Taking an “intentional stance” on eye-gaze shifts: A functional neuroimaging study of social perception in children

During middle childhood, children develop an increasing understanding of intentions and other social information conveyed through dynamic facial cues such as changes in eye-gaze direction. Recent work in our laboratory has focused on using functional magnetic resonance imaging (fMRI) in adults to map the neural circuitry subserving the visual analysis of others' actions and the intentions underlying these actions. In these studies, the superior temporal sulcus (STS) region has been continually implicated in processing shifts in eye gaze. Further, these studies have indicated that STS activity is modulated by the context within which eye-gaze shifts occur, suggesting that this region is involved in social perception via its role in the analysis of the intentions of observed actions. Still, no studies have investigated the neural circuitry supporting eye-gaze processing in children. We used event-related fMRI to examine brain activity in 7- to 10-year-old healthy children observing an animated virtual actor who shifted her eyes towards either a target object or empty space. Consistent with prior studies in adults, the STS, middle temporal gyrus, and inferior parietal lobule were sensitive to the intentions underlying the stimulus character's eye movements. These findings suggest that the neural circuitry underlying the processing of eye gaze and the detection of intentions conveyed through shifts in eye gaze in children are similar to that found previously in adults. We discuss these findings and potential implications for mapping the neurodevelopment of the social cognition and social perception abnormalities characteristic of autism.

[1]  D. Premack,et al.  Does the chimpanzee have a theory of mind? , 1978, Behavioral and Brain Sciences.

[2]  G. McCarthy,et al.  Neural basis of eye gaze processing deficits in autism. , 2005, Brain : a journal of neurology.

[3]  A. Hariri,et al.  Neural correlates of facial affect processing in children and adolescents with autism spectrum disorder. , 2004, Journal of the American Academy of Child and Adolescent Psychiatry.

[4]  A. Young,et al.  Understanding face recognition. , 1986, British journal of psychology.

[5]  James T. Voyvodic,et al.  Real-Time fMRI Paradigm Control, Physiology, and Behavior Combined with Near Real-Time Statistical Analysis , 1999, NeuroImage.

[6]  T. Allison,et al.  Brain activation evoked by perception of gaze shifts: the influence of context , 2003, Neuropsychologia.

[7]  Hua Guo,et al.  Single‐shot spiral image acquisition with embedded z‐shimming for susceptibility signal recovery , 2003, Journal of magnetic resonance imaging : JMRI.

[8]  E. Darcy Burgund,et al.  Comparison of functional activation foci in children and adults using a common stereotactic space , 2003, NeuroImage.

[9]  B. J. Casey,et al.  Amygdala response to fearful faces in anxious and depressed children. , 2001, Archives of general psychiatry.

[10]  T. Allison,et al.  Temporal Cortex Activation in Humans Viewing Eye and Mouth Movements , 1998, The Journal of Neuroscience.

[11]  Margot J. Taylor,et al.  Eyes first! Eye processing develops before face processing in children , 2001, Neuroreport.

[12]  P. Ekman Emotion in the human face , 1982 .

[13]  S. Baron-Cohen,et al.  The "Reading the Mind in the Eyes" Test revised version: a study with normal adults, and adults with Asperger syndrome or high-functioning autism. , 2001, Journal of child psychology and psychiatry, and allied disciplines.

[14]  J. Haxby,et al.  Distinct representations of eye gaze and identity in the distributed human neural system for face perception , 2000, Nature Neuroscience.

[15]  S. Baron-Cohen Mindblindness: An Essay on Autism and Theory of Mind , 1997 .

[16]  J. Decety,et al.  Brain Regions Involved in the Perception of Gaze: A PET Study , 1998, NeuroImage.

[17]  J. Talairach,et al.  Co-Planar Stereotaxic Atlas of the Human Brain: 3-Dimensional Proportional System: An Approach to Cerebral Imaging , 1988 .

[18]  C. Frith,et al.  Autism, Asperger syndrome and brain mechanisms for the attribution of mental states to animated shapes. , 2002, Brain : a journal of neurology.

[19]  G. Glover,et al.  Spiral‐in/out BOLD fMRI for increased SNR and reduced susceptibility artifacts , 2001, Magnetic resonance in medicine.

[20]  R. Buxton,et al.  The development of face and location processing: an fMRI study , 2003 .

[21]  S. Langton The Mutual Influence of Gaze and Head Orientation in the Analysis of Social Attention Direction , 2000, The Quarterly journal of experimental psychology. A, Human experimental psychology.

[22]  T. Allison,et al.  Social perception from visual cues: role of the STS region , 2000, Trends in Cognitive Sciences.

[23]  Jonathan D. Cohen,et al.  Improved Assessment of Significant Activation in Functional Magnetic Resonance Imaging (fMRI): Use of a Cluster‐Size Threshold , 1995, Magnetic resonance in medicine.

[24]  Kevin A. Pelphrey,et al.  Grasping the Intentions of Others: The Perceived Intentionality of an Action Influences Activity in the Superior Temporal Sulcus during Social Perception , 2004, Journal of Cognitive Neuroscience.

[25]  Mark H. Johnson,et al.  CONSPEC and CONLERN: a two-process theory of infant face recognition. , 1991, Psychological review.

[26]  G. McCarthy,et al.  When Strangers Pass , 2004, Psychological science.

[27]  V. Bruce,et al.  Do the eyes have it? Cues to the direction of social attention , 2000, Trends in Cognitive Sciences.

[28]  Monique Ernst,et al.  A developmental examination of gender differences in brain engagement during evaluation of threat , 2004, Biological Psychiatry.