding cortical-basal ganglia interaction in other human behaviors, and additionally indicate that firing-rate based models are insufficient for explaining basal ganglia circuit behavior.