Dissociable Roles of the Superior Temporal Sulcus and the Intraparietal Sulcus in Joint Attention: A Functional Magnetic Resonance Imaging Study

Previous imaging work has shown that the superior temporal sulcus (STS) region and the intraparietal sulcus (IPS) are specifically activated during the passive observation of shifts in eye gaze [Pelphrey, K. A., Singerman, J. D., Allison, T., & McCarthy, G. Brain activation evoked by perception of gaze shifts: The influence of context. Neuropsychologia, 41, 156170, 2003; Hoffman, E. A., & Haxby, J. V. Distinct representations of eye gaze and identity in the distributed human neural system for face perception. Nature Neuroscience, 3, 8084, 2000; Puce, A., Allison, T., Bentin, S., Gore, J. C., & McCarthy, G. Temporal cortex activation in humans viewing eye and mouth movements. Journal of Neuroscience, 18, 21882199, 1998; Wicker, B., Michel, F., Henaff, M. A., & Decety, J. Brain regions involved in the perception of gaze: A PET study. Neuroimage, 8, 221227, 1998]. Are the same brain regions also involved in extracting gaze direction in order to establish joint attention? In an event-related functional magnetic resonance imaging experiment, healthy human subjects actively followed the directional cue provided by the eyes of another person toward an object in space or, in the control condition, used a nondirectional symbolic cue to make an eye movement toward an object in space. Our results show that the posterior part of the STS region and the cuneus are specifically involved in extracting and using detailed directional information from the eyes of another person to redirect one's own gaze and establish joint attention. The IPS, on the other hand, seems to be involved in encoding spatial direction and mediating shifts of spatial attention independent of the type of cue that triggers this process.

[1]  D I Perrett,et al.  Organization and functions of cells responsive to faces in the temporal cortex. , 1992, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

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

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

[4]  Dan Milea,et al.  Cortical Mechanisms of Saccade Generation from Execution to Decision , 2005, Annals of the New York Academy of Sciences.

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

[6]  N. Emery,et al.  The eyes have it: the neuroethology, function and evolution of social gaze , 2000, Neuroscience & Biobehavioral Reviews.

[7]  S Baron-Cohen,et al.  Psychological markers in the detection of autism in infancy in a large population. , 1996, The British journal of psychiatry : the journal of mental science.

[8]  A. J. Mistlin,et al.  Visual cells in the temporal cortex sensitive to face view and gaze direction , 1985, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[9]  L. Adamson,et al.  Coordinating attention to people and objects in mother-infant and peer-infant interaction. , 1984, Child development.

[10]  T. Kemper,et al.  Histoanatomic observations of the brain in early infantile autism , 1985, Neurology.

[11]  I. Wilkinson,et al.  Investigating the functional anatomy of empathy and forgiveness , 2001, Neuroreport.

[12]  R. J. Seitz,et al.  Activation of frontoparietal cortices during memorized triple‐step sequences of saccadic eye movements: an fMRI study , 2001, The European journal of neuroscience.

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

[14]  P. Thuras,et al.  Purkinje Cell Size Is Reduced in Cerebellum of Patients with Autism , 2002, Cellular and Molecular Neurobiology.

[15]  T. Allison,et al.  Functional anatomy of biological motion perception in posterior temporal cortex: an FMRI study of eye, mouth and hand movements. , 2005, Cerebral cortex.

[16]  Richard S. Frackowiak,et al.  Superior temporal sulcus anatomical abnormalities in childhood autism: a voxel-based morphometry MRI study , 2004, NeuroImage.

[17]  E Courchesne,et al.  Parietal lobe abnormalities detected with MR in patients with infantile autism. , 1993, AJR. American journal of roentgenology.

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

[19]  Karl J. Friston,et al.  Statistical parametric mapping , 2013 .

[20]  A. Karmiloff-Smith,et al.  Are children with autism blind to the mentalistic significance of the eyes , 1995 .

[21]  Clinton D. Kilts,et al.  Dissociable Neural Pathways Are Involved in the Recognition of Emotion in Static and Dynamic Facial Expressions , 2003, NeuroImage.

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

[23]  Tony Charman,et al.  Why is joint attention a pivotal skill in autism? , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[24]  A. Scheibel,et al.  Lower Purkinje cell counts in the cerebella of four autistic subjects: initial findings of the UCLA-NSAC Autopsy Research Report. , 1986, The American journal of psychiatry.

