Affect-specific activation of shared networks for perception and execution of facial expressions

Abstract

Previous studies have shown overlapping neural activations for observation and execution or imitation of emotional facial expressions. These shared representations have been assumed to provide indirect evidence for a human mirror neuron system, which is suggested to be a prerequisite of action comprehension. We aimed at clarifying whether shared representations in and beyond human mirror areas are specifically activated by affective facial expressions or whether they are activated by facial expressions independent of the emotional meaning. During neuroimaging, participants observed and executed happy and non-emotional facial expressions. Shared representations were revealed for happy facial expressions in the pars opercularis, the precentral gyrus, in the superior temporal gyrus/medial temporal gyrus (MTG), in the pre-supplementary motor area and in the right amygdala. All areas showed less pronounced activation in the non-emotional condition. When directly compared, significant stronger neural responses emerged for happy facial expressions in the pre-supplementary motor area and in the MTG than for non-emotional stimuli. We assume that activation of shared representations depends on the affect and (social) relevance of the facial expression. The pre-supplementary motor area is a core-shared representation-structure supporting observation and execution of affective contagious facial expressions and might have a modulatory role during the preparation of executing happy facial expressions.

Fig. 1

(A) All video clips depicting actors were rated in a prior behavioral study. Participants of the rating study watched each video clip. Afterwards, they had to categorize the video to either one of the six basic emotions or to the neutral category. (B) Time course of one exemplary video clip. Each video started and ended with the actor having a neutral face without any movement.

Fig. 2

(A) Video clips were used as stimulus material in all conditions. In the observation condition, participants were presented with videos showing actors demonstrating a happy facial expression, a non-emotional facial movement, or a neutral face without any movement. Participants were asked to observe the actors without making any movement themselves. In the execution condition, scrambled video clips were presented; a colored fixation cross in the middle of the scramble indicated which movement had to be executed by the participants. (B) One block encompassed 4 video clips à 5 s. Blocks were separated by a low level baseline of 5 s duration.

Fig. 3

Shared neural network underlying observation and execution of happy facial expressions. The conjunction analysis was FWE-corrected at a threshold of P < 0.05. Shared representations were found in the pars opercularis, the STG extending to the MTG, the precentral gyrus and the (PRE)SMA. This network was less activated in the non-emotional condition (see inserts). Particularly the (PRE)SMA was not activated in the non-emotional facial gesture (see direct comparison in Figure 4). H, happy; NE, non-emotional; N, neutral; OBS, observation; EX, execution.

Fig. 4

Social relevance reflected in the direct comparison of emotional- with non-emotional shared representations. The conjunction analysis was FWE-corrected at a threshold of P < 0.05. Significant differences were found in the (PRE)SMA and the MTG.