Empathizing with basic emotions: Common and discrete neural substrates

Abstract Empathizing is a quantitative trait involving understanding another's mental state (including their emotion) and responding to this with an appropriate emotion. A reliable, behaviorally validated self-report questionnaire measure of this is the Empathy Quotient (EQ), which is continuously distributed across the general population. The “discrete emotions” model posits that each “basic” emotion has a relatively independent evolutionary antecedent and social-communicative function and is subserved by a discrete neural system. In this study, we investigate if and how empathy influences the perception of basic emotions. Twenty-five volunteers (13 female, 12 male) selected across EQ space participated in a correlational design 3T fMRI study. The stimuli were presented in a box-car design, where 5 blocks (each containing 4 video clips of any one of happy, sad, angry, disgust or neutral expressions from different actors) and a low-level baseline were presented in pseudo-random order. Using an exploratory analysis, we found different brain regions correlated with EQ, depending on which emotion was being perceived. In particular, the ventral striatal response to happy faces correlated positively with EQ, while the ventral striatal response to sad faces was negatively correlated with EQ. The precuneus and lateral prefrontal cortical response to angry faces correlated positively with EQ. The response of the insula and the superior temporal gyrus cortex to disgust faces were negatively correlated with EQ. These results are discussed in the light of the postulated evolutionary function of each emotion. Using a hypothesis-driven conjunction analysis, we found that a region in the left dorsal inferior frontal gyrus/premotor cortex was positively correlated to the EQ across all four emotions. This region could therefore constitute a biomarker for trait empathy across emotions. We conclude that there are common regions underlying empathy across different emotions, and there are regions that show an emotion-specific correlation with empathy. This pattern of results is interpreted using a modification of Haxby et al.'s model of face perception.

[1]  Andrew W. Young,et al.  Neuropsychology of fear and loathing , 2001, Nature Reviews Neuroscience.

[2]  C. Riccio Autism Diagnostic Interview—Revised , 2008 .

[3]  K. R. Ridderinkhof,et al.  Neurocognitive mechanisms of cognitive control: The role of prefrontal cortex in action selection, response inhibition, performance monitoring, and reward-based learning , 2004, Brain and Cognition.

[4]  G. Parker,et al.  Cognitive generation of affect in bipolar depression: an fMRI study , 2004, European Journal of Neuroscience.

[5]  Jennifer H. Pfeifer,et al.  Understanding emotions in others: mirror neuron dysfunction in children with autism spectrum disorders , 2006, Nature Neuroscience.

[6]  M J Brammer,et al.  The analysis of functional magnetic resonance images , 1997, Statistical methods in medical research.

[7]  E. Bullmore,et al.  Variations in the human cannabinoid receptor (CNR1) gene modulate striatal responses to happy faces , 2006, The European journal of neuroscience.

[8]  F. Gonzalez-Lima,et al.  Hypermetabolism of paraventricular hypothalamus in the congenitally helpless rat , 2001, Neuroscience Letters.

[9]  T. Walden,et al.  The development of social referencing. , 1988, Child development.

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

[11]  Simon Baron-Cohen,et al.  The Friendship Questionnaire: An Investigation of Adults with Asperger Syndrome or High-Functioning Autism, and Normal Sex Differences , 2003, Journal of autism and developmental disorders.

[12]  Karl J. Friston,et al.  A unified statistical approach for determining significant signals in images of cerebral activation , 1996, Human brain mapping.

[13]  G. Hall,et al.  Enhanced salience and emotion recognition in Autism: a PET study. , 2003, The American journal of psychiatry.

[14]  M. Greicius,et al.  Humor Modulates the Mesolimbic Reward Centers , 2003, Neuron.

[15]  S. Baron-Cohen,et al.  Systemizing empathy: Teaching adults with Asperger syndrome or high-functioning autism to recognize complex emotions using interactive multimedia , 2006, Development and Psychopathology.

[16]  G. Celani,et al.  The Understanding of the Emotional Meaning of Facial Expressions in People with Autism , 1999, Journal of autism and developmental disorders.

[17]  Thomas E. Nichols,et al.  Nonparametric permutation tests for functional neuroimaging: A primer with examples , 2002, Human brain mapping.

[18]  D. Perrett,et al.  A specific neural substrate for perceiving facial expressions of disgust , 1997, Nature.

[19]  J. Allman,et al.  Organization of the face representation in macaque motor cortex , 1980, The Journal of comparative neurology.

[20]  E. Bullmore,et al.  Permutation tests for factorially designed neuroimaging experiments , 2004, Human brain mapping.

[21]  John Suckling,et al.  Global, voxel, and cluster tests, by theory and permutation, for a difference between two groups of structural MR images of the brain , 1999, IEEE Transactions on Medical Imaging.

