A neurobehavioral evolutionary perspective on the mechanisms underlying empathy

Progress in Neurobiology

Volumn 98, Issue 1, 2012, Pages 38-48

  Decety, Jean ^a   Norman, Greg J ^a   Berntson, Gary G ^b   Cacioppo, John T ^a  

^a UNIVERSITY OF CHICAGO   (United States)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

Affective neuroscience; Attachment; Caring; Empathy; Evolution; Pro social behavior; Social neuroscience

Indexed keywords

DOPAMINE; NEUROHORMONE; OXYTOCIN;

AFFECT; ANALGESIA; AVOIDANCE BEHAVIOR; BRAIN STEM; CINGULATE GYRUS; COGNITION; CRYING; DEFENSIVE BEHAVIOR; DOPAMINE RELEASE; EMOTIONAL ATTACHMENT; EMOTIONAL STRESS; EMPATHY; EVENT RELATED POTENTIAL; EXECUTIVE FUNCTION; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUNCTIONAL NEUROIMAGING; HUMAN; HYPOTHALAMUS; INFORMATION PROCESSING; INSULA; LANGUAGE; LEARNING; LIMBIC SYSTEM; NEOCORTEX; NEUROANATOMY; NEUROBIOLOGY; NOCICEPTION; NONHUMAN; PARENTAL BEHAVIOR; PERIAQUEDUCTAL GRAY MATTER; PHYLOGENY; PREFRONTAL CORTEX; PRIORITY JOURNAL; PSYCHOPATHY; REVIEW; REWARD; SENSORIMOTOR FUNCTION; SOCIAL BEHAVIOR; SPINE; SUBCORTEX; SUPPLEMENTARY MOTOR AREA; WELFARE; WORKING MEMORY;

ANIMALS; BIOLOGICAL EVOLUTION; BRAIN; CEREBRAL CORTEX; EMPATHY; FEMALE; HUMANS; LIMBIC SYSTEM; MALE; MAMMALS; MATERNAL BEHAVIOR; NEURONS; NEUROPEPTIDES; PATERNAL BEHAVIOR; PHYLOGENY; RECEPTORS, NEUROPEPTIDE; SOCIAL BEHAVIOR;

EID: 84861606718     PISSN: 03010082     EISSN: 18735118     Source Type: Journal    
DOI: 10.1016/j.pneurobio.2012.05.001     Document Type: Review

References (120)

