Abstract

Observing other people in action activates the “mirror neuron system” that serves for action comprehension and prediction. Recent evidence suggests that this function requires a high level codification triggered not only by components of motor behavior, but also by the environment where the action is embedded. An overlooked component of action perceiving is the one related to the emotional information provided by the context where the observed action takes place. Indeed, whether valence and arousal associated to an emotion might exert an influence on motor system activation during action observation has not been assessed so far. Here, cortico-spinal excitability of the left motor cortex was recorded in three groups of subjects. In the first condition, motor-evoked potential (MEPs) were recorded from a muscle involved in the grasping movement (i.e., abductor pollicis brevis, APB) while participants were watching the same reach-to-grasp movement embedded in contexts with negative emotional valence, but different levels of arousal: sadness (low arousal), and disgust (high arousal) (“Context plus Movement-APB” condition). In the second condition, MEPs were recorded from APB muscle while participants were observing static images representing the contexts in which the movement observed by participants in “Context plus Movement-APB” condition took place (“Context Only-APB” condition). Finally, in the third condition, MEPS were recorded from a muscle not involved in the grasping action, i.e., abductor digiti minimi, ADM, while participants were watching the same videos shown during the “Context plus Movement-APB” condition (“Context plus Movement-ADM” condition). Results showed a greater increase of cortical excitability only during the observation of the hand moving in the context eliciting disgust, and these changes were specific for the muscle involved in the observed action. Our findings show that the emotional context in which a movement occurs modulates motor resonance and that the combination of negative valence/high arousal drives the greater response in the observer’s mirror neuron system in a strictly muscle specific fashion.

Highlights

  • In daily life we are constantly exposed to people acting in our social world

  • Post hoc test showed that only motor-evoked potentials (MEPs) collected while participants were observing the Disgust video were significantly higher than MEPs collected when subjects were observing the No-emotion video (Disgust vs. No-emotion: p = 0.0001) and the Sadness video (Disgust vs. Sadness: p = 0.002), whereas there was no difference between MEPs collected during the observation of the Sadness video and the grasping No-emotion video (p = 0.11)

  • Post hoc analysis revealed that only in the “Context plus movement-APB” condition, MEPs collected when subjects were observing the Disgust video were significantly higher than MEPs collected when subjects were observing the No-emotion (p = 0.001) and Sadness (p = 0.015) videos, with no difference between No-emotion and Sadness (p = 0.08)

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Summary

Introduction

In daily life we are constantly exposed to people acting in our social world. We are able to describe these actions, to understand their content and to predict their consequences; a link between the agent and the observer must be established. The amplitudes of MEPs in the contralateral target muscle (that is an index of cortico-spinal excitability) are modulated by action observation, a phenomenon described as “motor resonance” (Fadiga et al, 1995). This ‘motor resonance’ effect is thought to result from activity in MNS regions, which enhances the excitability of the primary motor cortex (M1) via cortico-cortical pathways (Fadiga et al, 2005; Avenanti et al, 2007; Koch et al, 2010; Naish et al, 2014). It has been extensively shown that MEPs recorded during action observation are modulated by premotor and parietal regions where mirror neurons have been commonly reported (Avenanti et al, 2007, 2013; Koch et al, 2010) (for an extensive review of TMS-MEPs studies addressing the features of motor resonance see Naish et al, 2014)

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