Mammalian empathy: Behavioural manifestations and neural basis

Nature Reviews Neuroscience

Volumn 18, Issue 8, 2017, Pages 498-509

  De Waal, Frans B M ^a   Preston, Stephanie D ^b  

^a EMORY UNIVERSITY   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALTRUISM; ANIMAL BEHAVIOR; BEHAVIORAL RESEARCH; BRAIN; CONSOLATION; COOPERATION; EMOTIONAL CONTAGION; EMPATHY; EVOLUTION; HUMAN; MAMMAL; MIRROR NEURON; NEUROSCIENCE; NONHUMAN; PAIN; PERCEPTION; PRIORITY JOURNAL; REVIEW; THEORY OF MIND; YAWNING; ANIMAL; BIOLOGICAL MODEL; CYTOLOGY; EMOTION; PHYSIOLOGY; PSYCHOLOGY;

ANIMALS; BEHAVIOR, ANIMAL; BIOLOGICAL EVOLUTION; BRAIN; EMOTIONS; EMPATHY; HUMANS; MAMMALS; MIRROR NEURONS; MODELS, NEUROLOGICAL;

EID: 85025100901     PISSN: 1471003X     EISSN: 14710048     Source Type: Journal    
DOI: 10.1038/nrn.2017.72     Document Type: Review

References (139)

1. Preston, S. D. & de Waal, F. B. M. Empathy: Its ultimate and proximate bases. Behav. Brain Sci. 25, 1-71 (2002).
2. Goldman, A. I. Simulating Minds: The Philosophy, Psychology, and Neuroscience of Mindreading (Oxford Univ. Press, 2006).
3. Baron-Cohen, S. in The Lost Self: Pathologies of the Brain and Identity (eds Feinberg, T. E. & Keenan, J. P.) 166-180 (Oxford Univ. Press, 2005).
4. Zahavi, D. Simulation, projection and empathy. Conscious. Cogn. 17, 514-522 (2008).
5. Lipps, T. Einfühlung, innere nachahmung und organenempfindungen [German]. Arch. Gesamte Psychol. 1, 465-519 (1903).
6. de Waal, F. B. M. Putting the altruism back into altruism: The evolution of empathy. Annu. Rev. Psychol. 59, 279-300 (2008).
7. Preston, S. D. & Hofelich, A. J. The many faces of empathy: Parsing empathic phenomena through a proximate, dynamic-systems view of representing the other in the self. Emot. Rev. 4, 24-33 (2012).
8. Zahn-Waxler, C. & Radke-Yarrow, M. The origins of empathic concern. Motiv. Emot. 14, 107-130 (1990).
9. Walter, H. Social cognitive neuroscience of empathy: Concepts, circuits, and genes. Emot. Rev. 4, 9-17 (2012).
10. Darwin, C. The Descent of Man, and Selection in Relation to Sex (Princeton Univ. Press, 1982).
11. Plutchik, R. in Empathy and its Development (eds Eisenberg, N. & Strayer, J.) 3-46 (Cambridge Univ. Press, 1987).
12. de Waal, F. B. M. Good Natured (Harvard Univ. Press, 1996).
13. Krupenye, C., Kano, F., Hirata, S., Call, J. & Tomasello, M. Great apes anticipate that other individuals will act according to false beliefs. Science 354, 110-114 (2016).
14. de Waal, F. B. M. The Age of Empathy (Harmony Books, 2009).
15. Yamamoto, S., Humle, T. & Tanaka, M. Chimpanzees' flexible targeted helping based on an understanding of conspecifics' goals. Proc. Natl Acad. Sci. USA 109, 3588-3592 (2012).
16. Hattori, Y., Leimgruber, K., Fujita, K. & de Waal, F. B. M. Food-related tolerance in capuchin monkeys (Cebus apella) varies with knowledge of the partner's previous food-consumption. Behaviour 149, 171- 185 (2012).
17. Bateson, P. & Laland, K. N. Tinbergen's four questions: An appreciation and an update. Trends Ecol. Evol. 28, 712-718 (2013).
18. Tinbergen, N. On aims and methods of ethology [German]. Z. Tierpsychol. 20, 410-433 (1963).
19. Church, R. M. Emotional reactions of rats to the pain of others. J. Comp. Physiol. Psychol. 52, 132-134 (1959).
20. Rice, G. E. & Gainer, P. "Altruism" in the albino rat. J. Comp. Physiol. Psychol. 55, 123-125 (1962).
21. Masserman, J. H., Wechkin, S. & Terris, W. "Altruistic" behavior in rhesus monkeys. Am. J. Psychiatry 121, 584-585 (1964).
