Individual differences in local gray matter density are associated with differences in affective and cognitive empathy

The understanding of empathy from a neuroscientific perspective has recently developed quickly, with numerous functional MRI studies associating different brain regions with different components of empathy. A recent meta-analysis across 40 fMRI studies revealed that affective empathy is most often associated with increased activity in the insula, whereas cognitive empathy is most often associated with activity in the midcingulate cortex and adjacent dorsomedial prefrontal cortex (MCC/dmPFC). To date, however, it remains unclear whether individual differences in brain morphometry in these regions underlie different dispositions in affective and cognitive empathy. In order to test this hypothesis, voxel-based morphometry (VBM) was used to examine the extent to which gray matter density predicts scores from an established empathy measure (Questionnaire of Cognitive and Affective Empathy; QCAE). One hundred and seventy-six participants completed the QCAE and underwent MRI in order to acquire a high-resolution, three-dimensional T1-weighted structural scans. A factor analysis of the questionnaire scores revealed two distinct factors of empathy, affective and cognitive, which confirmed the validity of the QCAE. VBM results revealed gray matter density differences associated with the distinct components of empathy. Higher scores on affective empathy were associated with greater gray matter density in the insula cortex and higher scores of cognitive empathy were associated with greater gray matter density in the MCC/dmPFC. Taken together, these results provide validation for empathy being a multi-component construct, suggesting that affective and cognitive empathy are differentially represented in brain morphometry as well as providing convergent evidence for empathy being represented by different neural and structural correlates.

[1]  F. Van Overwalle Social cognition and the brain: A meta‐analysis , 2009, Human brain mapping.

[2]  Carolyn Parkinson,et al.  Relating anatomical and social connectivity: white matter microstructure predicts emotional empathy. , 2014, Cerebral cortex.

[3]  Scott D. Brown,et al.  A purely confirmatory replication study of structural brain-behavior correlations , 2015, Cortex.

[4]  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.

[5]  G. Rizzolatti,et al.  Both of Us Disgusted in My Insula The Common Neural Basis of Seeing and Feeling Disgust , 2003, Neuron.

[6]  M. Rushworth,et al.  Connectivity-based subdivisions of the human right "temporoparietal junction area": evidence for different areas participating in different cortical networks. , 2012, Cerebral cortex.

[7]  K. Wiech,et al.  Anterior Insula Integrates Information about Salience into Perceptual Decisions about Pain , 2010, The Journal of Neuroscience.

[8]  P. Sessa,et al.  Taking one's time in feeling other-race pain: an event-related potential investigation on the time-course of cross-racial empathy. , 2014, Social cognitive and affective neuroscience.

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

[10]  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.

[11]  R. Peyron,et al.  Can We Share a Pain We Never Felt? Neural Correlates of Empathy in Patients with Congenital Insensitivity to Pain , 2009, Neuron.

[12]  Richard S. J. Frackowiak,et al.  Navigation-related structural change in the hippocampi of taxi drivers. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[13]  Christian Keysers,et al.  Inferior frontal gyrus activity triggers anterior insula response to emotional facial expressions. , 2008, Emotion.

[14]  G. Winocur,et al.  “I have often walked down this street before”: fMRI Studies on the hippocampus and other structures during mental navigation of an old environment , 2004, Hippocampus.

[15]  Chia-Yen Yang,et al.  Sensorimotor resonance is an outcome but not a platform to anticipating harm to others , 2012, Social neuroscience.

[16]  E. Phelps Emotion and cognition: insights from studies of the human amygdala. , 2006, Annual review of psychology.

[17]  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.

[18]  T. Ball,et al.  Structural basis of empathy and the domain general region in the anterior insular cortex , 2013, Front. Hum. Neurosci..

[19]  Mark H. Davis,et al.  A Multidimensional Approach to Individual Differences in Empathy , 1980 .

[20]  A. Perry,et al.  Understanding emotional and cognitive empathy: A neuropsychological , 2013 .

[21]  E. Phelps,et al.  Social learning of fear , 2007, Nature Neuroscience.

[22]  Simon Baron-Cohen,et al.  Empathizing with basic emotions: Common and discrete neural substrates , 2006, Social neuroscience.

[23]  V. Menon,et al.  Saliency, switching, attention and control: a network model of insula function , 2010, Brain Structure and Function.

[24]  Gaspare Galati,et al.  Transcranial magnetic stimulation highlights the sensorimotor side of empathy for pain , 2005, Nature Neuroscience.