1. Anderson M.L. Neural reuse: a fundamental organizational principle of the brain. Behavioral and Brain Sciences 2010, 33:245-313.
2. Anderson N.E., Kiehl K.A. The psychopath magnetized: insight from brain imaging. Trends in Cognitive Sciences 2012, 16:52-60.
3. Aniskiewicz A.S. Autonomic components of vicarious conditioning and psychopathy. Journal of Clinical Psychology 1979, 35:60-67.
4. Barnett M.A., Thompson S. The role of perspective taking and empathy in children's machiavellianism, prosocial behavior, and motive for helping. Journal of Genetic Psychology 2001, 146:295-305.
5. Barrett L.F., Henzi P., Dunbar R.I.M. Primate cognition: from what now to what if. Trends Cognitive Sciences 2003, 7:494-497.
6. Bartz J.A., Zaki J., Bolger N., Hollander E., Ludwig N.N., Kolevzon A., Ochsner K.N. Oxytocin selectively improves empathic accuracy. Psychological Science 2010, 114:1426-1428.
7. Batson C.D. These things called empathy: eight related but distinct phenomena. The Social Neuroscience of Empathy 2009, 3-15. MIT Press, Cambridge. J. Decety, W. Ickes (Eds.).
8. Batson C.D. Altruism in Humans 2011, Oxford University Press, New York.
9. Batson C.D., Early S., Salvarani H. Perspective taking: imagining how another feels versus imagining how you would feel. Personality and Social Psychology Bulletin 1997, 23:751-758.
10. Bell D.C. Evolution of parental caregiving. Personality and Social Psychology Review 2001, 5:216-229.
11. Bell D.C. The Dynamics of Connection 2010, Lexington Books, Plymouth, UK.
12. Ben-Ami Bartal I., Decety J., Mason P. Empathy and pro-social behavior in rats. Science 2011, 334:1427-1430.
13. Berntson G.G., Cacioppo J.T. The neuroevolution of motivation. Handbook of Motivation Science 2008, 188-200. Guilford, New York. J. Shah, W. Gardner (Eds.).
14. Blair R.J.R. Responsiveness to distress cues in the child with psychopathic tendencies. Personality and Individual Differences 1999, 27:135-145.
15. Blair R.J.R. A cognitive developmental approach to morality: investigating the psychopath. Cognition 1995, 57:1-29.
16. Bloom P. Moral nativism and moral psychology. The Social Psychology of Morality 2012, 71-89. APA, Washington, DC. M. Mikulincer, P.R. Shaver (Eds.).
17. Botvinick M., Jha A.P., Bylsma L.M., Fabian S., Solomon P., Prkachine K.M. Viewing facial expressions of pain engages cortical areas involved in the direct experience of pain. NeuroImage 2005, 25:312-319.
18. Brown J.L., Sheffield D., Leary M., Robinson M.E. Social support and experimental pain. Psychosomatic Medicine 2003, 65:276-283.
19. Brown S.L., Smith D.M., Schulz R., Kabeto M., Ubel P., Yee J., Kim C., Langa K. Caregiving and decreased mortality in a national sample of older adults. Psychological Science 2009, 20:488-494.
20. Buchanan T.W., Bagley S., Stansfield R.B., Preston S.D. The empathic, physiological resonance of stress. Social Neuroscience 2012, 7(2):191-201.
21. Cacioppo J.T., Hawkley L.C. Loneliness. Handbook of Individual Differences in Social Behavior 2009, 227-239. Guilford, New York. M.R. Leary, R.H. Hoyle (Eds.).
22. Cacioppo J.T., Patrick B. Loneliness: Human Nature and the Need for Social Connection 2009, W.W. Norton and Company, New York.
23. Carlezon W.A., Thomas M.J. Biological substrates of reward and aversion: a nucleus accumbens activity hypothesis. Neuropharmacology 2009, 56(Suppl. 1):122-132.
24. Carter C.S., Porges S.W. The neurobiology of social bonding and attachment. The Oxford Handbook of Social Neuroscience 2011, 151-163. Oxford University Press, New York. J. Decety, J.T. Cacioppo (Eds.).
25. Cheng Y., Chen C.Y., Lin C.P., Chou K.H., Decety J. Love hurts: an fMRI study. NeuroImage 2010, 51:923-929.
26. Cheng Y., Hung A., Decety J. Dissociation between affective sharing and emotion understanding in juvenile psychopaths. Development and Psychopathology 2012, 24:623-636.
27. Cheng Y., Lin C., Liu H.L., Hsu Y., Lim K., Hung D., Decety J. Expertise modulates the perception of pain in others. Current Biology 2007, 17:1708-1713.
