Processing social aspects of human gaze: A combined fMRI-DTI study

Laboratory for Behavioral Neurology & Imaging of Cognition, Department of Neuroscience & Clinic of Neurology, Medical School, University of Geneva, Switzerland.
NeuroImage (Impact Factor: 6.36). 03/2011; 55(1):411-9. DOI: 10.1016/j.neuroimage.2010.11.033
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Human gaze is a critical social cue that can reveal intentions and dispositions of others. The right posterior superior temporal sulcus (pSTS) is thought to be critically involved in processing eye gaze information. We combined diffusion tensor imaging (DTI) and functional magnetic resonance imaging (fMRI) to identify direct neural connections of right pSTS and to determine how these connections are modulated by the social significance of perceived gaze shifts. Participants saw faces with direct or averted gaze during event-related fMRI. Half of these faces remained static, and half displayed a dynamic gaze shift either towards or away from the subject. Social attention (dynamic gaze shifts towards the observer) not only increased activity in right pSTS, but also its functional connectivity with the right anterior insula (aIns) and right fusiform gyrus (FG). However, direct fiber connections from pSTS were demonstrated by DTI for the right aIns, but not the right FG. Moreover, the right FG responded to eye motion irrespective of direction and social significance; whereas the right aIns was selectively sensitive to social significance (i.e. gaze shifts towards the observer), but not generally to eye motion. We conclude that the social aspects of mutual gaze contact are processed by direct fiber pathways between right pSTS and right aIns; whereas increased connectivity with FG could reflect an enhanced perceptual analysis of changing facial features in dynamic gaze conditions and involves indirect fiber pathways with pSTS, perhaps via motion-selective regions in middle temporal (MT) gyrus that exhibited strong white-matter connections with both pSTS and FG and could thus provide inputs to these two areas.

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    • " et al . , 2008 ; Hoffman and Haxby , 2000 ; Pageler et al . , 2003 ; Pel - phrey et al . , 2003 ; Puce et al . , 1998 ] , amygdala [ Adams et al . , 2003 ; George et al . , 2001 ; Hadjikhani et al . , 2008 ; Hooker et al . , 2003 ; Kawashima et al . , 1999 ; Sato et al . , 2004 , 2010 ; Straube et al . , 2010 ; Wicker et al . , 2003 ] , MT / V5 [ Ethofer et al . , 2011 ; Hadjikhani et al . , 2008 ; Kuzmanovic et al . , 2009 ; Watanabe et al . , 2001 ; Wicker et al . , 2003 ] , and medial pre - frontal cortex [ MPFC ; Calder et al . , 2002 ; Conty et al . , 2007 ; Kampe et al . , 2003 ; Schilbach et al . , 2006 ] . Senju and Johnson [ 2009 ] explicitly focused in their review on the neural corre - late"
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    • "Dynamic gaze shifts have been found to increase activation in a well-established region of the social network including the right pSTS, anterior insula, and fusiform gyrus with direct connections noted between the right pSTS and anterior insula. These regions are thought to be supported by long-range network connections that project via the superior longitudinal fasciculus and are believed to be critical for extracting social meaning of eye gaze shifts [61]. Consistent with this purported social network, compared to those with ASD, our NT participants demonstrated significantly higher coherence between the right middle and inferior frontal gyri and the right superior temporal regions within the beta band frequency known to be critical for long-range connectivity. "
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