Empathy, ToM, and self–other differentiation: An fMRI study of internal states

This study used functional magnetic resonance imaging to examine the neural substrates of empathy, Theory of Mind (ToM), and self–other differentiation involved in the adaptive understanding of people’s internal states. Three conditions were distinguished in both sad and neutral (no obvious emotion) contexts. The empathy condition involved imagining what another person is feeling while the more cognitively loaded ToM condition involved imagining what would make another person feel better. The self-reference condition required participants to imagine how they would feel in someone else’s situation. Areas previously implicated in empathy, ToM, and self–other differentiation were identified within the different conditions, regardless of emotional context. Specifically, the frontal and temporal poles responded more strongly for ToM than for empathy. The self-reference condition was associated with stronger dorsolateral prefrontal response than the empathy condition, while the reverse comparison revealed a stronger role for right frontal pole. Activations in frontal pole and orbitofrontal cortex were shared between the three conditions. Contrasts of parameter estimates demonstrated modulation by emotional context. The findings of common and differential patterns of responding observed in prefrontal and temporal regions suggest that within the social cognition network empathy, ToM and self–other differentiation have distinct roles that are responsive to context.

[1]  R. Saxe,et al.  What gets the attention of the temporo-parietal junction? An fMRI investigation of attention and theory of mind , 2010, Neuropsychologia.

[2]  William A. Cunningham,et al.  Tools of the Trade Type I and Type II error concerns in fMRI research : rebalancing the scale , 2009 .

[3]  J. Decety,et al.  How Would You Feel versus How Do You Think She Would Feel? A Neuroimaging Study of Perspective-Taking with Social Emotions , 2004, Journal of Cognitive Neuroscience.

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

[5]  I. Olson,et al.  The Enigmatic temporal pole: a review of findings on social and emotional processing. , 2007, Brain : a journal of neurology.

[6]  Jean Decety,et al.  Annals of the New York Academy of Sciences the Neuroevolution of Empathy , 2022 .

[7]  J. Aharon-Peretz,et al.  Impairment in Cognitive and Affective Empathy in Patients with Brain Lesions: Anatomical and Cognitive Correlates , 2004, Journal of clinical and experimental neuropsychology.

[8]  Armand J. Quick,et al.  THE QUICK TEST , 1951 .

[9]  Rhiannon Corcoran,et al.  Autobiographical memory and theory of mind: evidence of a relationship in schizophrenia , 2003, Psychological Medicine.

[10]  G. Fink,et al.  Cerebral Representation of One’s Own Past: Neural Networks Involved in Autobiographical Memory , 1996, The Journal of Neuroscience.

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

[12]  B. Berger,et al.  Characterization of Empathy Deficits following Prefrontal Brain Damage: The Role of the Right Ventromedial Prefrontal Cortex , 2003, Journal of Cognitive Neuroscience.

[13]  Scott T. Grafton,et al.  Amygdala activity related to enhanced memory for pleasant and aversive stimuli , 1999, Nature Neuroscience.

[14]  Beate Sodian,et al.  Neural correlates of true and false belief reasoning , 2007, NeuroImage.

[15]  R. Corcoran,et al.  The QCAE: A Questionnaire of Cognitive and Affective Empathy , 2009, European Psychiatry.

[16]  R. Saxe,et al.  Making sense of another mind: The role of the right temporo-parietal junction , 2005, Neuropsychologia.

[17]  A. Damasio,et al.  Individuals with sociopathic behavior caused by frontal damage fail to respond autonomically to social stimuli , 1990, Behavioural Brain Research.

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

[19]  S-J Blakemore,et al.  Social Cognition. Foresight Cognitive Systems Project Research Review. , 2003 .

[20]  J. Gabrieli,et al.  Event-Related Activation in the Human Amygdala Associates with Later Memory for Individual Emotional Experience , 2000, The Journal of Neuroscience.

[21]  A. Woodward,et al.  Not all emotions are created equal: the negativity bias in social-emotional development. , 2008, Psychological bulletin.

[22]  J. Decety,et al.  A PET Investigation of the Attribution of Intentions with a Nonverbal Task , 2000, NeuroImage.

[23]  Kate Tchanturia,et al.  Sex differences in theory of mind: A male advantage on Happé's “cartoon” task , 2007 .

[24]  J. Gabrieli,et al.  The frontopolar cortex and human cognition: Evidence for a rostrocaudal hierarchical organization within the human prefrontal cortex , 2000, Psychobiology.

[25]  Stephen Lawrie,et al.  Functional Specialization within Rostral Prefrontal Cortex (Area 10): A Meta-analysis , 2006, Journal of Cognitive Neuroscience.

[26]  G. J. Vreeke,et al.  Empathy, an integrative model , 2003 .

[27]  Andy Field,et al.  Discovering statistics using SPSS, 2nd ed. , 2005 .

[28]  S. Baron-Cohen,et al.  The Empathy Quotient: An Investigation of Adults with Asperger Syndrome or High Functioning Autism, and Normal Sex Differences , 2004, Journal of autism and developmental disorders.

[29]  William A. Cunningham,et al.  Type I and Type II error concerns in fMRI research: re-balancing the scale. , 2009, Social cognitive and affective neuroscience.

[30]  M. Bradley,et al.  Neuroanatomical correlates of pleasant and unpleasant emotion , 1997, Neuropsychologia.

[31]  J. Decety,et al.  Effect of subjective perspective taking during simulation of action: a PET investigation of agency , 2001, Nature Neuroscience.

