Structural covariance networks of the dorsal anterior insula predict females' individual differences in empathic responding.

Previous functional imaging studies have shown key roles of the dorsal anterior insula (dAI) and anterior midcingulate cortex (aMCC) in empathy for the suffering of others. The current study mapped structural covariance networks of these regions and assessed the relationship between networks and individual differences in empathic responding in 94 females. Individual differences in empathy were assessed through average state measures in response to a video task showing others' suffering, and through questionnaire-based trait measures of empathic concern. Overall, covariance patterns indicated that dAI and aMCC are principal hubs within prefrontal, temporolimbic, and midline structural covariance networks. Importantly, participants with high empathy state ratings showed increased covariance of dAI, but not aMCC, to prefrontal and limbic brain regions. This relationship was specific for empathy and could not be explained by individual differences in negative affect ratings. Regarding questionnaire-based empathic trait measures, we observed a similar, albeit weaker modulation of dAI covariance, confirming the robustness of our findings. Our analysis, thus, provides novel evidence for a specific contribution of frontolimbic structural covariance networks to individual differences in social emotions beyond negative affect.

[1]  H. Wittchen,et al.  SKID. Strukturiertes Klinisches Interview für DSM-IV. Achse I und II. Handanweisung , 1997 .

[2]  K. Zilles,et al.  A link between the systems: functional differentiation and integration within the human insula revealed by meta-analysis , 2010, Brain Structure and Function.

[3]  C. Keysers,et al.  The Observation and Execution of Actions Share Motor and Somatosensory Voxels in all Tested Subjects: Single-Subject Analyses of Unsmoothed fMRI Data , 2008, Cerebral cortex.

[4]  Anderson M. Winkler,et al.  Cortical thickness or grey matter volume? The importance of selecting the phenotype for imaging genetics studies , 2010, NeuroImage.

[5]  T. Wager,et al.  Different circuits for different pain: Patterns of functional connectivity reveal distinct networks for processing pain in self and others , 2007, Social neuroscience.

[6]  Neda Bernasconi,et al.  Cortical thickness analysis in temporal lobe epilepsy , 2010, Neurology.

[7]  D. Pandya,et al.  Cingulate cortex of the rhesus monkey: II. Cortical afferents , 1987, The Journal of comparative neurology.

[8]  M. Mesulam,et al.  Insula of the old world monkey. II: Afferent cortical input and comments on the claustrum , 1982, The Journal of comparative neurology.

[9]  Claus Lamm,et al.  What Are You Feeling? Using Functional Magnetic Resonance Imaging to Assess the Modulation of Sensory and Affective Responses during Empathy for Pain , 2007, PloS one.

[10]  Marianna D. Eddy,et al.  Regionally localized thinning of the cerebral cortex in schizophrenia , 2003, Schizophrenia Research.

[11]  A. Schulze-Bonhage,et al.  Functional organization of the human anterior insular cortex , 2009, Neuroscience Letters.

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

[13]  C. Keysers,et al.  A Common Anterior Insula Representation of Disgust Observation, Experience and Imagination Shows Divergent Functional Connectivity Pathways , 2008, PloS one.

[14]  T. Singer,et al.  Functional neural plasticity and associated changes in positive affect after compassion training. , 2013, Cerebral cortex.

[15]  R. Bagby,et al.  Twenty-item Toronto Alexithymia Scale , 2011 .

[16]  Peter Erhard,et al.  A common neural basis for receptive and expressive communication of pleasant facial affect , 2005, NeuroImage.

[17]  J. Mattingley,et al.  Brain regions with mirror properties: A meta-analysis of 125 human fMRI studies , 2012, Neuroscience & Biobehavioral Reviews.

[18]  Katiuscia Sacco,et al.  Functional connectivity of the insula in the resting brain , 2011, NeuroImage.

[19]  J. Lerch,et al.  Patterns of Coordinated Anatomical Change in Human Cortical Development: A Longitudinal Neuroimaging Study of Maturational Coupling , 2011, Neuron.

