Distinct Neural Systems Involved in Agency and Animacy Detection

We designed an fMRI experiment comparing perception of human faces and robotic faces producing emotional expressions. The purpose of our experiment was to investigate engagement of different parts of the social brain by viewing these animate and inanimate agents. Both human and robotic face expressions evoked activity in face-responsive regions in the fusiform gyrus and STS and in the putative human mirror neuron system. These results suggest that these areas mediate perception of agency, independently of whether the agents are living or not. By contrast, the human faces evoked stronger activity than did robotic faces in the medial pFC and the anterior temporal cortex—areas associated with the representation of others' mental states (theory of mind), whereas robotic faces evoked stronger activity in areas associated with perception of objects and mechanical movements. Our data demonstrate that the representation of the distinction between animate and inanimate agents involves areas that participate in attribution of mental stance.

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

[2]  James V. Haxby Social Neuroscience and the Representation of Others , 2011 .

[3]  L. Parsons,et al.  Use of implicit motor imagery for visual shape discrimination as revealed by PET , 1995, Nature.

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

[5]  J. Haxby,et al.  Distributed Neural Systems for Face Perception , 2011 .

[6]  Stephanie M. Curenton,et al.  Children's Understanding of the Animacy Constraint on Pretense. , 2000 .

[7]  J. Haxby,et al.  Parallel Visual Motion Processing Streams for Manipulable Objects and Human Movements , 2002, Neuron.

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

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

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

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

[12]  R. Baillargeon,et al.  Young infants’ reasoning about physical events involving inert and self-propelled objects , 2009, Cognitive Psychology.

[13]  Aina Puce,et al.  Audiovisual Non-Verbal Dynamic Faces Elicit Converging fMRI and ERP Responses , 2009, Brain Topography.

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

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

[16]  Alice J. O'Toole,et al.  Partially Distributed Representations of Objects and Faces in Ventral Temporal Cortex , 2005, Journal of Cognitive Neuroscience.

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

[18]  Maria Ida Gobbini,et al.  Distributed Process for Retrieval of Person Knowledge , 2011 .

[19]  K. Nakayama,et al.  RESPONSE PROPERTIES OF THE HUMAN FUSIFORM FACE AREA , 2000, Cognitive neuropsychology.

[20]  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.

[21]  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.

[23]  Iwan C. Pritchard,et al.  Animate and inanimate objects in human visual cortex: Evidence for task-independent category effects , 2009, Neuropsychologia.

[24]  Daniel D. Dilks,et al.  Differential selectivity for dynamic versus static information in face-selective cortical regions , 2011, NeuroImage.

[25]  Scott T. Grafton,et al.  Functional anatomy of pointing and grasping in humans. , 1996, Cerebral cortex.

[26]  Jason P. Mitchell,et al.  Distinct neural systems subserve person and object knowledge , 2002, Proceedings of the National Academy of Sciences of the United States of America.

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

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

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

[30]  Cynthia Breazeal,et al.  Designing sociable robots , 2002 .

[31]  Karl J. Friston,et al.  Evidence of Mirror Neurons in Human Inferior Frontal Gyrus , 2009, The Journal of Neuroscience.

[32]  A. Calder,et al.  Neural mechanisms of social attention , 2009, Trends in Cognitive Sciences.

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

[34]  Christian Keysers,et al.  The anthropomorphic brain: The mirror neuron system responds to human and robotic actions , 2007, NeuroImage.

[35]  M. Teresa Espinal,et al.  Le-predicates and event modification in Mexican Spanish , 2012 .

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

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

[38]  N. Kanwisher,et al.  A Cortical Area Selective for Visual Processing of the Human Body , 2001, Science.

[39]  James V. Haxby,et al.  Mirror Neuron System Differentially Activated by Facial Expressions and Social Hand Gestures: A Functional Magnetic Resonance Imaging Study , 2008, Journal of Cognitive Neuroscience.

[40]  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.

[41]  James V. Haxby,et al.  The Well-Tempered Social Brain , 2009, Psychological science.

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

[43]  C. Neil Macrae,et al.  General and specific contributions of the medial prefrontal cortex to knowledge about mental states , 2005, NeuroImage.

[44]  A. Caramazza,et al.  Domain-Specific Knowledge Systems in the Brain: The Animate-Inanimate Distinction , 1998, Journal of Cognitive Neuroscience.

[45]  Aaron C. Koralek,et al.  Two Takes on the Social Brain: A Comparison of Theory of Mind Tasks , 2007, Journal of Cognitive Neuroscience.

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

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

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

[49]  D. Norman Emotional design : why we love (or hate) everyday things , 2004 .

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

[51]  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.

[52]  C. Frith,et al.  Social Cognition in Humans , 2007, Current Biology.

[53]  Lola Cañamero,et al.  Emotion understanding from the perspective of autonomous robots research , 2005, Neural Networks.

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

[55]  J. Haxby,et al.  Neural response to the visual familiarity of faces , 2006, Brain Research Bulletin.

[56]  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.

[57]  Susan C. Johnson Detecting agents. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[58]  Karl J. Friston,et al.  Activation in Posterior Superior Temporal Sulcus Parallels Parameter Inducing the Percept of Animacy , 2005, Neuron.

[59]  Luciano Fadiga,et al.  Do We Really Need Vision? How Blind People “See” the Actions of Others , 2009, The Journal of Neuroscience.

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

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

[62]  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.

[63]  R W Cox,et al.  AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. , 1996, Computers and biomedical research, an international journal.

[64]  Stephen José Hanson,et al.  Combinatorial codes in ventral temporal lobe for object recognition: Haxby (2001) revisited: is there a “face” area? , 2004, NeuroImage.

[65]  A. Young,et al.  Reading the mind from eye gaze , 2002, Neuropsychologia.

[66]  G. Rizzolatti,et al.  Motor and cognitive functions of the ventral premotor cortex , 2002, Current Opinion in Neurobiology.

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

[68]  Joseph F. Engelberger,et al.  Robotics in Service , 1989 .

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

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

[71]  G. Rizzolatti,et al.  Neural Circuits Underlying Imitation Learning of Hand Actions An Event-Related fMRI Study , 2004, Neuron.

[72]  Comrie Bernard Language Universals and Linguistic Typology , 1982 .

[73]  Carlo Umiltà The Cambridge Handbook of Consciousness: Consciousness and Control of Action , 2007 .

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

[75]  Gregory S. Berns,et al.  You cannot gamble on others: Dissociable systems for strategic uncertainty and risk in the brain , 2013 .

[76]  Daniel L. Schwartz,et al.  Young Children's Understanding of Animacy and Entertainment Robots , 2006, Int. J. Humanoid Robotics.

[77]  Keiji Tanaka,et al.  Matching Categorical Object Representations in Inferior Temporal Cortex of Man and Monkey , 2008, Neuron.

[78]  Andrew D. Engell,et al.  Facial expression and gaze-direction in human superior temporal sulcus , 2007, Neuropsychologia.

[79]  Glyn W. Humphreys,et al.  Distinct neural substrates for the perception of real and virtual visual worlds , 2005, NeuroImage.

[80]  P. Dario,et al.  Mechanisms and Functions for a Humanoid Robot to Express Human-like Emotions , 2006 .