When gaze opens the channel for communication: Integrative role of IFG and MPFC

Recent advances in the field of cognitive neuroscience have revealed that direct gaze modulates activity in cortical and subcortical key regions of the 'social brain network', including the inferior frontal gyrus (IFG) and the anterior rostral medial prefrontal cortex (arMPFC). However, very little is known about how direct gaze is processed during live interaction with a real partner. Here, for the first time we used an experimental setup allowing the participant inside an MRI scanner to interact face-to-face with a partner located in the scanner room. Depending on condition, the participant and the partner were instructed either to look at each other in the eyes or to direct their gaze away from the other. As control conditions, participants gazed at their own eyes, reflected in a mirror, or gazed at a picture of the partner's eyes. Results revealed that direct gaze by the partner was associated with activity in areas involved in production and comprehension of language and action, including the IFG, the premotor cortex (PM), and the supplementary motor area (SMA). Activations in these areas were observed regardless of the participant's gaze behavior. In contrast, increased activity in arMPFC, an area involved in inference of other mental states during social interaction and communication, was only observed when the participant reciprocated the partner's direct gaze so as to establish mutual gaze. Psychophysiological interaction (PPI) analysis revealed effective connectivity between the IFG and the arMPFC during mutual gaze. This suggests that, within a larger network concerned with the processing of social gaze, mutual gaze with a real partner is established by an increased coupling between areas involved in the detection of communicative intentions, language, and social interaction.