The psychophysiological measurement of empathy

Empathy is a multifaceted construct that has traditionally been studied using selfreport measures. The field of psychophysiology is increasingly offering additional measurement techniques to objectively record changes associated with empathy in the central and autonomic nervous system. The present chapter will review what can be gained by studying empathy using psychophysiological methods such as neuroimaging, electroencephalogram (EEG), facial electromyographic activity (EMG), startle blink reflexes, skin conductance responding, and heart rate. These psychophysiological measurements are particularly well suited to studying (a) the mimicry of facial expressions, (b) emotional contagion and the mirror neuron system, (c) correlates between nervous system changes and self-report measures of empathy, and (d) empathy in special populations. Moreover, psychophysiological measures may offer more objectivity than self-report measures and can be used in individuals for whom self-report measures may be unreliable or unsuitable (e.g., children). Future research using a multimethod approach combining self-report, behavioural, and psychophysiological measurements has the potential to significantly broaden and advance our understanding of empathy.

[1]  M. Bradley,et al.  Brain potentials in affective picture processing: covariation with autonomic arousal and affective report , 2000, Biological Psychology.

[2]  Albert Gjedde,et al.  Emotional valence modulates activity in the posterior fusiform gyrus and inferior medial prefrontal cortex in social perception , 2003, NeuroImage.

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

[4]  A. Gale,et al.  Extraversion–introversion, neuroticism–stability, and EEG indicators of positive and negative empathic mood , 2001 .

[5]  A. Meltzoff,et al.  What imitation tells us about social cognition: a rapprochement between developmental psychology and cognitive neuroscience. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[6]  C. Darwin,et al.  The Expression of the Emotions in Man and Animals , 1956 .

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

[8]  Hugo D. Critchley,et al.  Psychophysiology of neural, cognitive and affective integration: fMRI and autonomic indicants , 2008, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[9]  Michael J Vitacco,et al.  Neurobiology of empathy and callousness: implications for the development of antisocial behavior. , 2009, Behavioral sciences & the law.

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

[11]  Shihui Han,et al.  Temporal dynamic of neural mechanisms involved in empathy for pain: An event-related brain potential study , 2008, Neuropsychologia.

[12]  R. Levenson,et al.  Empathy: a physiological substrate. , 1992, Journal of personality and social psychology.

[13]  R. L. Hagen,et al.  Empathy: review of available measures , 1985 .

[14]  M. Hoffman How automatic and representational is empathy, and why , 2001 .

[15]  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.

[16]  Nadim Joni Shah,et al.  Gender differences in brain networks supporting empathy , 2008, NeuroImage.

[17]  U. Dimberg,et al.  Facial reactions to emotional stimuli: Automatically controlled emotional responses , 2002 .

[18]  Jean Decety,et al.  Who caused the pain? An fMRI investigation of empathy and intentionality in children , 2008, Neuropsychologia.

[19]  H. Soderstrom,et al.  Psychopathy as a disorder of empathy , 2003, European Child & Adolescent Psychiatry.

[20]  Tania Singer,et al.  The painful side of empathy , 2005, Nature Neuroscience.

[21]  M. Inzlicht,et al.  Empathy constrained: Prejudice predicts reduced mental simulation of actions during observation of outgroups. , 2010 .

[22]  W. Sato,et al.  Facial expression arousal level modulates facial mimicry. , 2010, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[23]  Riitta Parkkola,et al.  Is emotional contagion special? An fMRI study on neural systems for affective and cognitive empathy , 2008, NeuroImage.

[24]  Ravi S. Menon,et al.  Dissociating pain from its anticipation in the human brain. , 1999, Science.

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

[26]  B. Parkinson,et al.  Emotion and motivation , 1995 .

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

[28]  T. Farrow Empathy in Mental Illness: Neuroimaging of empathy , 2007 .

[29]  Timothy D. Wilson,et al.  Telling more than we can know: Verbal reports on mental processes. , 1977 .

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

[31]  G. Rizzolatti,et al.  Hearing Sounds, Understanding Actions: Action Representation in Mirror Neurons , 2002, Science.

[32]  Julia Schikora,et al.  Empathy and social desirability: a comparison of delinquent and non-delinquent participants using direct and indirect measures , 2009 .

