Brain network dynamics in the human articulatory loop

•Intracranial electrocorticography showed that tone sounds elicit early high-gamma (HG) augmentation in the precentral gyrus.•Stimulation of precentral HG sites in either hemisphere impairs vocalization.•Connectivity analyses reveal dynamic, reciprocal interactions across the articulatory loop network.

ObjectiveThe articulatory loop is a fundamental component of language function, involved in the short-term buffer of auditory information followed by its vocal reproduction. We characterized the network dynamics of the human articulatory loop, using invasive recording and stimulation.MethodsWe measured high-gamma activity70-110 Hz recorded intracranially when patients with epilepsy either only listened to, or listened to and then reproduced two successive tones by humming. We also conducted network analyses, and analyzed behavioral responses to cortical stimulation.ResultsPresentation of the initial tone elicited high-gamma augmentation bilaterally in the superior-temporal gyrus (STG) within 40 ms, and in the precentral and inferior-frontal gyri (PCG and IFG) within 160 ms after sound onset. During presentation of the second tone, high-gamma augmentation was reduced in STG but enhanced in IFG. The task requiring tone reproduction further enhanced high-gamma augmentation in PCG during and after sound presentation. Event-related causality (ERC) analysis revealed dominant flows within STG immediately after sound onset, followed by reciprocal interactions involving PCG and IFG. Measurement of cortico-cortical evoked-potentials (CCEPs) confirmed connectivity between distant high-gamma sites in the articulatory loop. High-frequency stimulation of precentral high-gamma sites in either hemisphere induced speech arrest, inability to control vocalization, or forced vocalization. Vocalization of tones was accompanied by high-gamma augmentation over larger extents of PCG.ConclusionsBilateral PCG rapidly and directly receives feed-forward signals from STG, and may promptly initiate motor planning including sub-vocal rehearsal for short-term buffering of auditory stimuli. Enhanced high-gamma augmentation in IFG during presentation of the second tone may reflect high-order processing of the tone sequence.SignificanceThe articulatory loop employs sustained reciprocal propagation of neural activity across a network of cortical sites with strong neurophysiological connectivity.