[32]  R. McCarley,et al.  Initial and Progressive Gray Matter Abnormalities in Insular Gyrus and Temporal Pole in First-Episode Schizophrenia Contrasted With First-Episode Affective Psychosis. , 2016, Schizophrenia bulletin.

[33]  J. Morrison Understanding Others by Understanding the Self: Neurobiological Models of Empathy and their Relevance to Personality Disorders. , 2004, The Canadian child and adolescent psychiatry review = La revue canadienne de psychiatrie de l'enfant et de l'adolescent.

[34]  K. Vohs,et al.  Case Western Reserve University , 1990 .

[35]  Willem A. Nolen,et al.  Inhibit yourself and understand the other: Neural basis of distinct processes underlying Theory of Mind , 2011, NeuroImage.

[36]  P. Lang International Affective Picture System (IAPS) : Technical Manual and Affective Ratings , 1995 .

[37]  Edward B. Royzman,et al.  Negativity Bias, Negativity Dominance, and Contagion , 2001 .

[38]  HighWire Press Philosophical Transactions of the Royal Society of London , 1781, The London Medical Journal.

[39]  Scott T. Grafton,et al.  Differential role of the orbital frontal lobe in emotional versus cognitive perspective-taking , 2006, Neuropsychologia.

[40]  Ludovico Minati,et al.  Slow Breathing and Hypoxic Challenge: Cardiorespiratory Consequences and Their Central Neural Substrates , 2015, PloS one.

[41]  L. Faust,et al.  Understanding Other Minds Perspectives From Developmental Cognitive Neuroscience , 2016 .

[42]  R. J. Seitz,et al.  Valuating other people’s emotional face expression: a combined functional magnetic resonance imaging and electroencephalography study , 2008, Neuroscience.

[43]  K. Luan Phan,et al.  Functional Neuroanatomy of Emotion: A Meta-Analysis of Emotion Activation Studies in PET and fMRI , 2002, NeuroImage.

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

[45]  Ulrike M. Krämer,et al.  Emotional and cognitive aspects of empathy and their relation to social cognition—an fMRI-study , 2010, Brain Research.

[46]  Silke Anders,et al.  The multiple facets of empathy: a survey of theory and evidence. , 2006, Progress in brain research.

[47]  Paul J. Eslinger,et al.  Neurological and Neuropsychological Bases of Empathy , 1998, European Neurology.

[48]  J. Decety,et al.  A Social-Neuroscience Perspective on Empathy , 2006 .

[49]  I. Wilkinson,et al.  Investigating the functional anatomy of empathy and forgiveness , 2001, Neuroreport.

[50]  Rebecca Elliott,et al.  Neuronal correlates of theory of mind and empathy: A functional magnetic resonance imaging study in a nonverbal task , 2006, NeuroImage.

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

[52]  T. Hergueta,et al.  The mini international neuropsychiatric interview , 1998, European Psychiatry.

[53]  Dennis A. Nowak,et al.  Dissociating cognitive from affective theory of mind: A TMS study , 2010, Cortex.

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

[55]  S. Shamay-Tsoory,et al.  Neuroanatomical and neurochemical bases of theory of mind , 2011, Neuropsychologia.

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

[57]  Simon Baron-Cohen,et al.  Understanding other minds: Perspectives from developmental cognitive neuroscience, 2nd ed. , 2000 .

[58]  G. Shulman,et al.  Medial prefrontal cortex and self-referential mental activity: Relation to a default mode of brain function , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[59]  R. Rosenthal Meta-analytic procedures for social research , 1984 .

[60]  J. Decety,et al.  What you believe versus what you think they believe: a neuroimaging study of conceptual perspective‐taking , 2003, The European journal of neuroscience.

[61]  Joel H Kramer,et al.  Patterns of Cognitive and Emotional Empathy in Frontotemporal Lobar Degeneration , 2005, Cognitive and behavioral neurology : official journal of the Society for Behavioral and Cognitive Neurology.

[62]  J Aharon-Peretz,et al.  The neuroanatomical basis of understanding sarcasm and its relationship to social cognition. , 2005, Neuropsychology.

[63]  Sterling C. Johnson,et al.  Metacognitive evaluation, self-relevance, and the right prefrontal cortex , 2004, NeuroImage.

[64]  John D E Gabrieli,et al.  Evaluating self-generated information: anterior prefrontal contributions to human cognition. , 2003, Behavioral neuroscience.

[65]  D. Sheehan,et al.  The Mini-International Neuropsychiatric Interview (M.I.N.I.): the development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. , 1998, The Journal of clinical psychiatry.

[66]  Darinka Radovic,et al.  Inside-out: comparing internally generated and externally generated basic emotions. , 2012, Emotion.

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

[68]  J. Sommerville,et al.  Shared representations between self and other: a social cognitive neuroscience view , 2003, Trends in Cognitive Sciences.

[69]  P. Burgess,et al.  Executive function , 2008, Current Biology.

[70]  C. Frith,et al.  Functional imaging of ‘theory of mind’ , 2003, Trends in Cognitive Sciences.

[71]  Iroise Dumontheil,et al.  The gateway hypothesis of rostral prefrontal cortex (area 10) function , 2007, Trends in Cognitive Sciences.

[72]  Simon Baron-Cohen,et al.  The systemizing quotient: an investigation of adults with Asperger syndrome or high-functioning autism, and normal sex differences. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.