22. Wechkin, S., Masserman, J. H. & Terris, W. Shock to a conspecific as an aversive stimulus. Psychon. Sci. 1, 47-48 (1964).
23. Miller, R. E., Murphy, J. V. & Mirsky, I. A. Relevance of facial expression and posture as cues in communication of affect between monkeys. AMA Arch. Gen. Psychiatry 1, 480-488 (1959).
24. Yerkes, R. M. Almost Human (Century, 1925).
25. Ladygina-Kohts, N. N. Infant Chimpanzee and Human Child (ed. de Waal, F. B. M.) (Oxford Univ. Press, 2001)
26. de Waal, F. B. M. & van Roosmalen, A. Reconciliation and consolation among chimpanzees. Behav. Ecol. Sociobiol. 5, 55-66 (1979).
27. Zahn-Waxler, C., Radke-Yarrow, M., Wagner, E. & Chapman, M. Development of concern for others. Dev. Psychol. 28, 126-136 (1992).
28. Liddle, M. J. E., Bradley, B. S. & Mcgrath, A. Baby empathy: Infant distress and peer prosocial responses. Infant Ment. Health J. 36, 446-458 (2015).
29. Roth-Hanania, R., Davidov, M. & Zahn-Waxler, C. Empathy development from 8 to 16 months: Early signs of concern for others. Infant Behav. Dev. 34, 447-458 (2011).
30. Dimberg, U., Thunberg, M. & Elmehed, K. Unconscious facial reactions to emotional facial expressions. Psychol. Sci. 11, 86-89 (2000).
31. Mancini, G., Ferrari, P. F. & Palagi, E. Rapid facial mimicry in geladas. Sci. Rep. 3, 1527 (2013).
32. Ross, M. D., Menzler, S. & Zimmermann, E. Rapid facial mimicry in orangutan play. Biol. Lett. 4, 27-30 (2008).
33. Dimberg, U., Andréasson, P. & Thunberg, M. Emotional empathy and facial reactions to facial expressions. J. Psychophysiol. 25, 26-31 (2011).
34. Campbell, M. W. & de Waal, F. B. M. Ingroup-outgroup bias in contagious yawning by chimpanzees supports link to empathy. PLoS ONE 6, e18283 (2011).
35. Norscia, I. & Palagi, E. Yawn contagion and empathy in Homo sapiens. PLoS ONE 6, e28472 (2011).
36. Romero, T., Konno, A. & Hasegawa, T. Familiarity bias and physiological responses in contagious yawning by dogs support link to empathy. PLoS ONE 8, e71365 (2013).
37. Gallup, A. C., Swartwood, L., Militello, J. & Sackett, S. Experimental evidence of contagious yawning in budgerigars (Melopsittacus undulatus). Anim. Cogn. 18, 1051-1058 (2015).
38. Silva, K., Bessa, J. & de Sousa, L. Auditory contagious yawning in domestic dogs (Canis familiaris): First evidence for social modulation. Anim. Cogn. 15, 721-724 (2012).
39. Visalberghi, E. & Fragaszy, D. M. in 'Language' and Intelligence in Monkeys and Apes: Comparative Developmental Perspectives (eds Parker, S. T. & Gibson, K. R.) 247-273 (Cambridge Univ. Press, 1990).
40. Ferrari, P. F. et al. Neonatal imitation in rhesus macaques. PLoS Biol. 4, e302 (2006).
41. Paukner, A., Suomi, S. J., Visalberghi, E. & Ferrari, P. F. Capuchin monkeys display affiliation toward humans who imitate them. Science 325, 880-883 (2009).
42. Perry, S. et al. Social conventions in wild white-faced capuchin monkeys: Evidence for traditions in a neotropical primate. Curr. Anthropol. 44, 241-268 (2003).
43. Dindo, M., Whiten, A. & de Waal, F. B. M. In-group conformity sustains different foraging traditions in capuchin monkeys (Cebus apella). PLoS ONE 4, e7858 (2009).
44. Horner, V. & Whiten, A. Causal knowledge and imitation/emulation switching in chimpanzees (Pan troglodytes) and children (Homo sapiens). Anim. Cogn. 8, 164-181 (2005).
