The widespread action observation/execution matching system for facial expression processing

Abstract

Observing and understanding others' emotional facial expressions, possibly through motor synchronization, plays a primary role in face-to-face communication. To understand the underlying neural mechanisms, previous functional magnetic resonance imaging (fMRI) studies investigated brain regions that are involved in both the observation/execution of emotional facial expressions and found that the neocortical motor regions constituting the action observation/execution matching system or mirror neuron system were active. However, it remains unclear (1) whether other brain regions in the limbic, cerebellum, and brainstem regions could be also involved in the observation/execution matching system for processing facial expressions, and (2) if so, whether these regions could constitute a functional network. To investigate these issues, we performed fMRI while participants observed dynamic facial expressions of anger and happiness and while they executed facial muscle activity associated with angry and happy facial expressions. Conjunction analyses revealed that, in addition to neocortical regions (i.e., the right ventral premotor cortex and right supplementary motor area), bilateral amygdala, right basal ganglia, bilateral cerebellum, and right facial nerve nucleus were activated during both the observation/execution tasks. Group independent component analysis revealed that a functional network component involving the aforementioned regions were activated during both observation/execution tasks. The data suggest that the motor synchronization of emotional facial expressions involves a widespread observation/execution matching network encompassing the neocortex, limbic system, basal ganglia, cerebellum, and brainstem.

Keywords: amygdala; cerebellum; dynamic facial expressions of emotion; facial nerve nucleus; group independent component analysis (ICA); mirror neuron system.

FIGURE 1

Illustrations of the facial expression observation/execution tasks. During the observation task, participants passively observed angry or happy dynamic facial expressions, or dynamic random mosaics. During the execution task, plus symbols of three different colors were presented, and participants activated specific facial muscles (corrugator supercilii or zygomatic major) or rested.

FIGURE 2

Statistical parametric maps and mean (± SE) effect size indicating shared activity in the neocortex between the observation (dynamic faces vs. dynamic mosaics) and execution tasks (facial actions vs. rest). The area is superposed on mean normalized structural images of the participants in this study.

FIGURE 3

Statistical parametric maps and mean (± SE) effect size indicating shared activity in the limbic, cerebellar, and brainstem regions between the observation (dynamic faces versus dynamic mosaics) and execution tasks (facial actions versus rest). The area is superposed on mean normalized structural images of the participants in this study.

FIGURE 4

Group independent component maps (component #7) and mean (± SE) effect size of the regression analysis on this component time course indicating significant network activity in both the observation (dynamic faces vs. dynamic mosaics) and execution (facial actions vs. rest) tasks. The component network is superposed on mean normalized structural images of the study participants. Yellow circles represent activation foci detected in the conjunction analysis, including the facial nerve nucleus (1), cerebellum (2), amygdala (3), pallidum (4), ventral premotor cortex (5), and supplementary motor area (6).