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

Abstract

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.

Keywords: action observation network; corticospinal excitability; finger kinematics; motor generalization; transcranial magnetic stimulation.

Fig. 1.

Experimental design. A: the procedure of the two experiments is detailed. In both experiments, a first baseline recording (B1) during which subjects were at rest was followed by an experimental session (EXP) during which participants observed videos clips, and by a second baseline recording (B2). B: the pictures show frames from each video clip representing the experimental stimuli for the first (left) and the second experiment (right). Opening and closing actions performed by the homologue (hand for both groups) and different effectors (mouth for group 1 and eyelid for group 2) are shown.

Fig. 2.

Experimental recording of the transcranial magnetic stimulation (TMS) evoked effects and dependent variables. A: the experimental setup used to measure the TMS-evoked movement and the motor evoked potentials (MEPs). The acceleration components recorded with the accelerometer in a representative subject are depicted for each trial (thin lines), and for the averaged value (thick line) for the z, x components and for the module. Single trials (thin lines) and averaged (thick line) values of the MEPs are instead represented on the right part of the same panel. The middle picture shows the setup to record accelerometer data and electromyography of the right flexor digitorum superficialis muscle. Bottom: the TMS-evoked movement parameters. B: opening or closing movement direction is derived from the positive or negative values, respectively, of the z-component. C: movement deviation expresses the angular displacement of the finger on the frontal axis (abduction/adduction movement) during the opening or closing motion (dashed line). This angle is expressed with respect to the ideal opening or closing movement (solid line). Higher movement deviation results in greater contribution of the abduction/adduction component.

Fig. 3.

Effect of opening and closing action observation (AO) on MEPs. Top: the modulation of the MEP amplitude ratio (condition/average baseline) due to the observation of opening (gray) and closing (black) movements of the homologue effector and the different effector. Bottom: the same data when the homologue and different effectors of the two experiments are separated. Values are means ± SE. *Significant comparisons.

Fig. 4.

Effect of AO on the movement direction. Changes in movement direction (%closing movements) for opening and closing AO, considering the homologue and different effectors (top) and by separating the homologue and different effectors of the two experiments (bottom). Values are mean angles ± SE of the movement deviation. *Significant comparisons.

Fig. 5.

Effect of AO on the movement deviation. Changes in movement deviation for opening (A) and closing (B) motion during AO, considering the homologue and different effectors (top) and by separating the homologue and different effectors of the two experiments (bottom). Values are mean angles ± SE of the movement deviation. *Significant comparisons.