[20]  Efstathios D. Gennatas,et al.  Network-level structural covariance in the developing brain , 2010, Proceedings of the National Academy of Sciences.

[21]  Daniel S. Margulies,et al.  Mapping the functional connectivity of anterior cingulate cortex , 2007, NeuroImage.

[22]  R. Bagby,et al.  The twenty-item Toronto Alexithymia Scale--I. Item selection and cross-validation of the factor structure. , 1994, Journal of psychosomatic research.

[23]  Claus Lamm,et al.  The Neural Substrate of Human Empathy: Effects of Perspective-taking and Cognitive Appraisal , 2007, Journal of Cognitive Neuroscience.

[24]  Naomi B. Pitskel,et al.  Three Systems of Insular Functional Connectivity Identified with Cluster Analysis , 2010, Cerebral cortex.

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

[26]  Patrik Vuilleumier,et al.  Felt and Seen Pain Evoke the Same Local Patterns of Cortical Activity in Insular and Cingulate Cortex , 2011, The Journal of Neuroscience.

[27]  Anders M. Dale,et al.  Reliability of MRI-derived measurements of human cerebral cortical thickness: The effects of field strength, scanner upgrade and manufacturer , 2006, NeuroImage.

[28]  B. Miller,et al.  Neurodegenerative Diseases Target Large-Scale Human Brain Networks , 2009, Neuron.

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

[30]  T. Singer,et al.  The empathic brain: how, when and why? , 2006, Trends in Cognitive Sciences.

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

[32]  Boris C. Bernhardt,et al.  Mapping limbic network organization in temporal lobe epilepsy using morphometric correlations: Insights on the relation between mesiotemporal connectivity and cortical atrophy , 2008, NeuroImage.

[33]  B. Vogt,et al.  Architecture and neurocytology of monkey cingulate gyrus , 2005, The Journal of comparative neurology.

[34]  K. Ochsner,et al.  The neuroscience of empathy: progress, pitfalls and promise , 2012, Nature Neuroscience.

[35]  Alan C. Evans,et al.  Detecting changes in nonisotropic images , 1999, Human brain mapping.

[36]  M. Mesulam,et al.  Insula of the old world monkey. Architectonics in the insulo‐orbito‐temporal component of the paralimbic brain , 1982, The Journal of comparative neurology.

[37]  C. Geula,et al.  Cytoarchitecture and neural afferents of orbitofrontal cortex in the brain of the monkey , 1992, The Journal of comparative neurology.

[38]  G. Rizzolatti,et al.  Neurophysiological mechanisms underlying the understanding and imitation of action , 2001, Nature Reviews Neuroscience.

[39]  M. Mesulam,et al.  Insula of the old world monkey. III: Efferent cortical output and comments on function , 1982, The Journal of comparative neurology.

[40]  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.

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

[42]  Luke J. Chang,et al.  Decoding the role of the insula in human cognition: functional parcellation and large-scale reverse inference. , 2013, Cerebral cortex.

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

[44]  D. Pandya,et al.  Efferent connections of the cingulate gyrus in the rhesus monkey , 1981, Experimental Brain Research.

[45]  D. Amaral,et al.  Amygdalo‐cortical projections in the monkey (Macaca fascicularis) , 1984, The Journal of comparative neurology.

[46]  KJ Worsley,et al.  SurfStat: A Matlab toolbox for the statistical analysis of univariate and multivariate surface and volumetric data using linear mixed effects models and random field theory , 2009, NeuroImage.

[47]  Marius V Peelen,et al.  The sight of others' pain modulates motor processing in human cingulate cortex. , 2007, Cerebral cortex.

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

[49]  D. Jeanmonod,et al.  The Insula of Reil Revisited: Multiarchitectonic Organization in Macaque Monkeys , 2011, Cerebral cortex.

[50]  A. Craig,et al.  How do you feel — now? The anterior insula and human awareness , 2009, Nature Reviews Neuroscience.

