Neurons firing both during self and other's motor behavior (mirror neurons) have been described in the brain of vertebrates including humans. The activation of somatic motor programs driven by perceived behavior has been taken as evidence for mirror neurons' contribution to cognition. The inverse relation, that is the influence of motor behavior on perception, is needed for demonstrating the long-hypothesized causal role of mirror neurons in action understanding. We provide here conclusive behavioral and neurophysiological evidence for that causal role by means of cross-modal adaptation coupled with a novel transcranial magnetic stimulation (TMS)-adaptation paradigm. Blindfolded repeated motor performance of an object-directed action (push or pull) induced in healthy participants a strong visual after-effect when categorizing others' actions, as a result of motor-to-visual adaptation of visuo-motor neurons. TMS over the ventral premotor cortex, but not over the primary motor cortex, suppressed the after-effect, thus localizing the population of adapted visuo-motor neurons in the premotor cortex. These data are exquisitely consistent in humans with the existence of premotor mirror neurons that have access to the action meaning. We also show that controlled manipulation of the firing properties of this neural population produces strong predictable changes in the way we categorize others' actions.
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.
Is a short visuomotor associative training sufficient to reverse the visuomotor tuning of mirror neurons in adult humans? We tested the effects of associative training on corticospinal modulation during action observation in the 100-320 ms interval after action onset. In two separate experiments, the acceleration of transcranial magnetic stimulation (TMS)-induced movements was recorded before and after training participants to respond to observed acts with an opposite or similar behavior. Before training, TMS-induced accelerations mirrored the observed action at 250 and 320 ms. After training, responses at 250 ms were unchanged and still mirrored the stimuli, without any effect of training direction. Only at 320 ms, we observed training-dependent changes in evoked responses. A control experiment with non-biological rotational movements as visual stimuli indicated that spatial stimulus-response compatibility is not sufficient to account for the results of the two main experiments. We show that the effects of a short visuomotor associative training are not pervasive on the automatic mirror responses. 'Early' (250 ms) responses were not influenced by training. Conversely only 'late' (320 ms) responses changed according to the training direction. This biphasic time course indicates that two distinct mechanisms produce the automatic mirror responses and the newly learned visuomotor associations.
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