Abstract The response of the motor neuron system to the observation of lateralized movements and expectation mismatches remains elusive. We investigated how observation of hand movement modulates corticospinal excitability as measured by motor evoked potentials to single pulse transcranial magnetic stimulation (TMS). Twenty-seven adults watched a series of egocentric video recordings of hands, with one hand either squeezing a foam ball as expected or both hands remaining stationary. Task conditions comprised observation-only and observation with synchronous imitation of the depicted motor action. Single TMS pulses were delivered to the motor cortex contralateral to the dominant hand at the video frame of maximal hand closure for squeeze videos and randomly for no-squeeze videos (in both observation-only or observation with synchronous imitation). We analyzed MEPs, from the First Dorsal Interosseous (FDI) muscle of the dominant hand. Observation alone (absence of motor intention) did not enhance corticospinal excitability; however, when paired with imitation (presence of motor intention), it tended to increase MEP amplitudes, regardless of the attended side (dominant or non-dominant) or depicted action (squeeze or not). Among conditions in which the dominant hand remained stationary, MEP amplitudes were elevated (p = 0.004) in observation with imitation of non-dominant hand squeezing, suggesting hemispheric dominance in coordinating motor actions. Additionally, MEP latencies tended to decrease during synchronous imitation of squeeze videos. Our findings support the consideration of observation with synchronous imitation as a task for brain state-dependent brain stimulation protocols for optimizing neuromotor recovery.
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