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

[52]  O. Sporns,et al.  Complex brain networks: graph theoretical analysis of structural and functional systems , 2009, Nature Reviews Neuroscience.

[53]  Alan C. Evans,et al.  Cortical thickness analysis examined through power analysis and a population simulation , 2005, NeuroImage.

[54]  K. Vogeley,et al.  Parsing the neural correlates of moral cognition: ALE meta-analysis on morality, theory of mind, and empathy , 2012, Brain Structure and Function.

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

[56]  Angela R. Laird,et al.  ALE meta-analysis of action observation and imitation in the human brain , 2010, NeuroImage.

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

[58]  Fred L. Bookstein,et al.  “Voxel-Based Morphometry” Should Not Be Used with Imperfectly Registered Images , 2001, NeuroImage.

[59]  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.

[60]  Karl J. Friston,et al.  Why Voxel-Based Morphometry Should Be Used , 2001, NeuroImage.

[61]  H. Critchley,et al.  A common role of insula in feelings, empathy and uncertainty , 2009, Trends in Cognitive Sciences.

[62]  T. Singer The neuronal basis and ontogeny of empathy and mind reading: Review of literature and implications for future research , 2006, Neuroscience & Biobehavioral Reviews.

[63]  A. Dale,et al.  Cortical Surface-Based Analysis II: Inflation, Flattening, and a Surface-Based Coordinate System , 1999, NeuroImage.

[64]  Haakon G Engen,et al.  Empathy circuits , 2013, Current Opinion in Neurobiology.

[65]  Tania Singer,et al.  University of Zurich Zurich Open Repository and Archive I Feel How You Feel but Not Always: the Empathic Brain and Its I Feel How You Feel but Not Always: the Empathic Brain and Its Modulation , 2009 .

[66]  J. O'Doherty,et al.  Empathic neural responses are modulated by the perceived fairness of others , 2006, Nature.

[67]  A. Craig How do you feel? Interoception: the sense of the physiological condition of the body , 2002, Nature Reviews Neuroscience.

[68]  A. Beck,et al.  Comparison of Beck Depression Inventories -IA and -II in psychiatric outpatients. , 1996, Journal of personality assessment.

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

[70]  J. R. Augustine Circuitry and functional aspects of the insular lobe in primates including humans , 1996, Brain Research Reviews.

[71]  Alan C. Evans,et al.  Mapping anatomical correlations across cerebral cortex (MACACC) using cortical thickness from MRI , 2006, NeuroImage.

[72]  B. Vogt,et al.  Contributions of anterior cingulate cortex to behaviour. , 1995, Brain : a journal of neurology.

[73]  Scott T Grafton,et al.  Functional imaging of face and hand imitation: towards a motor theory of empathy , 2004, NeuroImage.

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

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

[76]  A. Dale,et al.  Regional and progressive thinning of the cortical ribbon in Huntington’s disease , 2002, Neurology.

[77]  Neda Bernasconi,et al.  Graph-theoretical analysis reveals disrupted small-world organization of cortical thickness correlation networks in temporal lobe epilepsy. , 2011, Cerebral cortex.

[78]  K. Preuschoff,et al.  Neural Responses to Ingroup and Outgroup Members' Suffering Predict Individual Differences in Costly Helping , 2010, Neuron.

[79]  Anders M. Dale,et al.  Cortical Surface-Based Analysis I. Segmentation and Surface Reconstruction , 1999, NeuroImage.

[80]  C. Hohmann,et al.  Effects of brief stress exposure during early postnatal development in Balb/CByJ mice: II. Altered cortical morphology. , 2012, Developmental psychobiology.

[81]  R. Davidson,et al.  The integration of negative affect, pain and cognitive control in the cingulate cortex , 2011, Nature Reviews Neuroscience.

[82]  Mark H. Davis Measuring individual differences in empathy: Evidence for a multidimensional approach. , 1983 .