The social relevance and the temporal constraints of motor resonance in humans

Abstract

In humans, motor resonance effects can be tracked by measuring the enhancement of corticospinal excitability by action observation. Uncovering factors driving motor resonance is crucial for optimizing action observation paradigms in experimental and clinical settings. In the present study, we deepen motor resonance properties for grasping movements. Thirty-five healthy subjects underwent an action observation task presenting right-hand grasping movements differing from their action goal. Single-pulse transcranial magnetic stimulation was applied over the left primary motor cortex at 100, 200, or 300 ms from the onset of the visual stimulus depicting the action. Motor-evoked potentials were recorded from four muscles of the right hand and forearm. Results show a muscle-specific motor resonance effect at 200 ms after movement but selectively for observing a socially relevant grasp towards another human being. This effect correlates with observers' emotional empathy scores, and it was followed by inhibition of motor resonance at 300 ms post-stimulus onset. No motor resonance facilitation emerged while observing intransitive hand movement or object grasping. This evidence highlights the social side of motor resonance and its dependency on temporal factors.

Figure 1

(a) Experimental procedure. At first, participants underwent neuronavigation procedures and the assessment of the resting motor threshold (rMT). Then, the different blocks of the action observation task were administered. The order of the three experimental conditions (i.e., ‘intransitive grasping’, ‘object grasping’, and ‘social grasping’) was randomized across participants. Finally, the Interpersonal Reactivity Index (IRI) was administered. (b) Action observation task. The action observation paradigm consisted of a two-frame video-clip showing a right-hand grasping movement whose target was modulated according to the experimental condition. For ‘movement trials’, TMS over left M1 was administered at 120% rMT at 100, 200, or 300 ms from the onset of the action frame. For ‘static trials’—which served as a baseline for detecting motor resonance—the ‘action frame’ was replaced with another ‘static frame’, and TMS was delivered at its onset. In each condition, 136 trials were presented to participants. MEPs were simultaneously recorded from first dorsal interosseus (FDI), abductor digiti minimi (ADM), extensor carpi radialis (ECR), and flexor carpi radialis (FCR) muscles.

Figure 2

Motor resonance effects (i.e., MEP amplitude in ‘movement trials’ divided for MEP amplitude in ‘static hand trials’) in the three experimental conditions (a—‘intransitive grasping’; b—‘object grasping’; c—‘social grasping’) and for the four muscles (left panels: FDI—straight blue lines, ADM—dotted brown lines; right panels: ECR—straight green lines, FCR—dotted yellow lines) at the three timepoints of TMS administration (100, 200, 300 ms). *p < 0.05; **p < 0.01. Error bars: SE.

Figure 3

(a) Scatterplots between participants’ scores in the IRI’s four subscales (x-axis) and motor resonance effect for FDI muscle at 200 ms timing (y-axis). A significant correlation (Spearman’s rho) is found only for the EC scale. (b) IRI scores in the two clusters of our sample found running hierarchical clustering. No statistically significant differences were found between clusters. Error bars: SE.