Mammalian empathy: behavioural manifestations and neural basis

Key Points

  • Observational and experimental studies dating back to the 1950s demonstrate that mammals spontaneously help distressed conspecifics. Research emphasizes the untrained, unrewarded nature of this behaviour, which is also biased towards familiar individuals, thus arguing against explanations that are exclusively based on associative learning or conditioning.

  • The perception–action model extends an existing motor theory on overlapping representations to emotional phenomena; it states that observers who attend to a target's state understand and 'feel into' it through personal distributed representations of the target, the state and the situation. Easily observed manifestations of this mechanism are emotional contagion and motor mimicry, which have been demonstrated in many animals. In cognitive forms of empathy, the same representations are accessed from the top-down.

  • Experiments on two common mammalian expressions of empathy — the consolation of distressed individuals and spontaneous assistance to those in need — support the crucial role of caught distress and arousal because these behaviours are suppressed by anti-anxiety medication and engage the same neuropeptide system that supports social attachment.

  • The Russian-doll model seeks to arrange forms of empathy into layers that are built on top of each other — with the layers ranging from emotional contagion to more cognitive forms of empathy — in a functionally integrated whole based on perception–action processes. Perspective-taking is well developed in some non-human species, as manifested by theory-of-mind and targeted helping.

  • One can segregate emotional and cognitive empathy (as well as felt and observed states) in the brains of observers, but all forms require some initial access to the observer's distributed, shared, personal representations of the target's state. At least in the initial phase of processing, this access helps to decode the target's state and provide subsequent processing with content and meaning, even if the shared state is not experienced, or is incomplete or inaccurate.

  • Empathic pain does not usually include the peripheral sensation of the target's injury, but it can include sensory information when the stimuli and task instructions emphasize the specific nature of the feeling at the location of the injury.

Abstract

Recent research on empathy in humans and other mammals seeks to dissociate emotional and cognitive empathy. These forms, however, remain interconnected in evolution, across species and at the level of neural mechanisms. New data have facilitated the development of empathy models such as the perception–action model (PAM) and mirror-neuron theories. According to the PAM, the emotional states of others are understood through personal, embodied representations that allow empathy and accuracy to increase based on the observer's past experiences. In this Review, we discuss the latest evidence from studies carried out across a wide range of species, including studies on yawn contagion, consolation, aid-giving and contagious physiological affect, and we summarize neuroscientific data on representations related to another's state.

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Figure 1: The Russian-doll model of the evolution of empathy.
Figure 2: Behavioural manifestations of animal empathy.
Figure 3: From affect transfer to altruism.
Figure 4: Both cognitive and affective empathy access distributed, person-specific affective representations.
Figure 5: Neural regions that participate in human empathy.

References

  1. 1

    Preston, S. D. & de Waal, F. B. M. Empathy: its ultimate and proximate bases. Behav. Brain Sci. 25, 1–71 (2002). This paper offers the first summary of empathy as a perception–action process and reviews evidence from multiple levels of analysis.

    PubMed  PubMed Central  Article  Google Scholar 

  2. 2

    Goldman, A. I. Simulating Minds: the Philosophy, Psychology, and Neuroscience of Mindreading (Oxford Univ. Press, 2006).

    Google Scholar 

  3. 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).

    Google Scholar 

  4. 4

    Zahavi, D. Simulation, projection and empathy. Conscious. Cogn. 17, 514–522 (2008).

    PubMed  PubMed Central  Article  Google Scholar 

  5. 5

    Lipps, T. Einfühlung, innere nachahmung und organenempfindungen [German]. Arch. Gesamte Psychol. 1, 465–519 (1903).

    Google Scholar 

  6. 6

    de Waal, F. B. M. Putting the altruism back into altruism: the evolution of empathy. Annu. Rev. Psychol. 59, 279–300 (2008).

    PubMed  PubMed Central  Article  Google Scholar 

  7. 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).

