Speech induces spatiotemporal and frequency specific subthalamic-cortical spike-phase coupling events

Speaking evokes modulation of neuronal activity in the subthalamic nucleus (STN), a basal ganglia node that receives both mono- and polysynaptic inputs from cortex and subcortex. Indeed, speech provides a rich context for exploring interactions within human cortical-basal ganglia circuits, but direct intracranial recordings are rare. Here, we synchronously recorded electrocorticographic signals in the cortex and single units in the STN while participants performed a syllable repetition task during deep brain stimulation (DBS) surgery. STN neurons exhibited transient spike-phase coupling with frequency and spatiotemporal specificity. Theta and alpha spike-phase coupling was prominent in the superior temporal gyrus and supramarginal gyrus during speech production. Beta spike-phase coupling was prominent in some STN neurons during baseline but rebounded after speech termination in a separate population. Thus, STN-cortical interactions are coordinated via transient bursts of behavior-specific synchronization that involves multiple neuronal populations and timescales, suggesting mechanisms for auditory-sensorimotor integration during speech production.