28. Cheng Y., Yang C.Y., Lin C.P., Lee P.R., Decety J. The perception of pain in others suppresses somatosensory oscillations: a magnetoencephalography study. NeuroImage 2008, 40:1833-1840.
29. Church R.M. Emotional reactions of rats to the pain of others. Journal of Comparative and Physiological Psychology 1959, 52:132-134.
30. Cikara M., Botvinick M.M., Fiske S.T. Us versus them: social identity shapes responses to intergroup competition and harm. Psychological Science 2011, 22:306-313.
31. Clutton-Brock T.H. The Evolution of Parental Care 1991, Princeton University Press, Princeton, NJ.
32. Cockburn A. Prevalence of different modes of parental care in birds. Proceedings of the Royal Society London B: Biological Sciences 2006, 273:1375-2138.
33. Craig A.D. Interoception and emotion: a neuroanatomical perspective. Handbook of Emotion 2007, 272-288. Guilford Press, New York. 3rd ed. M. Lewis, J.M. Haviland-Jones, L.F. Barrett (Eds.).
34. Craig K.D. The social communication model of pain. Canadian Psychology 2009, 50:22-32.
35. Decety J. To what extent is the experience of empathy mediated by shared neural circuits?. Emotion Review 2010, 2:204-207.
36. Decety J. Dissecting the neural mechanisms mediating empathy. Emotion Review 2011, 3:92-108.
37. Decety J., Jackson P.L. The functional architecture of human empathy. Behavioral and Cognitive Neuroscience Reviews 2004, 3:71-100.
38. Decety J., Michalska K.J. Neurodevelopmental changes in the circuits underlying empathy and sympathy from childhood to adulthood. Developmental Science 2010, 13:886-899.
39. Decety J., Echols S.C., Correll J. The blame game: the effect of responsibility and social stigma on empathy for pain. Journal of Cognitive Neuroscience 2009, 22:985-997.
40. Decety J., Porges E.C. Imagining being the agent of actions that carry different moral consequences. Neuropsychologia 2011, 49:2994-3001.
41. Decety J., Yang C.Y., Cheng Y. Physicians down regulate their pain empathy response: an event-related brain potential study. NeuroImage 2010, 50:1676-1682.
42. De Waal F.B.M. Putting the altruism back into altruism: the evolution of empathy. Annual Review of Psychology 2008, 59:279-300.
43. Domes G., Heinrichs M., Michel A., Berger C., Herpertz S.C. Oxytocin attenuates amygdala responses to emotional faces regardless of valence. Biological Psychiatry 2007, 62:1187-1190.
44. Donaldson Z.R., Young L.J. Oxytocin, vasopressin, and the neurogenetics of sociality. Science 2008, 322:900-904.
45. Edgar J.L., Lowe J.C., Paul E.S., Nicol C.J. Avian maternal response to chick distress. Proceeding of the Royal Society: Biological Sciences 2011, 278:3129-3313.
46. Eisenberg N., Eggum N.D. Empathic responding: sympathy and personal distress. The Social Neuroscience of Empathy 2009, 71-83. MIT Press, Cambridge. J. Decety, W. Ickes (Eds.).
47. Eisenberger N. Why rejection hurts: what social neuroscience has revealed about the brain's response to social rejection. The Oxford Handbook of Social Neuroscience 2011, 586-598. Oxford University Press. J. Decety, J.T. Cacioppo (Eds.).
48. Ferris C.F., Kulkarni P., Sullivan J.M., Harder J.A., Messenger T.L., Febo M. Pup suckling is more rewarding than cocaine: evidence from functional magnetic resonance imaging and three-dimensional computational analysis. Journal of Neuroscience 2005, 25:149-156.
49. Fraser O.N., Stahl R.D., Aureli F. Stress reduction through consolation chimpanzees. Proceedings of the National Academy of Sciences of United States of America 2008, 105:8557-8856.
50. Goodwin N.B., Balshine-Earn S., Reynolds J.D. Evolutionary transitions in parental care in cichlid fish. Proceeding of the Royal Society: Biological Sciences 1998, 265:2265-3227.
51. Gu X., Liu X., Guise K.G., Naidich T.P., Hof P.R., Fan J. Functional dissociation of the frontoinsular and anterior cingulate cortices in empathy for pain. Journal of Neuroscience 2010, 30:3739-3744.
52. Haidt J., Graham J. When morality opposes justice: conservative have moral intuitions that liberals may not recognize. Social Justice Research 2007, 20:98-116.