    Article  Google Scholar 

  8. 8

    Zahn-Waxler, C. & Radke-Yarrow, M. The origins of empathic concern. Motiv. Emot. 14, 107–130 (1990).

    Article  Google Scholar 

  9. 9

    Walter, H. Social cognitive neuroscience of empathy: concepts, circuits, and genes. Emot. Rev. 4, 9–17 (2012).

    Article  Google Scholar 

  10. 10

    Darwin, C. The Descent of Man, and Selection in Relation to Sex (Princeton Univ. Press, 1982).

    Google Scholar 

  11. 11

    Plutchik, R. in Empathy and its Development (eds Eisenberg, N. & Strayer, J.) 3–46 (Cambridge Univ. Press, 1987).

    Google Scholar 

  12. 12

    de Waal, F. B. M. Good Natured (Harvard Univ. Press, 1996).

    Google Scholar 

  13. 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).

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  14. 14

    de Waal, F. B. M. The Age of Empathy (Harmony Books, 2009).

    Google Scholar 

  15. 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).

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  16. 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).

    Article  Google Scholar 

  17. 17

    Bateson, P. & Laland, K. N. Tinbergen's four questions: an appreciation and an update. Trends Ecol. Evol. 28, 712–718 (2013).

    PubMed  PubMed Central  Article  Google Scholar 

  18. 18

    Tinbergen, N. On aims and methods of ethology [German]. Z. Tierpsychol. 20, 410–433 (1963).

    Article  Google Scholar 

  19. 19

    Church, R. M. Emotional reactions of rats to the pain of others. J. Comp. Physiol. Psychol. 52, 132–134 (1959). This is the first rodent study to analyse emotional responses to the distress of others.

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  20. 20

    Rice, G. E. & Gainer, P. “Altruism” in the albino rat. J. Comp. Physiol. Psychol. 55, 123–125 (1962).

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  21. 21

    Masserman, J. H., Wechkin, S. & Terris, W. “Altruistic” behavior in rhesus monkeys. Am. J. Psychiatry 121, 584–585 (1964).

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  22. 22

    Wechkin, S., Masserman, J. H. & Terris, W. Shock to a conspecific as an aversive stimulus. Psychon. Sci. 1, 47–48 (1964).

    Article  Google Scholar 

  23. 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).

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  24. 24

    Yerkes, R. M. Almost Human (Century, 1925).

    Google Scholar 

  25. 25

    Ladygina-Kohts, N. N. Infant Chimpanzee and Human Child (ed. de Waal, F. B. M.) (Oxford Univ. Press, 2001)

    Google Scholar 

  26. 26

    de Waal, F. B. M. & van Roosmalen, A. Reconciliation and consolation among chimpanzees. Behav. Ecol. Sociobiol. 5, 55–66 (1979). This is the first non-human animal study to define and analyse consolation behaviour.

    Article  Google Scholar 

  27. 27

    Zahn-Waxler, C., Radke-Yarrow, M., Wagner, E. & Chapman, M. Development of concern for others. Dev. Psychol. 28, 126–136 (1992). This is a pioneering study of the early development of human consolation behaviour.

    Article  Google Scholar 

  28. 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).

    PubMed  PubMed Central  Article  Google Scholar 

  29. 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).

    PubMed  PubMed Central  Article  Google Scholar 

  30. 30

    Dimberg, U., Thunberg, M. & Elmehed, K. Unconscious facial reactions to emotional facial expressions. Psychol. Sci. 11, 86–89 (2000). This study is part of a series of studies on facial mimicry that first demonstrated the spontaneous nature of human empathic reactions.

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  31. 31

    Mancini, G., Ferrari, P. F. & Palagi, E. Rapid facial mimicry in geladas. Sci. Rep. 3, 1527 (2013).

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  32. 32

    Ross, M. D., Menzler, S. & Zimmermann, E. Rapid facial mimicry in orangutan play. Biol. Lett. 4, 27–30 (2008).

