The pain of a model in the personality of an onlooker: Influence of state-reactivity and personality traits on embodied empathy for pain

The study of inter-individual differences at behavioural and neural levels represents a new avenue for neuroscience. The response to socio-emotional stimuli varies greatly across individuals. For example, identification with the feelings of a movie character may be total for some people or virtually absent for others. Inter-individual differences may reflect both the on-line effect (state) of the observed stimuli and more stable personal characteristics (trait). Here we show that somatomotor mirror responses when viewing others' pain are modulated by both state- and trait-differences in empathy. We recorded motor-evoked potentials (MEPs) induced by Transcranial Magnetic Stimulation (TMS) in healthy individuals observing needles penetrating a model's hand. We found a reduction of corticospinal excitability that was specific for the muscle that subjects observed being penetrated. This inhibition correlated with sensory qualities of the pain ascribed to the model. Moreover, it was greater in subjects with high trait-cognitive empathy and lower in subjects with high trait-personal distress and in those with high aversion for the observed movies. Results indicate that somatomotor responses to others' pain are influenced by specific onlookers' personality traits and self-oriented emotional reactions. Our findings suggest that multiple distinct mechanisms shape mirror mapping of others' pain.

[1]  N. Eisenberg.  Emotion, regulation, and moral development. , 2000, Annual review of psychology.

[2]  K. Craig,et al.  Facing others in pain: the effects of empathy , 2005, Pain.

[3]  Riitta Hari,et al.  Activation of the human primary motor cortex during observation of tool use , 2004, NeuroImage.

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

[5]  C. Keysers,et al.  Empathy and the Somatotopic Auditory Mirror System in Humans , 2006, Current Biology.

[6]  Amy Coplan.  Simulating Minds: The Philosophy, Psychology, and Neuroscience of Mindreading by goldman, alvin , 2008 .

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

[8]  Amanda C.C. Williams,et al.  Facial expression of pain: An evolutionary account , 2002, Behavioral and Brain Sciences.

[9]  Robert C. Coghill,et al.  Neural correlates of interindividual differences in the subjective experience of pain , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[10]  Matthew D. Lieberman,et al.  Does Rejection Hurt? An fMRI Study of Social Exclusion , 2003, Science.

[11]  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.

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

[13]  C. Batson.  The Altruism Question: Toward A Social-psychological Answer , 1991 .

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

[15]  Beate Herpertz-Dahlmann,et al.  Response to emotional stimuli in boys with conduct disorder. , 2005, The American journal of psychiatry.

[16]  T. Chartrand,et al.  The chameleon effect: the perception-behavior link and social interaction. , 1999, Journal of personality and social psychology.

[17]  V. Gallese.  Intentional attunement: A neurophysiological perspective on social cognition and its disruption in autism , 2006, Brain Research.

[18]  M. Mancia.  Psychoanalysis and Neuroscience , 2006 .

[19]  Salvatore Maria Aglioti,et al.  Empathy for pain and touch in the human somatosensory cortex. , 2007, Cerebral cortex.

[20]  Richard P. DeShon,et al.  Combining effect size estimates in meta-analysis with repeated measures and independent-groups designs. , 2002, Psychological methods.

[21]  Po-Lei Lee,et al.  The perception of pain in others suppresses somatosensory oscillations: A magnetoencephalography study , 2008, NeuroImage.

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

[23]  M. Hallett,et al.  Depression of motor cortex excitability by low‐frequency transcranial magnetic stimulation , 1997, Neurology.

[24]  R. Peyron,et al.  Functional imaging of brain responses to pain. A review and meta-analysis (2000) , 2000, Neurophysiologie Clinique/Clinical Neurophysiology.

[25]  G. Rizzolatti,et al.  Corticocortical connections of area F3 (SMA‐proper) and area F6 (pre‐SMA) in the macaque monkey , 1993, The Journal of comparative neurology.

[26]  M. Sonnby-Borgström.  Automatic mimicry reactions as related to differences in emotional empathy. , 2002, Scandinavian journal of psychology.

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

[28]  Salvatore Maria Aglioti,et al.  Stimulus-driven modulation of motor-evoked potentials during observation of others' pain , 2006, NeuroImage.

[29]  W. Dunlap,et al.  Meta-Analysis of Experiments With Matched Groups or Repeated Measures Designs , 1996 .

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

[31]  Viviana Betti,et al.  Seeing the pain of others while being in pain: A laser-evoked potentials study , 2008, NeuroImage.

[32]  M. Hallett,et al.  Optimal Focal Transcranial Magnetic Activation of the Human Motor Cortex: Effects of Coil Orientation, Shape of the Induced Current Pulse, and Stimulus Intensity , 1992, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[33]  Jacob Cohen.  Statistical Power Analysis for the Behavioral Sciences , 1969, The SAGE Encyclopedia of Research Design.

[34]  S-J Blakemore,et al.  Somatosensory activations during the observation of touch and a case of vision-touch synaesthesia. , 2005, Brain : a journal of neurology.

[35]  P. Rainville.  Brain mechanisms of pain affect and pain modulation , 2002, Current Opinion in Neurobiology.

[36]  M Manfredi,et al.  Silent period in upper limb muscles after noxious cutaneous stimulation in man. , 1997, Electroencephalography and clinical neurophysiology.

[37]  Peter Svensson,et al.  Suppression of motor evoked potentials in a hand muscle following prolonged painful stimulation , 2003, European journal of pain.

