Observation-execution matching and action inhibition in human primary motor cortex during viewing of speech-related lip movements or listening to speech

Abstract

One influential theory posits that language has evolved from gestural communication through observation-execution matching processes in the mirror neuron system (MNS). This theory predicts that observation of speech-related lip movements or even listening to speech would result in effector and task specific increase of the excitability of the corresponding motor representations in the primary motor cortex (M1), since actual movement execution is known be effector and task specific. In addition, effector and task specific inhibitory control mechanisms should be important to prevent overt motor activation during observation of speech-related lip movements or listening to speech. We tested these predictions by applying focal transcranial magnetic stimulation to the left M1 of 12 healthy right-handed volunteers and measuring motor evoked potentials (MEPs) and short-interval intracortical inhibition (SICI) in a lip muscle, the right orbicularis oris (OO), vs. a hand muscle, the right first dorsal interosseus (FDI). We found that MEP and SICI increased only in the OO but not in the FDI during viewing of speech-related lip movements or listening to speech. These changes were highly task specific because they were absent when lip movements non-related to speech were viewed. Finally, the increase in MEP amplitude in the OO correlated inversely with accuracy of speech perception, i.e. the MEP increase was directly related to task difficulty. The MEP findings support the notion that observation-execution matching is an operating process in the putative human MNS that might have been fundamental for evolution of language. Furthermore, the SICI findings provide evidence that inhibitory mechanisms are recruited to prevent unwanted overt motor activation during action observation.