Understanding Actions of Others: The Electrodynamics of the Left and Right Hemispheres. A High-Density EEG Neuroimaging Study

Abstract

BackgroundWhen we observe an individual performing a motor act (e.g. grasping a cup) we get two types of information on the basis of how the motor act is done and the context: what the agent is doing (i.e. grasping) and the intention underlying it (i.e. grasping for drinking). Here we examined the temporal dynamics of the brain activations that follow the observation of a motor act and underlie the observer's capacity to understand what the agent is doing and why.Methodology/Principal FindingsVolunteers were presented with two-frame video-clips. The first frame (T0) showed an object with or without context; the second frame (T1) showed a hand interacting with the object. The volunteers were instructed to understand the intention of the observed actions while their brain activity was recorded with a high-density 128-channel EEG system. Visual event-related potentials (VEPs) were recorded time-locked with the frame showing the hand-object interaction (T1). The data were analyzed by using electrical neuroimaging, which combines a cluster analysis performed on the group-averaged VEPs with the localization of the cortical sources that give rise to different spatio-temporal states of the global electrical field. Electrical neuroimaging results revealed four major steps: 1) bilateral posterior cortical activations; 2) a strong activation of the left posterior temporal and inferior parietal cortices with almost a complete disappearance of activations in the right hemisphere; 3) a significant increase of the activations of the right temporo-parietal region with simultaneously co-active left hemispheric sources, and 4) a significant global decrease of cortical activity accompanied by the appearance of activation of the orbito-frontal cortex.Conclusions/SignificanceWe conclude that the early striking left hemisphere involvement is due to the activation of a lateralized action-observation/action execution network. The activation of this lateralized network mediates the understanding of the goal of object-directed motor acts (mirror mechanism). The successive right hemisphere activation indicates that this hemisphere plays an important role in understanding the intention of others.

The motor way: Clinical implications of understanding and shaping actions with the motor system in autism and drug addiction

“…Compelling neurophysiological and brain-imaging experiments also provide indirect evidence for the presence of similar motor understanding mechanisms in humans (Berchio et al, 2014;Cattaneo et al, 2007;Cattaneo, Sandrini, & Schwarzbach, 2010;Gazzola et al, 2007;Iacoboni et al, 2005;McGarry, Russo, Schalles, & Pineda, 2012;Ortigue, Sinigaglia, Rizzolatti, & Grafton, 2010;Peeters et al, 2009;Senna, Bolognini, & Maravita, 2014;Théoret et al, 2005; for a review, see Rizzolatti et al, 2014). Taken together, these data suggest that also in humans the cortical motor system does not exclusively encode the kinematics of actions but also-and more intriguingly-its meaning.…”

Spatio-temporal Brain Dynamics of Understanding Social Versus Private Intentions: An Electrical Neuroimaging Study

“…Recent theories of embodied cognition (i.e., implicit understanding of others' actions through our own past motor experiences) suggest one understands intention of others by shaping one's understanding and anticipation of actions performed by others based on one's own motor system (Jeannerod, 2001;Niedenthal, 2007;Grafton, 2009), which is a process that takes place in embodied cognition (Grafton, 2009;Rizzolatti & Sinigaglia, 2008;Jeannerod, 2000;Ortigue et al, 2010, Grafton, 2009. As Jackson and Decety (2004) initially noted, the existence of a system matching executed and perceived actions offers a parsimonious explanation of how one recognizes other people's intended actionsi.e., by a direct mapping of the visual representation of the observed action onto one's own motor representation of the same action.…”

“…Inferring intentions of other people from the observation of their actions recruits an inferior fronto-parietal action observation network (AON) as well as a putative social network (SN) that includes the posterior superior temporal sulcus (STS), the temporoparietal junction (TPJ), the anterior paracingulate and also the cingulate cortex, a key prefrontal region subserving theory of mind (ToM). Furthermore, electrophysiological studies using high-density EEG recordings in healthy volunteers provide further information regarding the temporal dynamics between these two brain networks (AON and SN) for private intentions (Ortigue et al, 2009(Ortigue et al, , 2010Sabbagh et al, 2004a;Wang et al, , 2010. For instance, Ortigue et al recently showed the dynamic involvement of both the posterior superior temporal sulcus (pSTS) and inferior parietal lobe (IPL) at early stages of information processing for private intentions, and without a strict segregation between the AON and SN networks (Ortigue et al, 2009;.…”

“…However, the poor temporal resolution of fMRI neuroimaging limits the characterization of the temporal dynamics of communicative intention decoding (Ortigue et al, 2009(Ortigue et al, , 2010. Methods using millisecond temporal resolution, e.g., high-density surface EEG recordings, may provide critical information about the temporal dynamics of intention understanding (Liu et al, 2009a(Liu et al, , 2009b(Liu et al, , 2004Wang et al, 2010Sabbagh et al, 2004a;Ortigue et al, 2009).…”

Object words modulate the activity of the mirror neuron system during action imitation

“…Considering that object words refer to the goal of actions, such enhancement in the object word condition provides further evidence that the MNS is associated with the encoding of the goal of action and high‐level cognitive process, such as inferring the intentions of others. The object of action is considered to be critical for understanding what the individual is doing (Ortigue, Sinigaglia, Rizzolatti, & Grafton, 2010; Ortigue, Thompson, Parasuraman, & Grafton, 2009). Our findings about the unique nature of the object word are therefore compatible with previous works that emphasized the goal understanding function of the MNS(Rizzolatti et al., 2014; Sperduti, Guionnet, Fossati, & Nadel, 2014).…”