Generalization of motor resonance during the observation of hand, mouth, and eye movements

Transcranial magnetic stimulation (TMS) of the motor cortex shows that hand action observation (AO) modulates corticospinal excitability (CSE). CSE modulation alternatively maps low-level kinematic characteristics or higher-level features, like object-directed action goals. However, action execution is achieved through the control of muscle synergies, consisting of coordinated patterns of muscular activity during natural movements, rather than single muscles or object-directed goals. This synergistic organization of action execution also underlies the ability to produce the same functional output (i.e., grasping an object) using different effectors. We hypothesize that motor system activation during AO may rely on similar principles. To investigate this issue, we recorded both hand CSE and TMS-evoked finger movements which provide a much more complete description of coordinated patterns of muscular activity. Subjects passively watched hand, mouth and eyelid opening or closing, which are performing non-object-directed (intransitive) actions. Hand and mouth share the same potential to grasp objects, whereas eyelid does not allow object-directed (transitive) actions. Hand CSE modulation generalized to all effectors, while TMS evoked finger movements only to mouth AO. Such dissociation suggests that the two techniques may have different sensitivities to fine motor modulations induced by AO. Differently from evoked movements, which are sensitive to the possibility to achieve object-directed action, CSE is generically modulated by "opening" vs. "closing" movements, independently of which effector was observed. We propose that motor activities during AO might exploit the same synergistic mechanisms shown for the neural control of movement and organized around a limited set of motor primitives.