Paying attention to social meaning: an FMRI study.

Animations of simple geometric shapes are readily interpreted as animate agents engaged in meaningful social interactions. Such animations have been shown to activate brain regions implicated in the detection of animate motion, in understanding the intentions of others as well as areas commonly linked to the processing of social and emotional information. However, attribution of animacy does not occur under all circumstances and the precise conditions under which specific regions are activated remains unclear. In a functional magnetic resonance imaging study we manipulated viewers' perspective to assess the part played by selective attention. Participants were cued to attend either to spatial properties of the movements or to the kind of social behavior it could represent. Activations that occurred to the initial cue, while observing the animations themselves and while responding to a postpresentation probe, were analyzed separately. Results showed that activity in the social brain network was strongly influenced by selective attention, and that remarkably similar activations were seen during film viewing and in response to probe questions. Our use of stimuli supporting rich and diverse social narratives likely enhanced the influence of top-down processes on neural activity in the social brain.

[1]  Rebecca Saxe,et al.  Dissociation between emotion and personality judgments: Convergent evidence from functional neuroimaging , 2005, NeuroImage.

[2]  David Premack,et al.  Origins of human social competence. , 1995 .

[3]  Geoffrey Bird,et al.  Attention does not modulate neural responses to social stimuli in autism spectrum disorders , 2006, NeuroImage.

[4]  Patrice D. Tremoulet,et al.  Perceptual causality and animacy , 2000, Trends in Cognitive Sciences.

[5]  J. Cacioppo,et al.  On seeing human: a three-factor theory of anthropomorphism. , 2007, Psychological review.

[6]  Jason P. Mitchell Activity in right temporo-parietal junction is not selective for theory-of-mind. , 2008, Cerebral cortex.

[7]  R. Cabeza,et al.  Imaging Cognition II: An Empirical Review of 275 PET and fMRI Studies , 2000, Journal of Cognitive Neuroscience.

[8]  T. Heatherton,et al.  Detecting agency from the biological motion of veridical vs animated agents. , 2007, Social cognitive and affective neuroscience.

[9]  Daniel Tranel,et al.  Amygdala damage impairs emotional memory for gist but not details of complex stimuli , 2005, Nature Neuroscience.

[10]  Kenji Kawano,et al.  Global and fine information coded by single neurons in the temporal visual cortex , 1999, Nature.

[11]  P. Barnard,et al.  Autobiographical memory and daily schemas at work. , 1994, Memory.

[12]  Kiyotaka Nemoto,et al.  The neural network for the mirror system and mentalizing in normally developed children: an fMRI study , 2004, Neuroreport.

[13]  Alan Kingstone,et al.  The eyes have it!: An fMRI investigation , 2004, Brain and Cognition.

[14]  Juha Silvanto,et al.  Stimulation of the human frontal eye fields modulates sensitivity of extrastriate visual cortex. , 2006, Journal of neurophysiology.

[15]  A P Leff,et al.  Impaired reading in patients with right hemianopia , 2000, Annals of neurology.

[16]  E. Maguire,et al.  The functional neuroanatomy of comprehension and memory: the importance of prior knowledge. , 1999, Brain : a journal of neurology.

[17]  Karl J. Friston,et al.  A unified statistical approach for determining significant signals in images of cerebral activation , 1996, Human brain mapping.

[18]  Jeffrey M. Zacks,et al.  Human Brain Activity Time-Locked to Narrative Event Boundaries , 2007, Psychological science.

[19]  J. Duncan,et al.  Common regions of the human frontal lobe recruited by diverse cognitive demands , 2000, Trends in Neurosciences.

[20]  James L. McClelland,et al.  The parallel distributed processing approach to semantic cognition , 2003, Nature Reviews Neuroscience.

[21]  P. Todd,et al.  Accurate judgments of intention from motion cues alone: A cross-cultural study , 2005 .

[22]  Marcus E Raichle,et al.  Intrinsic brain activity sets the stage for expression of motivated behavior , 2005, The Journal of comparative neurology.

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

[24]  R. Dolan,et al.  The Kuleshov Effect: the influence of contextual framing on emotional attributions. , 2006, Social cognitive and affective neuroscience.

[25]  Jordan Grafman,et al.  Social concepts are represented in the superior anterior temporal cortex , 2007, Proceedings of the National Academy of Sciences.

[26]  Thomas M. Moerland,et al.  Fate of unattended fearful faces in the amygdala is determined by both attentional resources and cognitive modulation , 2005, NeuroImage.

[27]  Alison J. Wiggett,et al.  Behavioral / Systems / Cognitive Functional Magnetic Resonance Imaging Investigation of Overlapping Lateral Occipitotemporal Activations Using Multi-Voxel Pattern Analysis , 2006 .

[28]  Ralph Adolphs,et al.  Impaired spontaneous anthropomorphizing despite intact perception and social knowledge. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[29]  N. Tzourio-Mazoyer,et al.  Automated Anatomical Labeling of Activations in SPM Using a Macroscopic Anatomical Parcellation of the MNI MRI Single-Subject Brain , 2002, NeuroImage.

[30]  Christopher D. Frith,et al.  Imaging the Intentional Stance in a Competitive Game , 2002, NeuroImage.

[31]  Jordan Grafman,et al.  Handbook of Neuropsychology , 1991 .