53. Harbaugh W.T., Mayr U., Burghart D.R. Neural responses to taxation and voluntary giving reveal motives for charitable donations. Science 2007, 316:1622-1625.
54. Harris P.L. Understanding emotion. Handbook of Emotions 2000, 281-292. Guilford Press, New York. M. Lewis, J.M. Haviland-Jones (Eds.).
55. Hatfield E., Rapson R.L., Le Y.C. Emotional contagion and empathy. The Social Neuroscience of Empathy 2009, 19-30. MIT Press, Cambridge, MA. J. Decety, W. Ickes (Eds.).
56. Hawes D.J., Dadds M.R. Revisiting the role of empathy in childhood pathways to antisocial behavior. Emotions, Imagination, and Moral Reasoning 2012, 45-70. Psychology Press, New York. R. Langdon, C. Mackenzie (Eds.).
57. Hurlemann R., Patin A., Onur O.A., Cohen M.X., Baumgartner T., Metzler S., Dziobek I., Gallinat J., Wagner M., Maier W., Kendrick K.M. Oxytocin enhances amygdala-dependent, socially reinforced learning and emotion empathy in humans. Journal of Neuroscience 2010, 30:4999-5007.
58. Insel T.R., Young L.J. The neurobiology of attachment. Nature Reviews Neuroscience 2001, 2:129-136.
59. Izuma K., Saito D.N., Sadato N. Processing of the incentive for social approval in the ventral striatum during charitable donation. Journal of Cognitive Neuroscience 2010, 22:621-631.
60. Jackson J.H. Evolution and Dissolution of the Nervous System (Croonian Lectures) 1884, Reprinted in: Taylor, J. (Ed.), 1958. Selected Writings of John Hughlings Jackson. Basic Books, New York.
61. Jackson P.L., Brunet E., Meltzoff A.N., Decety J. Empathy examined through the neural mechanisms involved in imagining how I feel versus how you feel pain: an event-related fMRI study. Neuropsychologia 2006, 44:752-761.
62. Jackson P.L., Meltzoff A.N., Decety J. How do we perceive the pain of others? A window into the neural processes involved in empathy. NeuroImage 2005, 24:771-779.
63. Jenkins A.C., Mitchell J.P. Medial prefrontal cortex subserves diverse forms of self-reflection. Social Neuroscience 2011, 6(3):211-218.
64. 2+ channels in ACC. Nature Neuroscience 2010, 13:482-488.
65. Kirsch P., Esslinger C., Chen Q., Mier D., Lis S., Siddhanti S., Gruppe H., Mattay V.S., Galhofer B., Meyer-Lindenberg A. Oxytocin modulates neural circuitry for social cognition and fear in humans. Journal of Neuroscience 2005, 25:11489-11493.
66. Kosson D.S., Lorenz A.R., Newman J.P. Effects of comorbid psychopathy on criminal offending and emotion processing in male offenders with antisocial personality disorder. Journal of Abnormal Psychology 2006, 115:798-806.
67. Kross E., Berman M.E., Mischel W., Smith E.E., Wager T.D. Social rejection shares somatosensory representations with physical pain. Proceedings of the National Academy of Sciences of United States of America 2011, 108:6270-6275.
68. Lamm C., Batson C.D., Decety J. The neural basis of human empathy: effects of perspective-taking and cognitive appraisal. Journal of Cognitive Neuroscience 2007, 19:42-58.
69. Lamm C., Decety J., Singer T. Meta-analytic evidence for common and distinct neural networks associated with directly experienced pain and empathy for pain. NeuroImage 2011, 54:2492-2502.
70. Lamm C., Meltzoff A.N., Decety J. How do we empathize with someone who is not like us?. Journal of Cognitive Neuroscience 2010, 2:362-376.
71. Langford D.J., Crager S.E., Shehzad Z., Smith S.B., Sotocinal S.G., Levenstadt J., et al. Social modulation of pain as evidence for empathy in mice. Science 2006, 312:1967-1970.
72. Langford D.J., Tuttleb A.H., Brown K., Deschenes S., Fischer D.B., Mutso A., Root K.C., Sotocinal S.G., Stern M.A., Mogil J.S., Sternberg W.F. Social approach to pain in laboratory mice. Social Neuroscience 2010, 5:163-170.
73. Legrain V., Iannetti G.D., Plaghki L., Moureaux A. The pain matrix reloaded: a salience detection system for the body. Progress in Neurobiology 2011, 93:111-124.
74. Lieberman M.D., Eisenberger N.I., Crockett M.J., Tom S.M., Pfeifer J.H., Way B.M. Putting feelings into words: affect labeling disrupts amygdala activity to affective stimuli. Psychological Science 2007, 18:421-428.
