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.

Highlights

  • Humans interact mostly verbally, non-verbal interactions are fundamental in social life

  • To statistically validate whether this Microstate 3 differed according to stimulus category, the values related to its duration were subjected to a repeated measure ANOVA with the within-subject factor of stimulus category (Figure 2A)

  • This ANOVA revealed that the duration of this Microstate 3 was significantly longer in use grip (Ug) = 28 ms and transport grip (Tg) = 26 ms than in Simple contact (Sc) (i.e., in the case of simple contact with the object; Sc = 18 ms; F(2,38) = 4.05; p = 0.03)

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Summary

Introduction

Humans interact mostly verbally, non-verbal interactions are fundamental in social life. There is a long tradition claiming that humans understand what others are doing by means of their capability to attribute a causal role to others’ internal mental states [5,6]. Single neuron recordings in the monkey and brain imaging and electrophysiological non-invasive techniques (Transcranial Magnetic Stimulation, TMS; Electroencephalogram, EEG; Magneto-Encephalogram, MEG) in humans showed that primates are endowed with a mechanism -the mirror mechanism- that matches the observed motor acts done by others on the observer’s motor representations of the same motor acts [7,8,9,10]. 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

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