An integrative model of the neural systems supporting the comprehension of observed emotional behavior

Understanding others' emotions requires both the identification of overt behaviors ("smiling") and the attribution of behaviors to a cause ("friendly disposition"). Previous research suggests that whereas emotion identification depends on a cortical mirror system that enables the embodiment of observed motor behavior within one's own motor system, causal attribution for emotion depends on a separate cortical mentalizing system, so-named because its function is associated with mental state representation. We used fMRI to test an Identification-Attribution model of mirror and mentalizing system contributions to the comprehension of emotional behavior. Normal volunteers watched a set of ecologically valid videos of human emotional displays. During each viewing, volunteers either identified an emotion-relevant motor behavior (explicit identification) or inferred a plausible social cause (explicit attribution). These explicit identification and attribution goals strongly distinguished activity in the mirror and mentalizing systems, respectively. However, frontal mirror areas, though preferentially engaged by the identification goal, nevertheless exhibited activation when observers possessed the attribution goal. One of these areas-right posterior inferior frontal gyrus-demonstrated effective connectivity with areas of the mentalizing system during attributional processing. These results support an integrative model of the neural systems supporting the comprehension of emotional behavior, where the mirror system helps facilitate the rapid identification of emotional expressions that then serve as inputs to attributional processing in the mentalizing system.

[1]  Dennis C. Tkach,et al.  Congruent Activity during Action and Action Observation in Motor Cortex , 2007, The Journal of Neuroscience.

[2]  S. Fiske,et al.  The Handbook of Social Psychology , 1935 .

[3]  Jason P. Mitchell Inferences about mental states , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[4]  V. Ramachandran,et al.  The simulating social mind: the role of the mirror neuron system and simulation in the social and communicative deficits of autism spectrum disorders. , 2007, Psychological bulletin.

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

[6]  J. Mattingley,et al.  The role of selective attention in matching observed and executed actions , 2009, Neuropsychologia.

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

[8]  Robert P. Spunt,et al.  Dissociable Neural Systems Support Retrieval of How and Why Action Knowledge , 2010, Psychological science.

[9]  David T. Neal,et al.  Embodied Emotion Perception , 2011 .

[10]  J. Aharon-Peretz,et al.  Two systems for empathy: a double dissociation between emotional and cognitive empathy in inferior frontal gyrus versus ventromedial prefrontal lesions. , 2009, Brain : a journal of neurology.

[11]  K. Ochsner,et al.  The Need for a Cognitive Neuroscience of Naturalistic Social Cognition , 2009, Annals of the New York Academy of Sciences.

[12]  R. Blair Responding to the emotions of others: Dissociating forms of empathy through the study of typical and psychiatric populations , 2005, Consciousness and Cognition.

[13]  Cecilia Heyes,et al.  Mesmerising mirror neurons , 2010, NeuroImage.

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

[15]  R. Saxe Against simulation: the argument from error , 2005, Trends in Cognitive Sciences.

[16]  Marcel Brass,et al.  Control of shared representations relies on key processes involved in mental state attribution , 2009, Human brain mapping.

[17]  Frank Van Overwalle,et al.  Understanding others' actions and goals by mirror and mentalizing systems: A meta-analysis , 2009, NeuroImage.

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

[19]  G. Rizzolatti,et al.  A unifying view of the basis of social cognition , 2004, Trends in Cognitive Sciences.

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

[21]  Pierre Rainville,et al.  Brain responses to facial expressions of pain: Emotional or motor mirroring? , 2010, NeuroImage.

[22]  H. Kelley The processes of causal attribution. , 1973 .

[23]  C. Keysers,et al.  Integrating simulation and theory of mind: from self to social cognition , 2007, Trends in Cognitive Sciences.

[24]  Keith Oatley,et al.  The Function of Fiction is the Abstraction and Simulation of Social Experience , 2008, Perspectives on psychological science : a journal of the Association for Psychological Science.

[25]  M. Mermillod,et al.  Is eye contact the key to the social brain? , 2010, Behavioral and Brain Sciences.

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

[27]  Gregory Hickok,et al.  Eight Problems for the Mirror Neuron Theory of Action Understanding in Monkeys and Humans , 2009, Journal of Cognitive Neuroscience.

[28]  N. Bolger,et al.  The neural bases of empathic accuracy , 2009, Proceedings of the National Academy of Sciences.

[29]  Karl J. Friston,et al.  Psychophysiological and Modulatory Interactions in Neuroimaging , 1997, NeuroImage.

[30]  S. Preston,et al.  Empathy: Its ultimate and proximate bases. , 2001, The Behavioral and brain sciences.

[31]  U. Dimberg,et al.  Unconscious Facial Reactions to Emotional Facial Expressions , 2000, Psychological science.

[32]  Maurizio Corbetta,et al.  The human brain is intrinsically organized into dynamic, anticorrelated functional networks. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[33]  Jamil Zaki,et al.  The Cognitive Neuroscience of Sharing and Understanding Others’ Emotions , 2011 .