75. Lucht M.J., Barnow S., Sonnenfeld C., Rosenberger A., Joergen Grabve H., Schroeder W., Völzke H., Freyberger H.J., Herrmann F.H., Kroemer H., Rosskopf D. Associations between the oxytocin receptor gene (OXTR) and affect, loneliness and intelligence in normal subjects. Progress in Neuro-Psychopharmacology and Biological Psychiatry 2009, 33:860-866.
76. MacDonald G., Leary M.R. Why does social exclusion hurt? The relationship between social and physical pain. Psychological Bulletin 2005, 131:202-223.
77. MacLean P.D. Brain evolution relating to family, play, and the separation call. Archives of General Psychiatry 1985, 42:405-417.
78. Maestripieri D. Neurobiology of social behavior. Primate Neuroethology 2010, 359-384. Oxford University Press, New York. M.I. Platt, A.A. Ghazanfar (Eds.).
79. Mason P., Ben Ami-Bartal I. How the social brain experiences empathy: summary of a gathering. Social Neuroscience 2010, 5:252-256.
80. Mayes L.C., Magidson J., Lejuez C.W., Nichols S.S. Social relationships as primary rewards. Handbook of Developmental Social Neuroscience 2009, 342-377. Guilford Press, New York. M. De Haan, M.R. Gunnar (Eds.).
81. Menon V., Uddin L.Q. Saliency, switching, attention and control: a network model of insula function. Brain Structure and Function 2010, 214:655-667.
82. Moll J., Krueger F., Zahn R., Pardini M., de Oliveira-Souza R., Grafman J. Human fronto-mesolimbic networks guide decisions about charitable donation. Proceedings of the National Academy of Sciences of United States of America 2006, 103:15623-21562.
83. Norman G.J., Karelina K., Morris J.S., Zhang N., Cochran M., DeVries A.C. Social interaction prevents the development of depressive-like behavior post nerve injury in mice: a potential role for oxytocin. Psychosomatic Medicine 2010, 72:519-526.
84. Norman G.J., Cacioppo J.T., Morris J.S., Karelina K., Malarkey W.B., DeVries A.C., Berntson G.G. Selective influences of oxytocin on the evaluative processing of social stimuli. Psychopharmacology 2011, 25(10):1313-1319.
85. Norman G.J., Hawkley L.C., Cole S.W., Berntson G.G., Cacioppo J.T. Social neuroscience: the social brain, oxytocin, and health. Social Neuroscience 2012, 7(1):18-29.
86. Norman G.J., Hawkley L., Luhmann M., Ball A.B., Cole S.W., Berntson G.G., Cacioppo J.T. Variation in the oxytocin receptor gene influences neurocardiac stress reactivity to social stress and HPA function: a population based study. Hormones and Behavior 2012, 61(1):134-139.
87. Norris C.J., Gollan J., Bertson G.G., Cacioppo J.T. The current status of research on the structure of the evaluative space. Biological Psychology 2010, 84:422-436.
88. Numan M. Hypothalamic neural circuits regulating maternal responsiveness toward infants. Behavioral Cognitive Neuroscience Reviews 2006, 5:163-190.
89. Panksepp J. Affective Neuroscience: The Foundations of Human and Animal Emotions 1998, Oxford University Press, London.
90. Panksepp J. Affective neuroscience of the emotional brain: evolutionary perspectives and implications for understanding depression. Dialogues in Clinical Neuroscience 2010, 12:389-399.
91. Panksepp J. Empathy and the laws of affect. Science 2011, 334:1358-1359.
92. Parr L.A. Cognitive and physiological markers of emotional awareness in chimpanzees (Pan troglodytes). Animal Cognition 2001, 4:223-229.
93. Parvizi J. Corticocentric myopia: old bias in new cognitive sciences. Trends in Cognitive Sciences 2009, 13:354-358.
94. Pinker S. The Better Angels of Our Nature 2011, Penguin Group, New York.
95. Porges S.W. Love: an emergent property of the mammalian autonomic nervous system. Psychoneuroendocrinology 1998, 23:837-861.
96. Pulvermuller F. Brain mechanisms linking language and action. Nature Reviews Neuroscience 2005, 6:576-582.
97. Rice G.E., Gainer P. Altruism in the albino rat. Journal of Comparative and Physiological Psychology 1962, 55:123-125.
98. Rodrigues S.M., Saslow L.R., Garcia N., John O.P., Keltner D. Oxytocin receptor genetic variation relates to empathy and stress reactivity in humans. Proceedings of the National Academy of Sciences of United States of America 2009, 106:21437-21441.