[22]  L. Parsons,et al.  Reciprocal limbic-cortical function and negative mood: converging PET findings in depression and normal sadness. , 1999, The American journal of psychiatry.

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

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

[25]  U. Frith Mind Blindness and the Brain in Autism , 2001, Neuron.

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

[27]  Volkmar Glauche,et al.  The human action recognition system and its relationship to Broca’s area: an fMRI study , 2003, NeuroImage.

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

[29]  S. Hurley Active perception and perceiving action : The Shared Circuits Hypothesis , 2004 .

[30]  P. Fox,et al.  Differential limbic–cortical correlates of sadness and anxiety in healthy subjects: implications for affective disorders , 2000, Biological Psychiatry.

[31]  S. Folstein,et al.  Recognition and expression of emotional cues by autistic and normal adults. , 1989, Journal of child psychology and psychiatry, and allied disciplines.

[32]  Klaus Opwis,et al.  Tracking the subprocesses of decision-based action in the human frontal lobes , 2006, NeuroImage.

[33]  T. Paus,et al.  Brain networks involved in viewing angry hands or faces. , 2006, Cerebral cortex.

[34]  Wolfgang Prinz,et al.  Common Mechanisms in Perception and Action: Attention and Performance Volume Xix , 2001 .

[35]  J. Mazziotta,et al.  Functional segregation within pars opercularis of the inferior frontal gyrus: evidence from fMRI studies of imitation and action observation. , 2005, Cerebral cortex.

[36]  A. Meltzoff,et al.  Does the End Justify the Means? A PET Exploration of the Mechanisms Involved in Human Imitation , 2002, NeuroImage.

[37]  Karl J. Friston,et al.  Dynamic causal modelling , 2003, NeuroImage.

[38]  S. Baron-Cohen Theory of mind and autism: A review , 2000 .

[39]  R. Hari,et al.  Abnormal imitation‐related cortical activation sequences in Asperger's syndrome , 2004, Annals of neurology.

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

[41]  J. Haxby,et al.  Human neural systems for face recognition and social communication , 2002, Biological Psychiatry.

[42]  B. Vogt Pain and emotion interactions in subregions of the cingulate gyrus , 2005, Nature Reviews Neuroscience.

[43]  Fanny Eugène,et al.  The impact of individual differences on the neural circuitry underlying sadness , 2003, NeuroImage.

[44]  J. O'Doherty,et al.  Neural Responses during Anticipation of a Primary Taste Reward , 2002, Neuron.

[45]  Richard J. Davidson,et al.  Exploring Hindu Indian Emotion Expressions: Evidence for Accurate Recognition by Americans and Indians , 2000, Psychological science.

[46]  J. O'Doherty,et al.  Reward representations and reward-related learning in the human brain: insights from neuroimaging , 2004, Current Opinion in Neurobiology.

[47]  A. Lawrence,et al.  Functional neuroanatomy of emotions: A meta-analysis , 2003, Cognitive, affective & behavioral neuroscience.

[48]  M. Posner The Brain and Emotion , 1999, Nature Medicine.

[49]  P. Ekman,et al.  Constants across cultures in the face and emotion. , 1971, Journal of personality and social psychology.

[50]  S. Baron-Cohen,et al.  Do children with autism recognise surprise? A research note , 1993 .

[51]  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.

[52]  Rebecca C. Knickmeyer,et al.  Fetal testosterone and empathy: Evidence from the Empathy Quotient (EQ) and the “Reading the Mind in the Eyes” Test , 2006, Social neuroscience.

[53]  D. Weinberger,et al.  Neocortical modulation of the amygdala response to fearful stimuli , 2003, Biological Psychiatry.

[54]  C. Tardif,et al.  Spatial Frequency and Face Processing in Children with Autism and Asperger Syndrome , 2004, Journal of autism and developmental disorders.

[55]  R. Hobson The autistic child's appraisal of expressions of emotion. , 1986, Journal of child psychology and psychiatry, and allied disciplines.

[56]  Scott T. Grafton,et al.  Actions or Hand-Object Interactions? Human Inferior Frontal Cortex and Action Observation , 2003, Neuron.

[57]  A. Meltzoff,et al.  A PET Exploration of the Neural Mechanisms Involved in Reciprocal Imitation , 2002, NeuroImage.

[58]  R. Adolphs,et al.  Impaired recognition of emotion in facial expressions following bilateral damage to the human amygdala , 1994, Nature.

[59]  A. Young,et al.  Neural responses to facial and vocal expressions of fear and disgust , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[60]  François Mauguière,et al.  Experiencing and detecting happiness in humans: The role of the supplementary motor area , 2006, Annals of neurology.