    Article  Google Scholar 

  33. 33

    Dimberg, U., Andréasson, P. & Thunberg, M. Emotional empathy and facial reactions to facial expressions. J. Psychophysiol. 25, 26–31 (2011).

    Article  Google Scholar 

  34. 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).

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  35. 35

    Norscia, I. & Palagi, E. Yawn contagion and empathy in Homo sapiens. PLoS ONE 6, e28472 (2011).

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  36. 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).

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  37. 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).

    PubMed  PubMed Central  Article  Google Scholar 

  38. 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).

    PubMed  PubMed Central  Article  Google Scholar 

  39. 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).

    Google Scholar 

  40. 40

    Ferrari, P. F. et al. Neonatal imitation in rhesus macaques. PLoS Biol. 4, e302 (2006).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  41. 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).

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  42. 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).

    Article  Google Scholar 

  43. 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).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  44. 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).

    PubMed  PubMed Central  Article  Google Scholar 

  45. 45

    Fuhrmann, D., Ravignani, A., Marshall-Pescini, S. & Whiten, A. Synchrony and motor mimicking in chimpanzee observational learning. Sci. Rep. 4, 5283 (2014).

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  46. 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).

    Article  Google Scholar 

  47. 47

    Langford, D. J. et al. Social modulation of pain as evidence for empathy in mice. Science 312, 1967–1970 (2006). This paper provides compelling evidence of emotional contagion in mice and set the stage for subsequent rodent research.

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  48. 48

    Langford, D. J. et al. Social approach to pain in laboratory mice. Soc. Neurosci. 5, 163–170 (2010).

    PubMed  PubMed Central  Article  Google Scholar 

  49. 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).

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  50. 50

    Burkett, J. et al. Oxytocin-dependent consolation behavior in rodents. Science 351, 375–378 (2016).

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  51. 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). This paper provides the first demonstration that stress — at the physiological level — spreads from one stressed human participant to empathic observers.

    PubMed  PubMed Central  Article  Google Scholar 

  52. 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. 53

    Clay, Z. & de Waal, F. B. M. Development of socio-emotional competence in bonobos. Proc. Natl Acad. Sci. USA 110, 18121–18126 (2013).

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  54. 54

    Fries, A. B. W. & Pollak, S. D. Emotion understanding in postinstitutionalized Eastern European children. Dev. Psychopathol. 16, 355–369 (2004).

    PubMed  PubMed Central  Article  Google Scholar 

  55. 55

    Kagan, J. Human morality is distinctive. J. Conscious. Stud. 7, 46–48 (2000).

    Google Scholar 

  56. 56

    Fehr, E. & Fischbacher, U. The nature of human altruism. Nature 425, 785–791 (2003).

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  57. 57

    Bartal, I. B.-A., Decety, J. & Mason, P. Empathy and pro-social behavior in rats. Science 334, 1427–1430 (2011).

    CAS  Article  PubMed Central  Google Scholar 

  58. 58

    Sato, N., Tan, L., Tate, K. & Okada, M. Rats demonstrate helping behavior toward a soaked conspecific. Anim. Cogn. 18, 1039–1047 (2015).

    PubMed  PubMed Central  Article  Google Scholar 

  59. 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).

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  60. 60

    Clay, Z. & de Waal, F. B. M. Bonobos respond to distress in others: consolation across the age spectrum. PLoS ONE 8, e55206 (2013).

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  61. 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).

    Article  Google Scholar 

  62. 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).

    Article  Google Scholar 

  63. 63

    Plotnik, J. M. & de Waal, F. B. M. Asian elephants (Elephas maximus) reassure others in distress. PeerJ 2, e278 (2014).

    PubMed  PubMed Central  Article  Google Scholar 

  64. 64

    Seed, A. M., Clayton, N. S. & Emery, N. J. Postconflict third-party affiliation in rooks, Corvus frugilegus. Curr. Biol. 17, 152–158 (2007).

