Corticospinal excitability during the observation of social behavior

Abstract

Evidence suggests that the observation of an action induces in the observers an enhancement of motor evoked potentials (MEPs) recorded by the observer’s muscles corresponding to those involved in the observed action. Although this is a well-studied phenomenon, it remains still unclear how the viewer’s motor facilitation is influenced by the social content characterizing the observed scene. In the present study we investigated the facilitation of the corticospinal system during the observation of either an action that does not imply a social interaction (i.e., an actor throwing a ball against a wall), or an action which implies a social interaction (i.e., an actor passing a ball to a partner). Results indicate that MEPs amplitude is enhanced during the observation of a social rather than an individual action. We contend that the increase in MEPs activation might reflect an enhancement of the simulative activity stemming from the mirror system during the observation of social interactions. Altogether these findings show that the human corticospinal system is sensitive to social interactions and may support the role of the mirror neurons system in social cognition.

Introduction

The capability to understand the meaning of others’ actions is an essential characteristic for the human adaptation to social and physical environments. Insights into the neural mechanisms of action understanding comes from the discovery of neurons activated during both the execution and the observation of a given action (the so-called mirror neurons) in the monkey premotor and parietal cortices (di Pellegrino et al., 1992, Gallese et al., 1996, Rizzolatti et al., 2001). Following this discovery, neurophysiological (Fadiga et al., 1995, Hari et al., 1998, Romani et al., 2005) and neuroimaging (Buccino et al., 2001, Decety et al., 1997, Grafton et al., 1996, Rizzolatti et al., 1996, Turella et al., 2009) studies have uncovered a similar system in humans. In particular, it has been suggested that the action observation–execution matching system would offer a parsimonious answer to how it is possible to understand others’ behavior. In this view, the observation of another’s behavior elicits changes in the cortical and corticospinal activity indicating that, in the observer, a motor representation for the same act is activated (e.g., Buccino et al., 2001, Fadiga et al., 2005).

More recently, it has been proposed that the action observation–execution matching system is not only modulated by the physical aspects of an action, but also by the social context within which an action is embedded (Becchio et al., 2012, Iacoboni et al., 2004, Kourtis et al., 2010, Oberman et al., 2007). For example, in a functional magnetic resonance imaging study, Iacoboni et al. (2004) reported an increase in activation within a key ‘mirror’ area, namely the inferior frontal gyrus, following the observation of a scene depicting two individuals interacting, as compared to a scene depicting one individual engaging in everyday activities. Oberman et al. (2007) measured mu rhythm oscillations (an index of mirror neurons activity), during the observation of actions characterized by a different degree of social interaction. They found a correspondence between the level of mu wave suppression and the degree of social interaction to which the subject was exposed – i.e., the highest amount of mu wave suppression was recorded for the interacting condition. Similarly, Kourtis et al. (2010) by analyzing the amplitude of the contingent negative variation (CNV) and the oscillations of beta rhythm as a measure of anticipation of other’s actions, have shown that the simulation of another person’s action depends on the degree of social relation between the actor and the observer – i.e., motor resonance is increased when subjects perceived the other person as an interacting partner. Further support to the idea that action simulation is sensitive to the social features characterizing an observed action comes from a series of transcranial magnetic stimulation (TMS) studies (Sartori, Bucchioni, & Castiello, 2012; Sartori et al., 2011a, Sartori et al., 2011b). This series of experiments has shown that corticospinal excitability varies depending on whether the observed action is performed in either an individual or a social context implying a complementary action by the observer.

Although the above evidence is indicative of a social sensitivity by the action observation–execution matching system, the scenarios considered in these experiments called for either an explicit or implicit involvement by the observer in terms of social interaction. What remains unclear is how the system reacts to either social or individual actions that in principle do not imply a first person involvement by the observer. Therefore the key question addressed in the present study is to highlight the role of the action observation–execution matching system in the processing of social stimuli from an external perspective. Specifically, we investigated the degree to which corticospinal excitability would be modulated based on the extent of the social content characterizing an observed action. To this end, we applied single pulse TMS on the participant’s left primary motor cortex (M1) and simultaneously recorded motor evoked potentials (MEPs) from the flexor carpi ulnaris (FCU) and the abductor digiti minimi, (ADM) while participants observed video-clips depicting the same action embedded in two different contexts: (i) a model passing a ball to a partner (social condition); and (ii) a model throwing a ball against a wall (individual condition). These two muscles are actually involved in the observed action. More specifically, we investigated both the degree to which corticospinal excitability would be modulated based on the social content of a given human action as well as whether the observer becomes somewhat involved by the scene.