[34]  Matthew D. Lieberman,et al.  Identifying the What, Why, and How of an Observed Action: An fMRI Study of Mentalizing and Mechanizing during Action Observation , 2011, Journal of Cognitive Neuroscience.

[35]  J. Mazziotta,et al.  Neural mechanisms of empathy in humans: A relay from neural systems for imitation to limbic areas , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[36]  Ruth Seurinck,et al.  Spontaneous and intentional trait inferences recruit a common mentalizing network to a different degree: Spontaneous inferences activate only its core areas , 2011, Social neuroscience.

[37]  M. Brass,et al.  Investigating Action Understanding: Inferential Processes versus Action Simulation , 2007, Current Biology.

[38]  A. Hamilton,et al.  Unbroken mirrors: challenging a theory of Autism , 2008, Trends in Cognitive Sciences.

[39]  Roel M. Willems,et al.  Complementary Systems for Understanding Action Intentions , 2008, Current Biology.

[40]  Thomas E. Nichols,et al.  Optimization of experimental design in fMRI: a general framework using a genetic algorithm , 2003, NeuroImage.

[41]  Gereon R. Fink,et al.  End or Means—The “What” and “How” of Observed Intentional Actions , 2009, Journal of Cognitive Neuroscience.

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

[43]  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.

[44]  K. Ochsner,et al.  Reintegrating the Study of Accuracy Into Social Cognition Research , 2011 .

[45]  John Suckling,et al.  Shared Neural Circuits for Mentalizing about the Self and Others , 2010, Journal of Cognitive Neuroscience.

[46]  C. Frith,et al.  The Neural Basis of Mentalizing , 2006, Neuron.

[47]  Arne D. Ekstrom,et al.  Single-Neuron Responses in Humans during Execution and Observation of Actions , 2010, Current Biology.

[48]  Ingrid E. Scheffer,et al.  Mirror neuron system involvement in empathy: A critical look at the evidence , 2011, Social neuroscience.

[49]  J. Decety To What Extent is the Experience of Empathy Mediated by Shared Neural Circuits? , 2010 .

[50]  M. Jeannerod,et al.  The motor theory of social cognition: a critique , 2005, Trends in Cognitive Sciences.

[51]  Jan Gläscher,et al.  Visualization of Group Inference Data in Functional Neuroimaging , 2009, Neuroinformatics.

[52]  W. Gardner,et al.  Love Makes You Real: Favorite Television Characters Are Perceived as “Real” in a Social Facilitation Paradigm , 2008 .

[53]  P. Jacob What Do Mirror Neurons Contribute to Human Social Cognition , 2008 .

[54]  J. Weber,et al.  Journal Section: Behavioral/systems/cognitive Social Cognitive Conflict Resolution: Contributions of Domain General and Domain Specific Neural Systems , 2022 .

[55]  S. Petersen,et al.  Characterizing the Hemodynamic Response: Effects of Presentation Rate, Sampling Procedure, and the Possibility of Ordering Brain Activity Based on Relative Timing , 2000, NeuroImage.

[56]  Karl J. Friston,et al.  Modeling regional and psychophysiologic interactions in fMRI: the importance of hemodynamic deconvolution , 2003, NeuroImage.

[57]  J. Uleman,et al.  Spontaneous inferences, implicit impressions, and implicit theories. , 2008, Annual review of psychology.

[58]  Uta Frith,et al.  Theory of mind , 2001, Current Biology.

[59]  E. E. Jones,et al.  From Acts To Dispositions The Attribution Process In Person Perception1 , 1965 .

[60]  E. Miller Handbook of Social Psychology , 1946, Mental Health.

[61]  D. Gilbert,et al.  On cognitive busyness: When person perceivers meet persons perceived. , 1988 .

[62]  Y. Trope Identification and Inferential Processes in Dispositional Attribution. , 1986 .

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

[64]  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.

[65]  D. Amaral,et al.  Neuroanatomy of autism , 2008, Trends in Neurosciences.

[66]  K. Ochsner,et al.  The role of social cognition in emotion , 2008, Trends in Cognitive Sciences.

[67]  C. Keysers,et al.  Evidence for mirror systems in emotions , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[68]  S. Shamay-Tsoory The Neural Bases for Empathy , 2011, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[69]  M. Iacoboni Imitation, empathy, and mirror neurons. , 2009, Annual review of psychology.

[70]  V. Gallese Before and below ‘theory of mind’: embodied simulation and the neural correlates of social cognition , 2007, Philosophical Transactions of the Royal Society B: Biological Sciences.

[71]  Jason P. Mitchell,et al.  Two Mechanisms for Simulating Other Minds , 2011 .

[72]  D G Pelli,et al.  Pixel independence: measuring spatial interactions on a CRT display. , 1997, Spatial vision.