45. Fuhrmann, D., Ravignani, A., Marshall-Pescini, S. & Whiten, A. Synchrony and motor mimicking in chimpanzee observational learning. Sci. Rep. 4, 5283 (2014).
46. Hopper, L. M., Lambeth, S. P., Schapiro, S. J. & Whiten, A. Observational learning in chimpanzees and children studied through 'ghost' conditions. Proc. R. Soc. B Biol. Sci. 275, 835-840 (2008).
47. Langford, D. J. et al. Social modulation of pain as evidence for empathy in mice. Science 312, 1967-1970 (2006).
48. Langford, D. J. et al. Social approach to pain in laboratory mice. Soc. Neurosci. 5, 163-170 (2010).
49. Martin, L. J. et al. Reducing social stress elicits emotional contagion of pain in mouse and human strangers. Curr. Biol. 25, 326-332 (2015).
50. Burkett, J. et al. Oxytocin-dependent consolation behavior in rodents. Science 351, 375-378 (2016).
51. Buchanan, T. W., Bagley, S. L., Stansfield, R. B. & Preston, S. D. The empathic, physiological resonance of stress. Soc. Neurosci. 7, 191-201 (2012).
52. Buchanan, T. W. & Preston, S. D. Stress leads to prosocial action in immediate need situations. Front. Behav. Neurosci. http://dx.doi.org/10.3389/ fnbeh.2014.00005 (2014).
53. Clay, Z. & de Waal, F. B. M. Development of socio-emotional competence in bonobos. Proc. Natl Acad. Sci. USA 110, 18121-18126 (2013).
54. Fries, A. B. W. & Pollak, S. D. Emotion understanding in postinstitutionalized Eastern European children. Dev. Psychopathol. 16, 355-369 (2004).
55. Kagan, J. Human morality is distinctive. J. Conscious. Stud. 7, 46-48 (2000).
56. Fehr, E. & Fischbacher, U. The nature of human altruism. Nature 425, 785-791 (2003).
57. Bartal, I. B.-A., Decety, J. & Mason, P. Empathy and pro-social behavior in rats. Science 334, 1427-1430 (2011).
58. Sato, N., Tan, L., Tate, K. & Okada, M. Rats demonstrate helping behavior toward a soaked conspecific. Anim. Cogn. 18, 1039-1047 (2015).
59. Romero, T., Castellanos, M. A. & de Waal, F. B. M. Consolation as possible expression of sympathetic concern among chimpanzees. Proc. Natl Acad. Sci. USA 107, 12110-12115 (2010).
60. Clay, Z. & de Waal, F. B. M. Bonobos respond to distress in others: Consolation across the age spectrum. PLoS ONE 8, e55206 (2013).
61. Palagi, E., Dall'Olio, S., Demuru, E. & Stanyon, R. Exploring the evolutionary foundations of empathy: Consolation in monkeys. Evol. Hum. Behav. 35, 341-349 (2014).
62. Cools, A. K., Van Hout, A. J. M. & Nelissen, M. H. Canine reconciliation and third-party-initiated postconflict affiliation: Do peacemaking social mechanisms in dogs rival those of higher primates?. Ethology 114, 53-63 (2008).
63. Plotnik, J. M. & de Waal, F. B. M. Asian elephants (Elephas maximus) reassure others in distress. PeerJ 2, e278 (2014).
64. Seed, A. M., Clayton, N. S. & Emery, N. J. Postconflict third-party affiliation in rooks, Corvus frugilegus. Curr. Biol. 17, 152-158 (2007).
65. Fraser, O. N., Stahl, D. & Aureli, F. Stress reduction through consolation in chimpanzees. Proc. Natl Acad. Sci. USA 105, 8557-8562 (2008).
66. Aureli, F., Preston, S. D. & de Waal, F. B. M. Heart rate responses to social interactions in free-moving rhesus macaques (Macaca mulatta): A pilot study. J. Comp. Psychol. 113, 59-65 (1999).
67. Ben-Ami Bartal, I. et al. Anxiolytic treatment impairs helping behavior in rats. Front. Psychol. 7, 850 (2016).
68. Warneken, F., Hare, B., Melis, A. P., Hanus, D. & Tomasello, M. Spontaneous altruism by chimpanzees and young children. PLoS Biol. 5, e184 (2007).
69. Warneken, F. & Tomasello, M. Extrinsic rewards undermine altruistic tendencies in 20-month-olds. Motiv. Sci. 1, 43-48 (2014).