[26]  G. Fink,et al.  Being with virtual others: Neural correlates of social interaction , 2006, Neuropsychologia.

[27]  E. Courchesne,et al.  Why the frontal cortex in autism might be talking only to itself: local over-connectivity but long-distance disconnection , 2005, Current Opinion in Neurobiology.

[28]  D. Perrett,et al.  Being the target of another’s emotion: a PET study , 2003, Neuropsychologia.

[29]  T. Allison,et al.  Brain Activity Evoked by the Perception of Human Walking: Controlling for Meaningful Coherent Motion , 2003, The Journal of Neuroscience.

[30]  D. Gitelman,et al.  Covert Visual Spatial Orienting and Saccades: Overlapping Neural Systems , 2000, NeuroImage.

[31]  C. Moore,et al.  The origins of joint visual attention in infants. , 1998, Developmental psychology.

[32]  Frank Bremmer,et al.  The encoding of saccadic eye movements within human posterior parietal cortex , 2004, NeuroImage.

[33]  Á. Pascual-Leone,et al.  Repetitive TMS over posterior STS disrupts perception of biological motion , 2005, Vision Research.

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

[35]  A. Treves,et al.  Morphing Marilyn into Maggie dissociates physical and identity face representations in the brain , 2005, Nature Neuroscience.

[36]  C. Moore,et al.  Attention and joint attention in preschool children with autism. , 2000, Developmental psychology.

[37]  Arthur W Toga,et al.  Cortical sulcal maps in autism. , 2003, Cerebral cortex.

[38]  J. Haxby,et al.  fMRI Responses to Video and Point-Light Displays of Moving Humans and Manipulable Objects , 2003, Journal of Cognitive Neuroscience.

[39]  K. Paller,et al.  Brain networks for analyzing eye gaze. , 2003, Brain research. Cognitive brain research.

[40]  K. Nakamura,et al.  The human amygdala plays an important role in gaze monitoring. A PET study. , 1999, Brain : a journal of neurology.

[41]  R. Blake,et al.  Brain Areas Involved in Perception of Biological Motion , 2000, Journal of Cognitive Neuroscience.

[42]  E. Bullmore,et al.  Social intelligence in the normal and autistic brain: an fMRI study , 1999, The European journal of neuroscience.

[43]  J. Bruner,et al.  The capacity for joint visual attention in the infant , 1975, Nature.

[44]  C. Moore,et al.  Targets and cues: gaze-following in children with autism. , 1998, Journal of child psychology and psychiatry, and allied disciplines.

[45]  D. V. van Essen,et al.  Windows on the brain: the emerging role of atlases and databases in neuroscience , 2002, Current Opinion in Neurobiology.

[46]  U. Frith,et al.  Vagaries of Visual Perception in Autism , 2005, Neuron.

[47]  G. Leichnetz.  Connections of the medial posterior parietal cortex (area 7m) in the monkey , 2001, The Anatomical record.

[48]  Jean-Luc Anton,et al.  Region of interest analysis using an SPM toolbox , 2010 .

[49]  David C. Van Essen,et al.  A Population-Average, Landmark- and Surface-based (PALS) atlas of human cerebral cortex , 2005, NeuroImage.

[50]  Rebecca Elliott,et al.  Neuronal correlates of theory of mind and empathy: A functional magnetic resonance imaging study in a nonverbal task , 2006, NeuroImage.

[51]  A. Cavanna,et al.  The precuneus: a review of its functional anatomy and behavioural correlates. , 2006, Brain : a journal of neurology.

[52]  J V Haxby,et al.  Dissociation of saccade-related and pursuit-related activation in human frontal eye fields as revealed by fMRI. , 1997, Journal of neurophysiology.

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

[54]  S. Baron-Cohen,et al.  Gaze Perception Triggers Reflexive Visuospatial Orienting , 1999 .

[55]  Karl J. Friston,et al.  How Many Subjects Constitute a Study? , 1999, NeuroImage.

[56]  A. Cowey,et al.  Sensitivity to eye gaze in prosopagnosic patients and monkeys with superior temporal sulcus ablation , 1990, Neuropsychologia.