Bottom-up and top-down visuomotor responses to action observation

Action observation produces automatic "mirror" responses in the observers' motor system. However, in daily life, nonimitative actions are often required to be produced in response to others' acts, generating a conflict between automatic and voluntary responses. First, we used single-pulse transcranial magnetic stimulation (TMS) to assess the temporal dynamics of motor output in healthy volunteers preparing rule-based counter-imitative motor responses cued by different observed hand movements. Second, we applied the same paradigm after 1-Hz repetitive TMS (rTMS) of the left posterior parietal cortex (PPC) and of the left dorsolateral prefrontal cortex (dlPFC). The results showed an early (150 ms from onset of visual stimuli) stimulus-driven mirror response that was followed by a later (300 ms) rule-based nonmirror response. rTMS applied to the PPC modulated only the early mirror response. Conversely, rTMS to the dlPFC modulated specifically the late rule-based motor response. The data indicate that a fast bottom-up process mediated by the dorsal visual stream produces automatic imitative responses. Arbitrary rule-based visuomotor associations are on the contrary mediated by a slower system, relying on the prefrontal cortex. The 2 systems are mutually independent and compete for motor output in socially relevant situations only at a distal level.