70. Andreoni, J. Giving with impure altruism: Applications to charity and Ricardian equivalence. J. Polit. Econ. 97, 1447-1458 (1989).
71. Wager, T. D. et al. Pain in the ACC?. Proc. Natl Acad. Sci. USA 113, E2474-E2475 (2016).
72. Ballesta, S. & Duhamel, J.-R. Rudimentary empathy in macaques' social decision-making. Proc. Natl Acad. Sci. USA 112, 15516-15521 (2015).
73. Christov-Moore, L. & Iacoboni, M. Self-other resonance, its control and prosocial inclinations: Brain-behavior relationships. Hum. Brain Mapp. 37, 1544-1558 (2016).
74. Hoffman, M. L. Is altruism part of human nature?. J. Pers. Soc. Psychol. 40, 121-137 (1981).
75. Nowbahari, E., Scohier, A., Durand, J.-L. & Hollis, K. L. Ants, Cataglyphis cursor, use precisely directed rescue behavior to free entrapped relatives. PLoS ONE 4, e6573 (2009).
76. Vasconcelos, M., Hollis, K., Nowbahari, E. & Kacelnik, A. Pro-sociality without empathy. Biol. Lett. 8, 910-912 (2012).
77. Wilson, E. O. A chemical releaser of alarm and digging behavior in the ant Pogonomyrmex badius (Latreille). Psyche 65, 41-51 (1958).
78. Preston, S. D. The origins of altruism in offspring care. Psychol. Bull. 139, 1305-1341 (2013).
79. MacLean, P. D. Brain evolution relating to family, play, and the separation call. Arch. Gen. Psychiatry 42, 405-417 (1985).
80. Sivaselvachandran, S., Acland, E. L., Abdallah, S. & Martin, L. J. Behavioral and mechanistic insight into rodent empathy. Neurosci. Biobehav. Rev. http:// dx.doi.org/10.1016/j.neubiorev.2016.06.007 (2016).
81. Edgar, J., Lowe, J., Paul, E. & Nicol, C. Avian maternal response to chick distress. Proc. R. Soc. B Biol. Sci. 278, 3129-3134 (2011).
82. Doody, J. S., Burghardt, G. M. & Dinets, V. Breaking the social-non-social dichotomy: A role for reptiles in vertebrate social behavior research?. Ethology 119, 95-103 (2013).
83. Donaldson, Z. R. & Young, L. J. Oxytocin, vasopressin, and the neurogenetics of sociality. Science 322, 900-904 (2008).
84. Chen, Q., Panksepp, J. B. & Lahvis, G. P. Empathy is moderated by genetic background in mice. PLoS ONE 4, e4387 (2009).
85. Dittus, W. P. & Ratnayeke, S. M. Individual and social behavioral responses to injury in wild toque macaques (Macaca sinica). Int. J. Primatol. 10, 215-234 (1989).
86. De Vignemont, F. & Singer, T. The empathic brain: How, when and why?. Trends Cogn. Sci. 10, 435-441 (2006).
87. de Waal, F. B. M. Chimpanzee Politics (John's Hopkins Univ. Press, 1998).
88. Wilson, M. L. et al. Lethal aggression in Pan is better explained by adaptive strategies than human impacts. Nature 513, 414-417 (2014).
89. Lanzetta, J. T. & Englis, B. G. Expectations of cooperation and competition and their effects on observers' vicarious emotional responses. J. Pers. Soc. Psychol. 56, 543-554 (1989).
90. Prinz, W. Perception and action planning. Eur. J. Cogn. Psychol. 9, 129-154 (1997).
91. di Pellegrino, G., Fadiga, L., Fogassi, L., Gallese, V. & Rizzolatti, G. Understanding motor events: A neurophysiological study. Exp. Brain Res. 91, 176-180 (1992).
92. Grafton, S. T., Fadiga, L., Arbib, M. A. & Rizzolatti, G. Premotor cortex activation during observation and naming of familiar tools. Neuroimage 6, 231-236 (1997).
93. Adolphs, R., Damasio, H., Tranel, D., Cooper, G. & Damasio, A. R. A role for somatosensory cortices in the visual recognition of emotion as revealed by three-dimensional lesion mapping. J. Neurosci. 20, 2683-2690 (2000).
94. 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. Neuropsychologia 44, 752-761 (2006).
