Shared attention and interindividual neural synchronization in the human right inferior frontal cortex

Abstract

During a dyadic social interaction, two individuals can share visual attention through gaze, directed to each other (eye contact) or to a third person or an object (joint attention). Eye contact and joint attention are tightly coupled to generate the state of shared attention across individuals. Hyperscanning fMRI conducted with pairs of adults during joint attention tasks showed interindividual neural synchronization in the right inferior frontal gyrus. To explore how joint attention generates the state of shared attention, and whether its memory trace persists during a subsequent eye-contact condition, two-day hyperscanning fMRI study was conducted, in which pairs of participants performed a real-time mutual gaze task followed by a joint attention task on the first day and mutual gaze tasks several days later. The joint attention task enhanced eye-blink synchronization, which is a behavioral index of shared attention. When the same participant pairs underwent mutual gaze without joint attention on the second day, enhanced eye-blink synchronization persisted, which was positively correlated with interindividual neural synchronization within the right inferior frontal gyrus. Neural synchronization was also positively correlated with enhanced eye-blink synchronization during the previous joint attention task session. These results indicate that shared attention is represented and retained by pair-specific neural synchronization during mutual gaze that cannot be reduced to the individual level. This interbrain effect highlights the role of the right inferior frontal gyrus in the execution and learning of attentional coordination and sharing attention between self and others.