[38]  Fausta Lui,et al.  Does It Look Painful or Disgusting? Ask Your Parietal and Cingulate Cortex , 2008, The Journal of Neuroscience.

[39]  Jean Decety,et al.  Expertise Modulates the Perception of Pain in Others , 2007, Current Biology.

[40]  D. Drubach.  Absence of Embodied Empathy During Pain Observation in Asperger Syndrome , 2009 .

[41]  E. Wassermann.  Risk and safety of repetitive transcranial magnetic stimulation: report and suggested guidelines from the International Workshop on the Safety of Repetitive Transcranial Magnetic Stimulation, June 5-7, 1996. , 1998, Electroencephalography and clinical neurophysiology.

[42]  Jacob Cohen,et al.  A power primer. , 1992, Psychological bulletin.

[43]  Riitta Hari,et al.  The compassionate brain: humans detect intensity of pain from another's face. , 2006, Cerebral cortex.

[44]  B. Thorn,et al.  Catastrophizing and perceived partner responses to pain , 2004, Pain.

[45]  S. Aglioti,et al.  Left hemisphere dominance in reading the sensory qualities of others’ pain? , 2006, Social neuroscience.

[46]  P. Rossini,et al.  Non-invasive electrical and magnetic stimulation of the brain, spinal cord and roots: basic principles and procedures for routine clinical application. Report of an IFCN committee. , 1994, Electroencephalography and clinical neurophysiology.

[47]  Lawrence H Staib,et al.  Neural correlates of exposure to traumatic pictures and sound in Vietnam combat veterans with and without posttraumatic stress disorder: a positron emission tomography study , 1999, Biological Psychiatry.

[48]  Chester W. Harris,et al.  On factors and factor scores , 1967 .

[49]  R. R. Reno,et al.  Relation of sympathy and personal distress to prosocial behavior: a multimethod study. , 1989, Journal of personality and social psychology.

[50]  G. Rizzolatti,et al.  Motor facilitation during action observation: a magnetic stimulation study. , 1995, Journal of neurophysiology.

[51]  Thomas Straube,et al.  Waiting for spiders: Brain activation during anticipatory anxiety in spider phobics , 2007, NeuroImage.

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

[53]  L. Fogassi,et al.  A Touching Sight SII/PV Activation during the Observation and Experience of Touch , 2004, Neuron.

[54]  P P Urban,et al.  Different short‐term modulation of cortical motor output to distal and proximal upper‐limb muscles during painful sensory nerve stimulation , 2004, Muscle & nerve.

[55]  J. Decety,et al.  Gender Differences in the Mu Rhythm of the Human Mirror-Neuron System , 2008, PloS one.

[56]  D. Murphy,et al.  Motor cortex excitability correlates with an anxiety-related personality trait , 2001, Biological Psychiatry.

[57]  Jejo D. Koola,et al.  Emotion facilitates action: a transcranial magnetic stimulation study of motor cortex excitability during picture viewing. , 2007, Psychophysiology.

[58]  C. Babiloni,et al.  Influence of the supplementary motor area on primary motor cortex excitability during movements triggered by neutral or emotionally unpleasant visual cues , 2003, Experimental Brain Research.

[59]  S. Boniface,et al.  Magnetic brain stimulation with a double coil: the importance of coil orientation. , 1992, Electroencephalography and clinical neurophysiology.

[60]  Á. Pascual-Leone,et al.  Psychopathy and the mirror neuron system: Preliminary findings from a non-psychiatric sample , 2008, Psychiatry Research.

[61]  Natalie Sebanz,et al.  Simulation, mirroring, and a different argument from error , 2005, Trends in Cognitive Sciences.

[62]  R. C. Oldfield.  The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[63]  G. V. Van Hoesen,et al.  Cingulate input to the primary and supplementary motor cortices in the rhesus monkey: Evidence for somatotopy in areas 24c and 23c , 1992, The Journal of comparative neurology.

[64]  E. Sanavio,et al.  Semantics of pain in Italy: the Italian version of the McGill Pain Questionnaire , 1985, Pain.

[65]  A. Meltzoff,et al.  Empathy examined through the neural mechanisms involved in imagining how I feel versus how you feel pain , 2006, Neuropsychologia.

[66]  D G von Keyserlingk,et al.  Representation of cortical motor function as revealed by stereotactic transcranial magnetic stimulation. , 1998, Electroencephalography and clinical neurophysiology.

[67]  M. Hoffman,et al.  Interaction of affect and cognition in empathy. , 1985 .

[68]  Nadia Bolognini,et al.  Somatic and Motor Components of Action Simulation , 2007, Current Biology.

[69]  S. Aglioti,et al.  The Sensorimotor Side of Empathy for Pain , 2006 .

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

[71]  Jean Decety,et al.  Empathy and judging other's pain: an fMRI study of alexithymia. , 2007, Cerebral cortex.

[72]  C. Keysers,et al.  Towards a unifying neural theory of social cognition. , 2006, Progress in brain research.

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

[74]  R. Melzack.  The McGill Pain Questionnaire: Major properties and scoring methods , 1975, PAIN.

[75]  Massimiliano Valeriani,et al.  Pain-related modulation of the human motor cortex , 2003, Neurological research.

[76]  Mark H. Davis.  Empathy: A Social Psychological Approach , 1994 .