95. Singer, T. & Lamm, C. The social neuroscience of empathy. Ann. NY Acad. Sci. 1156, 81-96 (2009).
96. Zaki, J. & Ochsner, K. N. The neuroscience of empathy: Progress, pitfalls and promise. Nat. Neurosci. 15, 675-680 (2012).
97. Wicker, B. et al. Both of us disgusted in my insula: The common neural basis of seeing and feeling disgust. Neuron 40, 655-664 (2003).
98. Preston, S. D. et al. The neural substrates of cognitive empathy. Soc. Neurosci. 2, 254-275 (2007).
99. Morelli, S. A. & Lieberman, M. D. The role of automaticity and attention in neural processes underlying empathy for happiness, sadness, and anxiety. Front. Hum. Neurosci. 7, 160 (2013).
100. Zaki, J., Wager, T. D., Singer, T., Keysers, C. & Gazzola, V. The anatomy of suffering: Understanding the relationship between nociceptive and empathic pain. Trends Cogn. Sci. 20, 249-259 (2016).
101. Mohr, A. H., Kross, E. & Preston, S. D. Devil in the details: Effects of depression on the prosocial response depend on timing and similarity. Adapt. Hum. Behav. Physiol. 2, 281-297 (2016).
102. Hodges, S. D., Kiel, K. J., Kramer, A. D., Veach, D. & Villanueva, B. R. Giving birth to empathy: The effects of similar experience on empathic accuracy, empathic concern, and perceived empathy. Pers. Soc. Psychol. Bull. 36, 398-409 (2010).
103. Völlm, B. A. et al. Neuronal correlates of theory of mind and empathy: A functional magnetic resonance imaging study in a nonverbal task. Neuroimage 29, 90-98 (2006).
104. Lamm, C., Nusbaum, H. C., Meltzoff, A. N. & Decety, J. What are you feeling? Using functional magnetic resonance imaging to assess the modulation of sensory and affective responses during empathy for pain. PLoS ONE 2, e1292 (2007).
105. Nummenmaa, L., Hirvonen, J., Parkkola, R. & Hietanen, J. K. Is emotional contagion special? An fMRI study on neural systems for affective and cognitive empathy. Neuroimage 43, 571-580 (2008).
106. Schnell, K., Bluschke, S., Konradt, B. & Walter, H. Functional relations of empathy and mentalizing: An fMRI study on the neural basis of cognitive empathy. Neuroimage 54, 1743-1754 (2011).
107. Blair, R. J. R. Responding to the emotions of others: Dissociating forms of empathy through the study of typical and psychiatric populations. Conscious. Cogn. 14, 698-718 (2005).
108. Derntl, B., Seidel, E.-M., Schneider, F. & Habel, U. How specific are emotional deficits? A comparison of empathic abilities in schizophrenia, bipolar and depressed patients. Schizophr. Res. 142, 58-64 (2012).
109. Samson, D., Apperly, I. A., Chiavarino, C. & Humphreys, G. W. Left temporoparietal junction is necessary for representing someone else's belief. Nat. Neurosci. 7, 499-500 (2004).
110. Saxe, R. & Wexler, A. Making sense of another mind: The role of the right temporo-parietal junction. Neuropsychologia 43, 1391-1399 (2005).
111. Adolphs, R., Baron-Cohen, S. & Tranel, D. Impaired recognition of social emotions following amygdala damage. J. Cogn. Neurosci. 14, 1264-1274 (2002).
112. Blair, R. J. R. Fine cuts of empathy and the amygdala: Dissociable deficits in psychopathy and autism. Q. J. Exp. Psychol. (Hove) 61, 157-170 (2008).
113. Marsh, A. A. Neural, cognitive, and evolutionary foundations of human altruism. Wiley Interdiscip. Rev. Cogn. Sci. 7, 59-71 (2016).
114. Singer, T. et al. Empathy for pain involves the affective but not sensory components of pain. Science 303, 1157-1162 (2004).
115. Morrison, I., Lloyd, D., di Pellegrino, G. & Roberts, N. Vicarious responses to pain in anterior cingulate cortex: Is empathy a multisensory issue?. Cogn. Affect. Behav. Neurosci. 4, 270-278 (2004).
116. 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 24, 771-779 (2005).
117. Morrison, I. & Downing, P. E. Organization of felt and seen pain responses in anterior cingulate cortex. Neuroimage 37, 642-651 (2007).
