Distinct sensitivities of the lateral prefrontal cortex and extrastriate body area to contingency between executed and observed actions

Detecting relationships between our own actions and the subsequent actions of others is critical for our social behavior. Self-actions differ from those of others in terms of action kinematics, body identity, and feedback timing. Thus, the detection of social contingency between self-actions and those of others requires comparison and integration of these three dimensions. Neuroimaging studies have highlighted the role of the frontotemporal network in action representation, but the role of each node and their relationships are still controversial. Here, we conducted a functional MRI experiment to test the hypothesis that the lateral prefrontal cortex and lateral occipito-temporal cortex are critical for the integration processes for social contingency. Twenty-four adults performed right finger gestures and then observed them as feedback. We manipulated three parameters of visual feedback: action kinematics (same or different gestures), body identity (self or other), and feedback timing (simultaneous or delayed). Three-way interactions of these factors were observed in the left inferior and middle frontal gyrus (IFG/MFG). These areas were active when self-actions were directly fed back in real-time (i.e., the condition causing a sense of agency), and when participants observed gestures performed by others after a short delay (i.e., the condition causing social contingency). In contrast, the left extrastriate body area (EBA) was sensitive to the concordance of action kinematics regardless of body identity or feedback timing. Body identity × feedback timing interactions were observed in regions including the superior parietal lobule (SPL). An effective connectivity analysis supported the model wherein experimental parameters modulated connections from the occipital cortex to the IFG/MFG via the EBA and SPL. These results suggest that both social contingency and the sense of agency are achieved by hierarchical processing that begins with simple concordance coding in the left EBA, leading to the complex coding of social relevance in the left IFG/MFG.