[33]  Dc Washington Diagnostic and Statistical Manual of Mental Disorders, 4th Ed. , 1994 .

[34]  P. Jönsson,et al.  Emotional Empathy as Related to Mimicry Reactions at Different Levels of Information Processing , 2003 .

[35]  A. Sirigu,et al.  Racial Bias Reduces Empathic Sensorimotor Resonance with Other-Race Pain , 2010, Current Biology.

[36]  T. Reik Listening with the third ear : the inner experience of a psychoanalyst , 1972 .

[37]  L. Fogassi,et al.  Audiovisual mirror neurons and action recognition , 2003, Experimental Brain Research.

[38]  Maria Luisa Gorno-Tempini,et al.  Structural anatomy of empathy in neurodegenerative disease. , 2006, Brain : a journal of neurology.

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

[40]  S. Filipović,et al.  Psychophysiology: Human Behavior and Physiological Response (4th ed.) , 2001 .

[41]  D Krebs Empathy and altruism. , 1975, Journal of personality and social psychology.

[42]  Gilles Pourtois,et al.  Simultaneous recording of EEG and facial muscle reactions during spontaneous emotional mimicry , 2008, Neuropsychologia.

[43]  Michael J. Brammer,et al.  The role of ‘shared representations’ in social perception and empathy: An fMRI study , 2006, NeuroImage.

[44]  Tokiko Harada,et al.  Neural basis of extraordinary empathy and altruistic motivation , 2010, NeuroImage.

[45]  Lihua Mao,et al.  Event-related theta and alpha oscillations mediate empathy for pain , 2008, Brain Research.

[46]  A. M. Meneghini,et al.  Adattamento italiano della Balanced Emotional Empathy Scale (BEES) di Albert Mehrabian , 2012 .

[47]  A. Anokhin,et al.  Startle modulation by affective faces , 2010, Biological Psychology.

[48]  Tilo Kircher,et al.  Neural mechanisms of empathy in adolescents with autism spectrum disorder and their fathers , 2010, NeuroImage.

[49]  Xiaoying Wang,et al.  Do You Feel My Pain? Racial Group Membership Modulates Empathic Neural Responses , 2009, The Journal of Neuroscience.

[50]  A. Mehrabian,et al.  A measure of emotional empathy. , 1972, Journal of personality.

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

[52]  W. Iacono Psychophysiological Assessment of Psychopathology , 1991 .

[53]  John C. Mazziotta,et al.  Mirroring others' emotions relates to empathy and interpersonal competence in children , 2008, NeuroImage.

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

[55]  M. Bushnell,et al.  Cortical representation of the sensory dimension of pain. , 2001, Journal of neurophysiology.

[56]  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.

[57]  F. D. de Waal Putting the altruism back into altruism: the evolution of empathy. , 2008, Annual review of psychology.

[58]  J. Decety,et al.  Gender differences in the mu rhythm during empathy for pain: An electroencephalographic study , 2009, Brain Research.

[59]  L. Brothers,et al.  A biological perspective on empathy. , 1989, The American journal of psychiatry.

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

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

[62]  Robert T. Knight,et al.  Neural activity during social signal perception correlates with self-reported empathy , 2010, Brain Research.

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

[64]  J. Cacioppo,et al.  Handbook Of Psychophysiology , 2019 .

[65]  M. Bradley,et al.  Looking at facial expressions: Dysphoria and facial EMG , 2002, Biological Psychology.

[66]  Ute Habel,et al.  Multidimensional assessment of empathic abilities: Neural correlates and gender differences , 2010, Psychoneuroendocrinology.

[67]  Clara E. Hill,et al.  The current state of empathy research , 1996 .

[68]  Jaime Vila,et al.  Startle reflex modulation, affective ratings and autonomic reactivity in incarcerated Spanish psychopaths. , 2003, Psychophysiology.

[69]  Ruud Zaalberg,et al.  Facial EMG responses to dynamic emotional facial expressions in boys with disruptive behavior disorders. , 2006, Journal of psychiatric research.

[70]  J. Decety,et al.  Perspective taking is associated with specific facial responses during empathy for pain , 2008, Brain Research.

[71]  P. Winkielman,et al.  When the social mirror breaks: deficits in automatic, but not voluntary, mimicry of emotional facial expressions in autism. , 2006, Developmental science.