99. Romero T., Castellanos M.A., de Waal F.B.M. Consolation as possible expression of sympathetic concern among chimpanzees. Proceedings of the National Academy of Sciences of United States of America 2010, 107:12110-12115.
100. Ross H.E., Freeman S.M., Spiegel L.L., Ren X., Terwilliger E.F., Young L.J. Variation in oxytocin receptor density in the nucleus accumbens has differential effects on affiliative behaviors in monogamous and polygamous voles. Journal of Neuroscience 2009, 29:1312-1318.
101. Roth-Hanania R., Davidov M., Zahn-Waxler C. Empathy development from 8 to 16 months: early signs of concern for others. Infant Behavior and Development 2011, 34:447-458.
102. Ruby P., Decety J. How would you feel versus how do you think she would feel? A neuroimaging study of perspective taking with social emotions. Journal of Cognitive Neuroscience 2004, 16:988-999.
103. Ruby P., Decety J. What you believe versus what you think they believe? A neuroimaging study of conceptual perspective taking. European Journal of Neuroscience 2003, 17:2475-2480.
104. Sambo C.F., Howard M., Kopelman M., Williams S., Fotopoulou A. Knowing you care: effects of perceived empathy and attachment style on pain perception. Pain 2010, 151:687-693.
105. Shackman A.J., Salomons T.V., Slagter H., Fox A.S., Winter J.J., Davidson R.J. The integration of negative affect, pain and cognitive control in the cingulate cortex. Nature Review Neuroscience 2011, 12:154-167.
106. Singer P. The Expanding Circle: Ethics and Sociobiology 1986, Princeton University Press, Princeton, NJ.
107. Singer T., Seymour B., O'Doherty J., et al. Empathy for pain involves the affective but not the sensory components of pain. Science 2004, 303:1157-1161.
108. Singer T., Seymour B., O'Doherty J.P., Stephan K.E., Dolan R.D., Frith C.D. Empathic neural responses are modulated by the perceived fairness of others. Nature 2006, 439:466-469.
109. Stone V. The moral dimensions of human social intelligence. Philosophical Explorations 2006, 9:55-68.
110. Strathearn L., Fonagy P., Amico J., Montague P.R. Adult attachment predicts maternal brain and oxytocin response to infant cues. Neuropharmacology 2009, 13:2655-2666.
111. Tabibnia G., Lieberman M.D., Craske M.G. The lasting effect of words on feelings: words may facilitate exposure effects to threatening images. Emotion 2008, 8:307-317.
112. Taylor S.E. The Tending Instinct 2002, Henry Holt, New York.
113. Tost H., Kolachana B., Hakimi S., Lemaitre H., Verchinski B.A., Mattay V.S., et al. A common allele in the oxytocin receptor gene (OXTR) impacts prosocial temperament and human hypothalamic-limbic structure and function. Proceedings of the National Academy of Sciences of United States of America 2010, 107:13936-13941.
114. Tucker D.M., Luu P., Derryberry D. Love hurts: the evolution of empathic concern through the encephalization of nociceptive capacity. Development and Psychopathology 2005, 17:699-713.
115. Uchino B.N., Cacioppo J.T., Kiecolt-Glaser J.K. The relationship between social support and physiological processes: a review with emphasis on underlying mechanisms and implications for health. Psychological Bulletin 1996, 119:488-531.
116. Vaish A., Warneken F. Social-cognitive contributors to young children's empathic and prosocial behavior. Empathy - From Bench to Bedside 2012, 131-146. MIT Press, Cambridge. J. Decety (Ed.).
117. Warneken F., Hare B., Melis A.P., Hanus D., Tomasello M. Spontaneous altruism by chimpanzees and young children. PLoS Biology 2007, 5:e184.
118. Watt D.F. The centrencephalon and thalamocortical integration: neglected contributions of periaqueductal gray. Emotion and Consciousness 2000, 1:93-116.
119. Wilson E.O. Sociobiology: The New Synthesis 1975, Belknap, Cambridge, MA.
120. Xu X., Zuo X., Wang L., Han S. Do you feel my pain? Racial group membership modulates empathic neural responses. Journal of Neuroscience 2009, 29:8525-8529.