Grasping the Intentions of Others: The Perceived Intentionality of an Action Influences Activity in the Superior Temporal Sulcus during Social Perception

An explication of the neural substrates for social perception is an important component in the emerging field of social cognitive neuroscience and is relevant to the field of cognitive neuroscience as a whole. Prior studies from our laboratory have demonstrated that passive viewing of biological motion (Pelphrey, Mitchell, et al., 2003; Puce et al., 1998) activates the posterior superior temporal sulcus (STS) region. Furthermore, recent evidence has shown that the perceived context of observed gaze shifts (Pelphrey, Singerman, et al., 2003; Pelphrey et al., 2004) modulates STS activity. Here, using event-related functional magnetic resonance imaging at 4 T, we investigated brain activity in response to passive viewing of goal- and non-goal- directed reaching-to-grasp movements. Participants viewed an animated character making reaching-to-grasp movements either toward (correct) or away (incorrect) from a blinking dial. Both conditions evoked significant posterior STS activity that was strongly right lateralized. By examining the time course of the blood oxygenation level-dependent response from areas of activation, we observed a functional dissociation. Incorrect trials evoked significantly greater activity in the STS than did correct trials, while an area posterior and inferior to the STS (likely corresponding to the MT/V5 complex) responded equally to correct and incorrect movements. Parietal cortical regions, including the superior parietal lobule and the anterior intraparietal sulcus, also responded equally to correct and incorrect movements, but showed evidence for differential responding based on the hand and arm (left or right) of the animated character used to make the reaching-to-grasp movement. The results of this study further suggest that a region of the right posterior STS is involved in analyzing the intentions of other people's actions and that activity in this region is sensitive to the context of observed biological motions.

[1]  Karl J. Friston,et al.  A direct demonstration of functional specialization in human visual cortex , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[2]  R. Blake,et al.  Brain activity evoked by inverted and imagined biological motion , 2001, Vision Research.

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

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

[5]  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.

[6]  G. Rizzolatti,et al.  Action observation activates premotor and parietal areas in a somatotopic manner: an fMRI study , 2001, The European journal of neuroscience.

[7]  B. Bertenthal,et al.  Does Perception of Biological Motion Rely on Specific Brain Regions? , 2001, NeuroImage.

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

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

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

[11]  H. Bekkering,et al.  Imitation of gestures in children is goal-directed. , 2000, The Quarterly journal of experimental psychology. A, Human experimental psychology.

[12]  T. Goschke,et al.  Representation of intentions: Persisting activation in memory. , 1993 .

[13]  Alan C. Evans,et al.  Specific Involvement of Human Parietal Systems and the Amygdala in the Perception of Biological Motion , 1996, The Journal of Neuroscience.

[14]  D. Dennett The Intentional Stance. , 1987 .

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

[16]  M. Arbib,et al.  Language within our grasp , 1998, Trends in Neurosciences.

[17]  J C Mazziotta,et al.  Reafferent copies of imitated actions in the right superior temporal cortex , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[18]  R. Blake,et al.  Brain Areas Active during Visual Perception of Biological Motion , 2002, Neuron.

[19]  A. J. Mistlin,et al.  Visual analysis of body movements by neurones in the temporal cortex of the macaque monkey: A preliminary report , 1985, Behavioural Brain Research.

[20]  E. Spelke,et al.  The development of thoughts about animate and inanimate objects: Implications for research in social cognition , 1981 .

[21]  W. Prinz,et al.  Compatibility between Observed and Executed Finger Movements: Comparing Symbolic, Spatial, and Imitative Cues , 2000, Brain and Cognition.

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

[23]  Michael A. Arbib,et al.  Synthetic brain imaging: grasping, mirror neurons and imitation , 2000, Neural Networks.

[24]  J. Decety,et al.  Neural mechanisms subserving the perception of human actions , 1999, Trends in Cognitive Sciences.

[25]  P. Sinha,et al.  Functional neuroanatomy of biological motion perception in humans , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[26]  F. Heider,et al.  An experimental study of apparent behavior , 1944 .

[27]  A. Klin Attributing social meaning to ambiguous visual stimuli in higher-functioning autism and Asperger syndrome: The Social Attribution Task. , 2000, Journal of child psychology and psychiatry, and allied disciplines.

[28]  S. Wapner,et al.  Imitation of a model's hand movements: age changes in transposition of left-right relations. , 1968, Child development.

[29]  R. Adolphs Cognitive neuroscience: Cognitive neuroscience of human social behaviour , 2003, Nature Reviews Neuroscience.

[30]  J. Mazziotta,et al.  Cortical mechanisms of human imitation. , 1999, Science.

[31]  Ravi S. Menon,et al.  Visually guided grasping produces fMRI activation in dorsal but not ventral stream brain areas , 2003, Experimental Brain Research.

[32]  Richard S. J. Frackowiak,et al.  Area V5 of the human brain: evidence from a combined study using positron emission tomography and magnetic resonance imaging. , 1993, Cerebral cortex.

[33]  A. Meltzoff,et al.  The detection of contingency and animacy from simple animations in the human brain. , 2003, Cerebral cortex.

[34]  A. Dale,et al.  Visual motion aftereffect in human cortical area MT revealed by functional magnetic resonance imaging , 1995, Nature.

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

[36]  J. Decety,et al.  Does visual perception of object afford action? Evidence from a neuroimaging study , 2002, Neuropsychologia.

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

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

[39]  N. Kanwisher,et al.  Neuroimaging of cognitive functions in human parietal cortex , 2001, Current Opinion in Neurobiology.

[40]  D I Perrett,et al.  Frameworks of analysis for the neural representation of animate objects and actions. , 1989, The Journal of experimental biology.

[41]  John C. Gore,et al.  Brain activation associated with visual motion studied by functional magnetic resonance imaging in humans , 1994 .

[42]  Ruth Feldman,et al.  Maternal perception of infant intentionality at 4 and 8 months , 1996 .

[43]  Gregory McCarthy,et al.  Polysensory interactions along lateral temporal regions evoked by audiovisual speech. , 2003, Cerebral cortex.

[44]  H. Karnath New insights into the functions of the superior temporal cortex , 2001, Nature Reviews Neuroscience.

[45]  Gregory McCarthy,et al.  Taking an “intentional stance” on eye-gaze shifts: A functional neuroimaging study of social perception in children , 2005, NeuroImage.

[46]  Riitta Hari,et al.  Impaired Mirror-Image Imitation in Asperger and High-Functioning Autistic Subjects , 2003, Current Biology.

[47]  Gregory McCarthy,et al.  Regional Brain Activation Evoked When Approaching a Virtual Human on a Virtual Walk , 2005, Journal of Cognitive Neuroscience.