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Mirror Neuron Activation Prior to Action Observation in a Predictable Context

A fundamental capacity of social animals consists in the predictive representation of upcoming events in the outside world, such as the actions of others. Here, we tested the activity of ventral premotor area F5 mirror neurons (MNs) while monkeys observed an experimenter performing (Action condition) or withholding (Inaction condition) a grasping action, which could be predicted on the basis of previously presented auditory instructions. Many of the recorded MNs discharged only during action observation (Action MNs), but one-third also encoded the experimenter's withheld action (Inaction MNs). Interestingly, while most of Action MNs exhibited reactive discharge during action observation, becoming active after the go signal, the majority of Inaction MNs showed predictive discharge. MN population activity as a whole displayed an overall predictive activation pattern, becoming active, on average, 340 ms before the go signal. Furthermore, MNs became active earlier when the observed action was performed in the monkeys' extrapersonal rather than peripersonal space, suggesting that context-based neural prediction of others' actions plays different roles depending on the monkeys' ability to interact with the observed agent.