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

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

[27]  Paul J. Laurienti,et al.  An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets , 2003, NeuroImage.

[28]  Elizabeth K. Baker,et al.  fMRI Hippocampal Activity During a VirtualRadial Arm Maze , 2005, Applied psychophysiology and biofeedback.

[29]  A. Field,et al.  Vicarious learning and the development of fears in childhood. , 2007, Behaviour research and therapy.

[30]  D. Farrington,et al.  Examining the relationship between low empathy and bullying , 2006 .

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

[32]  J. O'Doherty,et al.  Empathy for Pain Involves the Affective but not Sensory Components of Pain , 2004, Science.

[33]  T. Singer,et al.  The neural basis of empathy. , 2012, Annual review of neuroscience.

[34]  G. Pellegrino,et al.  Vicarious responses to pain in anterior cingulate cortex: Is empathy a multisensory issue? , 2004, Cognitive, affective & behavioral neuroscience.

[35]  Karl J. Friston,et al.  Voxel-Based Morphometry—The Methods , 2000, NeuroImage.

[36]  J. Decety Dissecting the Neural Mechanisms Mediating Empathy , 2011 .

[37]  J. Decety,et al.  Neural correlates of feeling sympathy , 2003, Neuropsychologia.

[38]  E. Hatfield,et al.  Emotional Contagion and Empathy , 2009 .

[39]  Nikolaus Weiskopf,et al.  A comparison between voxel-based cortical thickness and voxel-based morphometry in normal aging , 2009, NeuroImage.

[40]  John Ashburner,et al.  A fast diffeomorphic image registration algorithm , 2007, NeuroImage.

[41]  T. Singer,et al.  The Social Neuroscience of Empathy , 2009, Annals of the New York Academy of Sciences.

[42]  J. Decety,et al.  Empathic responsiveness in amygdala and anterior cingulate cortex in youths with psychopathic traits. , 2013, Journal of child psychology and psychiatry, and allied disciplines.

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

[44]  J. Decety,et al.  The functional architecture of human empathy. , 2004, Behavioral and cognitive neuroscience reviews.

[45]  Perrine Ruby,et al.  Distinct Regions of the Medial Prefrontal Cortex Are Associated with Self-referential Processing and Perspective Taking , 2007, Journal of Cognitive Neuroscience.

[46]  L. Aziz-Zadeh,et al.  Witnessing hateful people in pain modulates brain activity in regions associated with physical pain and reward , 2013, Front. Psychol..

[47]  Alan C. Evans,et al.  Changes in brain activity related to eating chocolate: from pleasure to aversion. , 2001, Brain : a journal of neurology.

[48]  J. Decety,et al.  Human Empathy Through the Lens of Social Neuroscience , 2006, TheScientificWorldJournal.

[49]  T. Singer,et al.  The role of anterior insular cortex in social emotions , 2010, Brain Structure and Function.

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

[51]  J. Perner,et al.  Neuroscience and Biobehavioral Reviews Fractionating Theory of Mind: a Meta-analysis of Functional Brain Imaging Studies , 2022 .

[52]  Claus Lamm,et al.  Meta-analytic evidence for common and distinct neural networks associated with directly experienced pain and empathy for pain , 2011, NeuroImage.

[53]  J. Decety,et al.  To what extent do we share the pain of others? Insight from the neural bases of pain empathy , 2006, Pain.

[54]  Bostjan Likar,et al.  A Review of Methods for Correction of Intensity Inhomogeneity in MRI , 2007, IEEE Transactions on Medical Imaging.

[55]  Geraint Rees,et al.  Inter-individual differences in empathy are reflected in human brain structure , 2012, NeuroImage.

[56]  Kevin N. Ochsner,et al.  The neural correlates of direct and reflected self-knowledge , 2005, NeuroImage.

[57]  J. Decety,et al.  The Role of the Right Temporoparietal Junction in Social Interaction: How Low-Level Computational Processes Contribute to Meta-Cognition , 2007, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[58]  Christian Keysers,et al.  Empathy for positive and negative emotions in the gustatory cortex , 2007, NeuroImage.

[59]  Jin Fan,et al.  Anterior insular cortex is necessary for empathetic pain perception. , 2012, Brain : a journal of neurology.

[60]  Niall W. Duncan,et al.  Is there a core neural network in empathy? An fMRI based quantitative meta-analysis , 2011, Neuroscience & Biobehavioral Reviews.