Uncertainty in contextual and kinematic cues jointly modulates motor resonance in primary motor cortex.

Abstract

Contextual information accompanying others' actions modulates "motor resonance", i.e., neural activity within motor areas that is elicited by movement observation. One possibility is that we weigh and combine such information in a Bayesian manner according to their relative uncertainty. Therefore, contextual information becomes particularly useful when others' actions are difficult to discriminate. It is unclear, however, whether this uncertainty modulates the neural activity in primary motor cortex (M1) during movement observation. Here, we applied single-pulse transcranial magnetic stimulation (TMS) while subjects watched different grasping actions. We operationalized motor resonance as grip-specific modulation of corticomotor excitability measured in the index (FDI) versus the little finger abductor (ADM). We experimentally modulated either the availability of kinematic information ( experiment 1) or the reliability of contextual cues ( experiment 2). Our results indicate that even in the absence of movement kinematics, reliable contextual information is enough to trigger significant muscle-specific corticomotor excitability changes in M1, which are strongest when both kinematics and contextual information are available. These findings suggest that bottom-up mechanisms that activate motor representations as a function of the observed kinematics and top-down mechanisms that activate motor representations associated with arbitrary cues converge in M1. NEW & NOTEWORTHY Our study reveals new neurophysiological insights in support of the Bayesian account of action observation by showing that "motor resonance", i.e., neural activity evoked by observing others' actions, incorporates the uncertainty related to both contextual (prior beliefs) and kinematic (sensory evidence) cues. Notably, we show that muscle-specific modulation of M1 is strongest when context and movement kinematics are available, and it can be elicited even in the absence of movement kinematics.