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

[73]  D. Price Psychological and neural mechanisms of the affective dimension of pain. , 2000, Science.

[74]  J. Maisog,et al.  Pain intensity processing within the human brain: a bilateral, distributed mechanism. , 1999, Journal of neurophysiology.

[75]  J. Cacioppo,et al.  Handbook Of Psychophysiology , 2019 .

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

[77]  Jeff T. Larsen,et al.  Effects of positive and negative affect on electromyographic activity over zygomaticus major and corrugator supercilii. , 2003, Psychophysiology.

[78]  C. Patrick,et al.  Emotion and psychopathy: startling new insights. , 1994, Psychophysiology.

[79]  Nancy Eisenberg,et al.  Sex Differences in Empathy and Related Capacities , 1983 .

[80]  J. Kwon,et al.  Multi-level comparison of empathy in schizophrenia: An fMRI study of a cartoon task , 2010, Psychiatry Research: Neuroimaging.

[81]  Benjamin B. Lahey,et al.  Atypical empathic responses in adolescents with aggressive conduct disorder: A functional MRI investigation , 2009, Biological Psychology.

[82]  William Ickes,et al.  Naturalistic Social Cognition: Empathic Accuracy in Mixed-Sex Dyads , 1990 .

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

[84]  M. Shane,et al.  The Developmental Trajectory from Amodal Perception to Empathy and Communication: The Role of Mirror Neurons in This Process , 2001 .

[85]  I. Wilkinson,et al.  Quantifiable change in functional brain response to empathic and forgivability judgments with resolution of posttraumatic stress disorder , 2005, Psychiatry Research: Neuroimaging.

[86]  Peter J. Lang,et al.  Affective reactions to pictures of ingroup and outgroup members , 2006, Biological Psychology.

[87]  J. Andreassi Psychophysiology: Human Behavior and Physiological Response , 1980 .

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

[89]  Andreas Kleinschmidt,et al.  A structural neural deficit in adolescents with conduct disorder and its association with lack of empathy , 2007, NeuroImage.

[90]  D. Neumann,et al.  Empathy-related responses to moving film stimuli depicting human and non-human animal targets in negative circumstances , 2008, Biological Psychology.

[91]  U. Dimberg,et al.  Facial reactions to different emotionally relevant stimuli , 1997 .

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

[93]  Jean Decety,et al.  Physicians down-regulate their pain empathy response: An event-related brain potential study , 2010, NeuroImage.

[94]  Simone G. Shamay-Tsoory,et al.  The neural correlates of understanding the other's distress: A positron emission tomography investigation of accurate empathy , 2005, NeuroImage.

[95]  U. Dimberg,et al.  Rapid facial reactions to emotional facial expressions. , 1998, Scandinavian journal of psychology.

[96]  C. Batson These things called empathy: Eight related but distinct phenomena. , 2009 .

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

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

[99]  U Dimberg,et al.  Facial electromyography and emotional reactions. , 1990, Psychophysiology.

[100]  The Independent Effects of Attention and Lead Stimulus Properties on the Acoustic Blink Reflex , 2003 .

[101]  M. Bradley,et al.  Emotion in the criminal psychopath: startle reflex modulation. , 1993, Journal of abnormal psychology.

[102]  The clinical relevance of psychophysiology: support for the psychobiology of empathy and psychodynamic process. , 2005, American journal of psychotherapy.

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

[104]  U. Dimberg,et al.  Unconscious Facial Reactions to Emotional Facial Expressions , 2000, Psychological science.

[105]  Richard J Davidson,et al.  Empathy is associated with dynamic change in prefrontal brain electrical activity during positive emotion in children. , 2009, Child development.

[106]  Andrew N. Meltzoff,et al.  How do we perceive the pain of others? A window into the neural processes involved in empathy , 2005, NeuroImage.

[107]  Peter W. R. Woodruff,et al.  Empathy in Mental Illness , 2007 .

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

[109]  M. Bushnell,et al.  Pain affect encoded in human anterior cingulate but not somatosensory cortex. , 1997, Science.

[110]  Lihua Mao,et al.  Gender difference in empathy for pain: An electrophysiological investigation , 2008, Brain Research.