Two Takes on the Social Brain: A Comparison of Theory of Mind Tasks

We compared two tasks that are widely used in research on mentalizingfalse belief stories and animations of rigid geometric shapes that depict social interactionsto investigate whether the neural systems that mediate the representation of others' mental states are consistent across these tasks. Whereas false belief stories activated primarily the anterior paracingulate cortex (APC), the posterior cingulate cortex/precuneus (PCC/PC), and the temporo-parietal junction (TPJ)components of the distributed neural system for theory of mind (ToM)the social animations activated an extensive region along nearly the full extent of the superior temporal sulcus, including a locus in the posterior superior temporal sulcus (pSTS), as well as the frontal operculum and inferior parietal lobule (IPL)components of the distributed neural system for action understandingand the fusiform gyrus. These results suggest that the representation of covert mental states that may predict behavior and the representation of intentions that are implied by perceived actions involve distinct neural systems. These results show that the TPJ and the pSTS play dissociable roles in mentalizing and are parts of different distributed neural systems. Because the social animations do not depict articulated body movements, these results also highlight that the perception of the kinematics of actions is not necessary to activate the mirror neuron system, suggesting that this system plays a general role in the representation of intentions and goals of actions. Furthermore, these results suggest that the fusiform gyrus plays a general role in the representation of visual stimuli that signify agency, independent of visual form.

[1]  John R. Searle,et al.  The Intentionality of Intention and Action , 1980, Cogn. Sci..

[2]  R. E Passingham,et al.  Inferring false beliefs from the actions of oneself and others: an fMRI study , 2004, NeuroImage.

[3]  F. Binkofski,et al.  The mirror neuron system and action recognition , 2004, Brain and Language.

[4]  A. Leslie Pretense and representation: The origins of "theory of mind." , 1987 .

[5]  N. Andreasen,et al.  Visualizing how one brain understands another: a PET study of theory of mind. , 2003, The American journal of psychiatry.

[6]  G. Rizzolatti,et al.  I Know What You Are Doing A Neurophysiological Study , 2001, Neuron.

[7]  C. Frith,et al.  Meeting of minds: the medial frontal cortex and social cognition , 2006, Nature Reviews Neuroscience.

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

[9]  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.

[10]  E. Procyk,et al.  Brain activity during observation of actions. Influence of action content and subject's strategy. , 1997, Brain : a journal of neurology.

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

[12]  N. Kanwisher,et al.  The Fusiform Face Area: A Module in Human Extrastriate Cortex Specialized for Face Perception , 1997, The Journal of Neuroscience.

[13]  Yasuhiro Maeda,et al.  Anatomical Segregation of Representations of Personally Familiar and Famous People in the Temporal and Parietal Cortices , 2009, Journal of Cognitive Neuroscience.

[14]  J. Haxby,et al.  The distributed human neural system for face perception , 2000, Trends in Cognitive Sciences.

[15]  J. Mazziotta,et al.  Grasping the Intentions of Others with One's Own Mirror Neuron System , 2005, PLoS biology.

[16]  A. Bailey,et al.  Are there theory of mind regions in the brain? A review of the neuroimaging literature , 2009, Human brain mapping.

[17]  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.

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

[19]  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.

[20]  A. Meltzoff,et al.  A PET Exploration of the Neural Mechanisms Involved in Reciprocal Imitation , 2002, NeuroImage.

[21]  Rebecca Saxe,et al.  The neural basis of belief encoding and integration in moral judgment , 2008, NeuroImage.

[22]  Henrik Walter,et al.  Understanding Intentions in Social Interaction: The Role of the Anterior Paracingulate Cortex , 2004, Journal of Cognitive Neuroscience.

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

[24]  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.

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

[26]  D G Pelli,et al.  The VideoToolbox software for visual psychophysics: transforming numbers into movies. , 1997, Spatial vision.

[27]  Nicola Vanello,et al.  Differential modulation of neural activity throughout the distributed neural system for face perception in patients with Social Phobia and healthy subjects , 2008, Brain Research Bulletin.

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

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

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

[31]  E. Leibenluft,et al.  Mothers' neural activation in response to pictures of their children and other children , 2004, Biological Psychiatry.

[32]  Frank C Keil,et al.  Reflections of other minds: how primate social cognition can inform the function of mirror neurons , 2006, Current Opinion in Neurobiology.

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

[34]  R Saxe,et al.  People thinking about thinking people The role of the temporo-parietal junction in “theory of mind” , 2003, NeuroImage.

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

[36]  K. Richard,et al.  Adsorption of Palm Oil Carotene and Free Fatty Acids onto Acid Activated Cameroonian Clays , 2007 .

[37]  T. Allison,et al.  Face-Specific Processing in the Human Fusiform Gyrus , 1997, Journal of Cognitive Neuroscience.