[32]  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.

[33]  Bridgette A. Martin,et al.  Segmenting Ambiguous Events , 2003 .

[34]  James K Rilling,et al.  The neural correlates of theory of mind within interpersonal interactions , 2004, NeuroImage.

[35]  Chris Rorden,et al.  Spatial Normalization of Brain Images with Focal Lesions Using Cost Function Masking , 2001, NeuroImage.

[36]  B. Levine,et al.  The functional neuroanatomy of autobiographical memory: A meta-analysis , 2006, Neuropsychologia.

[37]  Matthew Brett,et al.  An Evaluation of the Use of Magnetic Field Maps to Undistort Echo-Planar Images , 2003, NeuroImage.

[38]  Jodie A. Baird,et al.  Discerning intentions in dynamic human action , 2001, Trends in Cognitive Sciences.

[39]  P. Skudlarski,et al.  The role of the fusiform face area in social cognition: implications for the pathobiology of autism. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[40]  D. Amaral,et al.  The Amygdala, Social Behavior, and Danger Detection , 2003, Annals of the New York Academy of Sciences.

[41]  Jeffrey M. Zacks,et al.  Human brain activity time-locked to perceptual event boundaries , 2001, Nature Neuroscience.

[42]  G. V. Simpson,et al.  Preparatory deployment of attention to motion activates higher-order motion-processing brain regions , 2004, NeuroImage.

[43]  Alex Martin,et al.  NEURAL FOUNDATIONS FOR UNDERSTANDING SOCIAL AND MECHANICAL CONCEPTS , 2003, Cognitive neuropsychology.

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

[45]  Mitsuo Kawato,et al.  Activation of the Human Superior Temporal Gyrus during Observation of Goal Attribution by Intentional Objects , 2004, Journal of Cognitive Neuroscience.

[46]  Istvan Molnar-Szakacs,et al.  Watching social interactions produces dorsomedial prefrontal and medial parietal BOLD fMRI signal increases compared to a resting baseline , 2004, NeuroImage.

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

[48]  R. Cabeza,et al.  Imaging Cognition: An Empirical Review of PET Studies with Normal Subjects , 1997, Journal of Cognitive Neuroscience.

[49]  Philip J. Barnard,et al.  Affect, Cognition and Change: Re-Modelling Depressive Thought , 1993 .

[50]  P. Cavanagh,et al.  Cortical fMRI activation produced by attentive tracking of moving targets. , 1998, Journal of neurophysiology.

[51]  E. Bizzi,et al.  The Cognitive Neurosciences , 1996 .

[52]  R. Saxe Uniquely human social cognition , 2006, Current Opinion in Neurobiology.

[53]  Daniel Houser,et al.  A functional imaging study of cooperation in two-person reciprocal exchange , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[54]  Darren Newtson An Interactionist Perspective on Social Knowing , 1980 .

[55]  Mahzarin R. Banaji,et al.  Encoding-Specific Effects of Social Cognition on the Neural Correlates of Subsequent Memory , 2004, The Journal of Neuroscience.

[56]  Anthony R. McIntosh,et al.  Parallel networks operating across attentional deployment and motion processing: A multi-seed partial least squares fMRI study , 2006, NeuroImage.

[57]  S. G. Cox,et al.  Functional MRI study of the cognitive generation of affect. , 1999, The American journal of psychiatry.

[58]  S. Fiske,et al.  Comprar Social Beings: A Core Motives Approach to Social Psychology | Benjamin L. Miller | 9780470129111 | Wiley , 2009 .

[59]  C. Frith,et al.  Movement and Mind: A Functional Imaging Study of Perception and Interpretation of Complex Intentional Movement Patterns , 2000, NeuroImage.

[60]  Shawn C. Milleville,et al.  Understanding Animate Agents , 2007, Psychological science.

[61]  M. Corbetta,et al.  Control of goal-directed and stimulus-driven attention in the brain , 2002, Nature Reviews Neuroscience.

[62]  Pascal Boyer,et al.  How the brain perceives causality: an event-related fMRI study , 2001, Neuroreport.

[63]  B. Parkinson Ideas and realities of emotion , 1995 .

[64]  C. Frith,et al.  Development and neurophysiology of mentalizing. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[65]  J. Bargh What have we been priming all these years? On the development, mechanisms, and ecology of nonconscious social behavior. , 2006, European journal of social psychology.

[66]  G. Glover,et al.  Reflecting upon Feelings: An fMRI Study of Neural Systems Supporting the Attribution of Emotion to Self and Other , 2004, Journal of Cognitive Neuroscience.

[67]  Joseph T. Devlin,et al.  Orienting attention to semantic categories , 2006, NeuroImage.

[68]  C. Frith,et al.  How we predict what other people are going to do , 2006, Brain Research.

[69]  M. Behrmann,et al.  Seeing it differently: visual processing in autism , 2006, Trends in Cognitive Sciences.

[70]  Dharshan Kumaran,et al.  The Human Hippocampus: Cognitive Maps or Relational Memory? , 2005, The Journal of Neuroscience.

[71]  R. Buckner,et al.  Self-projection and the brain , 2007, Trends in Cognitive Sciences.

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

[73]  J. Lancaster,et al.  Using the talairach atlas with the MNI template , 2001, NeuroImage.