Neural substrates and inter-individual functional connectivity during mutual gaze and joint attention using dual functional MRI

Eye contact provides a communicative link between humans, prompting joint attention. As spontaneous brain activity might have an important role in the coordination of neuronal processing within the brain, their inter-subject synchronization might occur during eye contact. To test this, we conducted simultaneous functional MRI in pairs of adults. Eye contact was maintained at baseline while the subjects engaged in real-time gaze exchange in a joint attention task. Averted gaze activated the bilateral occipital pole extending to the right posterior superior temporal sulcus, the dorso-medial prefrontal cortex, and the bilateral inferior frontal gyrus. After all the task-related effects were modeled out, inter-individual correlation analysis of residual time-courses was performed. Paired subjects showed more prominent correlations than non-paired subjects in the right inferior frontal gyrus (IFG), suggesting that this region is involved in sharing intention during eye contact that provides the context for joint attention. Lack of joint attention and eye contact is an early signs of autism spectrum disorders (ASD). To depict its neural underpinning, identical protocol was applied to ASD subjects paired with normal subjects. Performance was not only impaired in ASD subjects, but also their paired normal subjects. Inter-brain coherence in the right IFG was significantly less prominent in the ASD - Normal pairs than Normal-Normal pairs. Thus the impairment of joint attention in ASD is partly related to difficulty in obtaining the shared intention through eye contact that is represented by the reduced inter-subject synchronization of the right IFG.