Tracking the Time Course of Top-Down Contextual Effects on Motor Responses during Action Comprehension

Context plays a key role in coding high-level components of others' behavior, including the goal and the intention of an observed action. However, little is known about its possible role in shaping lower levels of action processing, such as simulating action kinematics and muscular activity. Furthermore, there is no evidence regarding the time course and the neural mechanisms subserving this modulation. To address these issues, we combined single-pulse transcranial magnetic stimulation and motor-evoked potentials while healthy humans watched videos of everyday actions embedded in congruent, incongruent, or ambiguous contexts. Video endings were occluded from view and participants had to predict action unfolding. Transcranial magnetic stimulation was delivered at 80, 240, and 400 ms after action onset. An earlier selective facilitation of motor resonance occurring at 240 ms was observed for actions embedded in congruent contexts, compared with those occurring in incongruent and ambiguous ones. Later on, at 400 ms, a selective inhibition of motor resonance was found for actions embedded in incongruent contexts, compared with those taking place in congruent and ambiguous ones. No modulations were observed at 80 ms. Together, these findings indicate that motor resonance can be modulated by contextual information with different timings, depending on the (in)congruency between the different levels of action representation. Furthermore, the different time course of these effects suggests that they stem from partially independent mechanisms, with the early facilitation directly involving M1, and the later inhibition recruiting high-level structures outside the motor system. SIGNIFICANCE STATEMENT Previous studies indicate that, when we observe other people's actions, the context in which actions take place influences intention understanding. However, little is known about the precise mechanisms involved in the contextual modulation of action representation (i.e., inhibition vs facilitation) and how they unfold in time. The present study sheds light on these aspects. Specifically, we show an early top-down facilitation (at ∼240 ms) and a later inhibition (at ∼400 ms) of motor resonance in response to actions observed in congruent and incongruent contexts, respectively.

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