118. 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 54, 2492-2502 (2011).
119. Mischkowski, D., Crocker, J. & Way, B. M. From painkiller to empathy killer: Acetaminophen (paracetamol) reduces empathy for pain. Soc. Cogn. Affect. Neurosci. 11, 1345-1353 (2016).
120. Rütgen, M. et al. Placebo analgesia and its opioidergic regulation suggest that empathy for pain is grounded in self pain. Proc. Natl Acad. Sci. USA 112, E5638-E5646 (2015).
121. Rutgen, M., Seidel, E. M., Riecansky, I. & Lamm, C. Reduction of empathy for pain by placebo analgesia suggests functional equivalence of empathy and first-hand emotion experience. J. Neurosci. 35, 8938-8947 (2015).
122. Danziger, N., Prkachin, K. M. & Willer, J.-C. Is pain the price of empathy? The perception of others' pain in patients with congenital insensitivity to pain. Brain 129, 2494-2507 (2006).
123. Lieberman, M. D. & Eisenberger, N. I. The dorsal anterior cingulate cortex is selective for pain: Results from large-scale reverse inference. Proc. Natl Acad. Sci. USA 112, 15250-15255 (2015).
124. Krishnan, A. et al. Somatic and vicarious pain are represented by dissociable multivariate brain patterns. eLife 5, e15166 (2016).
125. Fan, Y., Duncan, N. W., de Greck, M. & Northoff, G. Is there a core neural network in empathy?. An fMRI based quantitative meta-analysis. Neurosci. Biobehav. Rev. 35, 903-911 (2011).
126. Corradi-Dell'Acqua, C., Tusche, A., Vuilleumier, P. & Singer, T. Cross-modal representations of first-hand and vicarious pain, disgust and fairness in insular and cingulate cortex. Nat. Commun. 7, 10904 (2016).
127. Danziger, N., Faillenot, I. & Peyron, R. Can we share a pain we never felt?. Neural correlates of empathy in patients with congenital insensitivity to pain. Neuron 61, 203-212 (2008).
128. Craig, A. D. How do you feel? Interoception: The sense of the physiological condition of the body. Nat. Rev. Neurosci. 3, 655-666 (2002).
129. de la Vega, A., Chang, L. J., Banich, M. T., Wager, T. D. & Yarkoni, T. Large-scale meta-analysis of human medial frontal cortex reveals tripartite functional organization. J. Neurosci. 36, 6553-6562 (2016).
130. Shackman, A. J. et al. The integration of negative affect, pain and cognitive control in the cingulate cortex. Nat. Rev. Neurosci. 12, 154-167 (2011).
131. Morrison, I., Peelen, M. V. & Downing, P. E. The sight of others' pain modulates motor processing in human cingulate cortex. Cereb. Cortex 17, 2214-2222 (2007).
132. Carr, L., Iacoboni, M., Dubeau, M. C., Mazziotta, J. C. & Lenzi, G. L. Neural mechanisms of empathy in humans: A relay from neural systems for imitation to limbic areas. Proc. Natl Acad. Sci. USA 100, 5497-5502 (2003).
133. Calder, A. J., Keane, J., Manes, F., Antoun, N. & Young, A. W. Impaired recognition and experience of disgust following brain injury. Nat. Neurosci. 3, 1077-1078 (2000).
134. Bechara, A., Damasio, H. & Damasio, A. R. Emotion, decision making and the orbitofrontal cortex. Cereb. Cortex 10, 295-307 (2000).
135. Gallese, V., Keysers, C. & Rizzolatti, G. A unifying view of the basis of social cognition. Trends Cogn. Sci. 8, 396-403 (2004).
136. Iacoboni, M. Imitation, empathy, and mirror neurons. Annu. Rev. Psychol. 60, 653-670 (2008).
137. Mukamel, R., Ekstrom, A. D., Kaplan, J., Iacoboni, M. & Fried, I. Single-neuron responses in humans during execution and observation of actions. Curr. Biol. 20, 750-756 (2010).
138. Keysers, C. & Gazzola, V. Social neuroscience: Mirror neurons recorded in humans. Curr. Biol. 20, R353-R354 (2010).
139. Shamay-Tsoory, S. G., Aharon-Peretz, J. & Perry, D. Two systems for empathy: A double dissociation between emotional and cognitive empathy in inferior frontal gyrus versus ventromedial prefrontal lesions. Brain 132, 617-627 (2009).