[61]  Kenneth I Forster,et al.  DMDX: A Windows display program with millisecond accuracy , 2003, Behavior research methods, instruments, & computers : a journal of the Psychonomic Society, Inc.

[62]  Rebecca C. Knickmeyer,et al.  Foetal testosterone, social relationships, and restricted interests in children. , 2005, Journal of child psychology and psychiatry, and allied disciplines.

[63]  D. Swaab,et al.  The stress system in the human brain in depression and neurodegeneration , 2005, Ageing Research Reviews.

[64]  D. Amaral,et al.  Increased social fear and decreased fear of objects in monkeys with neonatal amygdala lesions , 2001, Neuroscience.

[65]  E. Bullmore,et al.  The amygdala theory of autism , 2000, Neuroscience & Biobehavioral Reviews.

[66]  D. Perrett,et al.  Opinion TRENDS in Cognitive Sciences Vol.8 No.11 November 2004 Demystifying social cognition: a Hebbian perspective , 2022 .

[67]  C. Darwin The Expression of the Emotions in Man and Animals , .

[68]  I. Gottesman,et al.  The endophenotype concept in psychiatry: etymology and strategic intentions. , 2003, The American journal of psychiatry.

[69]  S. Baron-Cohen,et al.  The Cambridge Mindreading (CAM) Face-Voice Battery: Testing Complex Emotion Recognition in Adults with and without Asperger Syndrome , 2006, Journal of autism and developmental disorders.

[70]  Clark McCauley,et al.  Individual differences in sensitivity to disgust: A scale sampling seven domains of disgust elicitors , 1994 .

[71]  Richard S. J. Frackowiak,et al.  Other minds in the brain: a functional imaging study of “theory of mind” in story comprehension , 1995, Cognition.

[72]  G. Rizzolatti,et al.  Premotor cortex and the recognition of motor actions. , 1996, Brain research. Cognitive brain research.

[73]  Hanneke E. M. den Ouden,et al.  Thinking about intentions , 2005, NeuroImage.

[74]  C. Darwin,et al.  The Expression of the Emotions in Man and Animals , 1872 .

[75]  A. Couteur,et al.  Autism Diagnostic Interview-Revised: A revised version of a diagnostic interview for caregivers of individuals with possible pervasive developmental disorders , 1994, Journal of autism and developmental disorders.

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

[77]  J. Prinz Which Emotions Are Basic , 2007 .

[78]  G. Rizzolatti,et al.  The mirror-neuron system. , 2004, Annual review of neuroscience.

[79]  A. Lawrence,et al.  Homologizing human emotions , 2004 .

[80]  S. Baron-Cohen,et al.  Is There a "Language of the Eyes"? Evidence from Normal Adults, and Adults with Autism or Asperger Syndrome , 1997 .

[81]  S. Baron-Cohen The extreme male brain theory of autism , 2002, Trends in Cognitive Sciences.

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

[83]  Jennifer S. Beer,et al.  Facial expression of emotion. , 2003 .

[84]  J C Mazziotta,et al.  Reafferent copies of imitated actions in the right superior temporal cortex , 2001, Proceedings of the National Academy of Sciences of the United States of America.

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

[86]  A. Damasio,et al.  Subcortical and cortical brain activity during the feeling of self-generated emotions , 2000, Nature Neuroscience.

[87]  J. Winn,et al.  Brain , 1878, The Lancet.

[88]  C. Lord,et al.  Austism diagnostic observation schedule: A standardized observation of communicative and social behavior , 1989, Journal of autism and developmental disorders.

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

[90]  Jill Keane,et al.  Impaired recognition of anger following damage to the ventral striatum. , 2004, Brain : a journal of neurology.

[91]  V. Gallese The Roots of Empathy: The Shared Manifold Hypothesis and the Neural Basis of Intersubjectivity , 2003, Psychopathology.

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

[93]  J. Mazziotta,et al.  Modulation of cortical activity during different imitative behaviors. , 2003, Journal of neurophysiology.

[94]  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.

[95]  J. Hollerman,et al.  Reward processing in primate orbitofrontal cortex and basal ganglia. , 2000, Cerebral cortex.

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

[97]  J. Panksepp Affective Neuroscience: The Foundations of Human and Animal Emotions , 1998 .

[98]  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.

[99]  Joseph E LeDoux Emotion circuits in the brain. , 2009, Annual review of neuroscience.

[100]  P. Mundy,et al.  Empathy and cognition in high-functioning children with autism. , 1992, Child development.

[101]  E. Bullmore,et al.  Investigation of facial recognition memory and happy and sad facial expression perception: an fMRI study , 1998, Psychiatry Research: Neuroimaging.