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.
Robotics, Brain and Cognitive Sciences Department, Italian Institute of Technology, Genova, Italy; Dipartimento di Scienze Umane, Università Degli Studi di Udine, Udine, Italy;
Alessandra
A
Finisguerra
Robotics, Brain and Cognitive Sciences Department, Italian Institute of Technology, Genova, Italy;
Laura
L
Maffongelli
Robotics, Brain and Cognitive Sciences Department, Italian Institute of Technology, Genova, Italy; Center for Neuroprosthetics, École Polytechnique Fédérale de Lausanne, Lausanne, Switzerland; and.
Michela
M
Bassolino
Robotics, Brain and Cognitive Sciences Department, Italian Institute of Technology, Genova, Italy;
Marco
M
Jacono
Robotics, Brain and Cognitive Sciences Department, Italian Institute of Technology, Genova, Italy; IUF, INSERM U1093 Cognition, Action et Plasticité Sensorimotrice, Université de Bourgogne, Dijon, France.
Thierry
T
Pozzo
Robotics, Brain and Cognitive Sciences Department, Italian Institute of Technology, Genova, Italy; alessandro.dausilio@iit.it.
Alessandro
A
D'Ausilio
D061725:Accelerometry; D001696:Biomechanical Phenomena; D004576:Electromyography; D019054:Evoked Potentials, Motor / Q000502:physiology; D005123:Eye; D005133:Eye Movements; D005260:Female; D005385:Fingers / Q000502:physiology*; D006801:Humans; D008297:Male; D009039:Motion Perception / Q000502:physiology*; D009043:Motor Activity / Q000502:physiology*; D009044:Motor Cortex / Q000502:physiology*; D009055:Mouth; D050781:Transcranial Magnetic Stimulation; D014741:Video Recording; D055815:Young Adult
action observation network; corticospinal excitability; finger kinematics; motor generalization; transcranial magnetic stimulation