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
Source: PubMed


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.

Download full-text


Available from: Markus Gschwind, Oct 04, 2015
27 Reads
  • Source
    • " 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"
    [Show abstract] [Hide abstract]
    ABSTRACT: The Mona Lisa effect describes the phenomenon when the eyes of a portrait appear to look at the observer regardless of the observer's position. Recently, the metaphor of a cone of gaze has been proposed to describe the range of gaze directions within which a person feels looked at. The width of the gaze cone is about five degrees of visual angle to either side of a given gaze direction. We used functional magnetic resonance imaging to investigate how the brain regions involved in gaze direction discrimination would differ between centered and decentered presentation positions of a portrait exhibiting eye contact. Subjects observed a given portrait's eyes. By presenting portraits with varying gaze directions-eye contact (0°), gaze at the edge of the gaze cone (5°), and clearly averted gaze (10°), we revealed that brain response to gaze at the edge of the gaze cone was similar to that produced by eye contact and different from that produced by averted gaze. Right fusiform gyrus and right superior temporal sulcus showed stronger activation when the gaze was averted as compared to eye contact. Gaze sensitive areas, however, were not affected by the portrait's presentation location. In sum, although the brain clearly distinguishes averted from centered gaze, a substantial change of vantage point does not alter neural activity, thus providing a possible explanation why the feeling of eye contact is upheld even in decentered stimulus positions. Hum Brain Mapp, 2014. © 2014 Wiley Periodicals, Inc.
    Human Brain Mapping 02/2015; 36(2). DOI:10.1002/hbm.22651 · 5.97 Impact Factor
  • Source
    • "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. "
    [Show abstract] [Hide abstract]
    ABSTRACT: Background: Gaze processing deficits are a seminal, early, and enduring behavioral deficit in autism spectrum disorder (ASD); however, a comprehensive characterization of the neural processes mediating abnormal gaze processing in ASD has yet to be conducted. Methods: This study investigated whole-brain patterns of neural synchrony during passive viewing of direct and averted eye gaze in ASD adolescents and young adults (M Age = 16.6) compared to neurotypicals (NT) (M Age = 17.5) while undergoing magnetoencephalography. Coherence between each pair of 54 brain regions within each of three frequency bands (low frequency (0 to 15 Hz), beta (15 to 30 Hz), and low gamma (30 to 45 Hz)) was calculated. Results: Significantly higher coherence and synchronization in posterior brain regions (temporo-parietal-occipital) across all frequencies was evident in ASD, particularly within the low 0 to 15 Hz frequency range. Higher coherence in fronto-temporo-parietal regions was noted in NT. A significantly higher number of low frequency cross-hemispheric synchronous connections and a near absence of right intra-hemispheric coherence in the beta frequency band were noted in ASD. Significantly higher low frequency coherent activity in bilateral temporo-parieto-occipital cortical regions and higher gamma band coherence in right temporo-parieto-occipital brain regions during averted gaze was related to more severe symptomology as reported on the Autism Diagnostic Interview-Revised (ADI-R). Conclusions: The preliminary results suggest a pattern of aberrant connectivity that includes higher low frequency synchronization in posterior cortical regions, lack of long-range right hemispheric beta and gamma coherence, and decreased coherence in fronto-temporo-parietal regions necessary for orienting to shifts in eye gaze in ASD; a critical behavior essential for social communication.
    Journal of Neurodevelopmental Disorders 06/2014; 6(1):15. DOI:10.1186/1866-1955-6-15 · 3.27 Impact Factor
  • Source
    • "Unlike typical individuals, ASD failed to show increased activation in the anterior insula for averted fearful gaze. The anterior insula, structurally connected with the posterior STS through the superior longitudinal fasciculus, is sensitive to the social significance of eye gaze [56]. The insular cortex has been associated with multiple functions, ranging from performance monitoring [57] and attention to sensory and sensorimotor processing [58], and the activation in the ventral part of the anterior insula observed in controls is likely related to socio-emotional processing [58], [59], that is absent in ASD. "
    [Show abstract] [Hide abstract]
    ABSTRACT: Intuitive grasping of the meaning of subtle social cues is particularly affected in autism spectrum disorders (ASD). Despite their relevance in social communication, the effect of averted gaze in fearful faces in conveying a signal of environmental threat has not been investigated using real face stimuli in adults with ASD. Here, using functional MRI, we show that briefly presented fearful faces with averted gaze, previously shown to be a strong communicative signal of environmental danger, produce different patterns of brain activation than fearful faces with direct gaze in a group of 26 normally intelligent adults with ASD compared with 26 matched controls. While implicit cue of threat produces brain activation in attention, emotion processing and mental state attribution networks in controls, this effect is absent in individuals with ASD. Instead, individuals with ASD show activation in the subcortical face-processing system in response to direct eye contact. An effect of differences in looking behavior was excluded in a separate eye tracking experiment. Our data suggest that individuals with ASD are more sensitive to direct eye contact than to social signals of danger conveyed by averted fearful gaze.
    PLoS ONE 12/2013; 8(12):e81206. DOI:10.1371/journal.pone.0081206 · 3.23 Impact Factor
Show more