[38]  P. Downing,et al.  Selectivity for the human body in the fusiform gyrus. , 2005, Journal of neurophysiology.

[39]  M. Milders,et al.  Frontal operculum temporal difference signals and social motor response learning , 2009, Human brain mapping.

[40]  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.

[41]  Michael X. Cohen,et al.  Gamma-band activity in the human superior temporal sulcus during mentalizing from nonverbal social cues. , 2009, Psychophysiology.

[42]  G. Rizzolatti,et al.  The mirror-neuron system. , 2004, Annual review of neuroscience.

[43]  K. Doya,et al.  A unifying computational framework for motor control and social interaction. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[44]  I. Gauthier,et al.  Expertise for cars and birds recruits brain areas involved in face recognition , 2000, Nature Neuroscience.

[45]  V. Gallese The Roots of Empathy: The Shared Manifold Hypothesis and the Neural Basis of Intersubjectivity , 2003, Psychopathology.

[46]  Richard S. J. Frackowiak,et al.  Other minds in the brain: a functional imaging study of “theory of mind” in story comprehension , 1995, Cognition.

[47]  Andrew D. Engell,et al.  The Neural Bases of Cognitive Conflict and Control in Moral Judgment , 2004, Neuron.

[48]  J. Haxby,et al.  Neural systems for recognition of familiar faces , 2007, Neuropsychologia.

[49]  F. Happé An advanced test of theory of mind: Understanding of story characters' thoughts and feelings by able autistic, mentally handicapped, and normal children and adults , 1994, Journal of autism and developmental disorders.

[50]  Jason P. Mitchell,et al.  Dissociable Medial Prefrontal Contributions to Judgments of Similar and Dissimilar Others , 2006, Neuron.

[51]  Lindsey J. Powell,et al.  It's the Thought That Counts , 2006, Psychological science.

[52]  L L Chao,et al.  Are face-responsive regions selective only for faces? , 1999, Neuroreport.

[53]  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.

[54]  C. Frith,et al.  Reading the mind in cartoons and stories: an fMRI study of ‘theory of mind’ in verbal and nonverbal tasks , 2000, Neuropsychologia.

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

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

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

[58]  Kimberly J. Montgomery,et al.  Communicative hand gestures and object-directed hand movements activated the mirror neuron system. , 2007, Social cognitive and affective neuroscience.

[59]  Scott T. Grafton,et al.  Localization of grasp representations in humans by positron emission tomography , 1996, Experimental Brain Research.

[60]  M. Sereno,et al.  Point-Light Biological Motion Perception Activates Human Premotor Cortex , 2004, The Journal of Neuroscience.

[61]  G. Rizzolatti,et al.  Action recognition in the premotor cortex. , 1996, Brain : a journal of neurology.

[62]  J. Mandler How to build a baby: II. Conceptual primitives. , 1992, Psychological review.

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

[64]  Alison J. Wiggett,et al.  Patterns of fMRI Activity Dissociate Overlapping Functional Brain Areas that Respond to Biological Motion , 2006, Neuron.

[65]  M. Corbetta,et al.  The Reorienting System of the Human Brain: From Environment to Theory of Mind , 2008, Neuron.

[66]  C. Frith,et al.  Interacting minds--a biological basis. , 1999, Science.

[67]  D H Brainard,et al.  The Psychophysics Toolbox. , 1997, Spatial vision.

[68]  Alison Gopnik,et al.  Toddlers' understanding of intentions, desires and emotions: Explorations of the dark ages. , 1999 .

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

[70]  J. O'Doherty,et al.  Automatic and intentional brain responses during evaluation of trustworthiness of faces , 2002, Nature Neuroscience.

[71]  Ellen Leibenluft,et al.  Social and emotional attachment in the neural representation of faces , 2004, NeuroImage.

[72]  E. Bullmore,et al.  Activation of auditory cortex during silent lipreading. , 1997, Science.

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

[74]  M. Petrides Comparative architectonic analysis of the human and the macaque frontal cortex , 1994 .

[75]  A. Leslie Pretending and believing: issues in the theory of ToMM , 1994, Cognition.

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

[77]  Geoffrey K. Aguirre,et al.  Imaging visual recognition: PET and fMRI studies of the functional anatomy of human visual recognition , 1999, Trends in Cognitive Sciences.

[78]  J. Decety,et al.  The effects of learning and intention on the neural network involved in the perception of meaningless actions. , 1999, Brain : a journal of neurology.

[79]  G. Rizzolatti,et al.  Understanding motor events: a neurophysiological study , 2004, Experimental Brain Research.

[80]  M. Tarr,et al.  Activation of the middle fusiform 'face area' increases with expertise in recognizing novel objects , 1999, Nature Neuroscience.

[81]  G. Rizzolatti,et al.  Parietal Lobe: From Action Organization to Intention Understanding , 2005, Science.

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