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  65. 65

    Fraser, O. N., Stahl, D. & Aureli, F. Stress reduction through consolation in chimpanzees. Proc. Natl Acad. Sci. USA 105, 8557–8562 (2008).

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  66. 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).

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  67. 67

    Ben-Ami Bartal, I. et al. Anxiolytic treatment impairs helping behavior in rats. Front. Psychol. 7, 850 (2016).

    PubMed  PubMed Central  Article  Google Scholar 

  68. 68

    Warneken, F., Hare, B., Melis, A. P., Hanus, D. & Tomasello, M. Spontaneous altruism by chimpanzees and young children. PLoS Biol. 5, e184 (2007).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  69. 69

    Warneken, F. & Tomasello, M. Extrinsic rewards undermine altruistic tendencies in 20-month-olds. Motiv. Sci. 1, 43–48 (2014).

    Article  Google Scholar 

  70. 70

    Andreoni, J. Giving with impure altruism: applications to charity and Ricardian equivalence. J. Polit. Econ. 97, 1447–1458 (1989).

    Article  Google Scholar 

  71. 71

    Wager, T. D. et al. Pain in the ACC? Proc. Natl Acad. Sci. USA 113, E2474–E2475 (2016).

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  72. 72

    Ballesta, S. & Duhamel, J.-R. Rudimentary empathy in macaques' social decision-making. Proc. Natl Acad. Sci. USA 112, 15516–15521 (2015).

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  73. 73

    Christov-Moore, L. & Iacoboni, M. Self–other resonance, its control and prosocial inclinations: brain–behavior relationships. Hum. Brain Mapp. 37, 1544–1558 (2016).

    PubMed  PubMed Central  Article  Google Scholar 

  74. 74

    Hoffman, M. L. Is altruism part of human nature? J. Pers. Soc. Psychol. 40, 121–137 (1981).

    Article  Google Scholar 

  75. 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).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  76. 76

    Vasconcelos, M., Hollis, K., Nowbahari, E. & Kacelnik, A. Pro-sociality without empathy. Biol. Lett. 8, 910–912 (2012).

    PubMed  PubMed Central  Article  Google Scholar 

  77. 77

    Wilson, E. O. A chemical releaser of alarm and digging behavior in the ant Pogonomyrmex badius (Latreille). Psyche 65, 41–51 (1958).

    Article  Google Scholar 

  78. 78

    Preston, S. D. The origins of altruism in offspring care. Psychol. Bull. 139, 1305–1341 (2013). This is a comprehensive review of the offspring-care perspective on how altruism and heroic rescue evolved and are encoded in the brain.

    PubMed  PubMed Central  Article  Google Scholar 

  79. 79

    MacLean, P. D. Brain evolution relating to family, play, and the separation call. Arch. Gen. Psychiatry 42, 405–417 (1985).

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  80. 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. 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).

    CAS  Article  Google Scholar 

  82. 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).

    Article  Google Scholar 

  83. 83

    Donaldson, Z. R. & Young, L. J. Oxytocin, vasopressin, and the neurogenetics of sociality. Science 322, 900–904 (2008).

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  84. 84

    Chen, Q., Panksepp, J. B. & Lahvis, G. P. Empathy is moderated by genetic background in mice. PLoS ONE 4, e4387 (2009).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  85. 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).

    Article  Google Scholar 

  86. 86

    De Vignemont, F. & Singer, T. The empathic brain: how, when and why? Trends Cogn. Sci. 10, 435–441 (2006).

    PubMed  PubMed Central  Article  Google Scholar 

  87. 87

    de Waal, F. B. M. Chimpanzee Politics (John's Hopkins Univ. Press, 1998).

    Google Scholar 

  88. 88

    Wilson, M. L. et al. Lethal aggression in Pan is better explained by adaptive strategies than human impacts. Nature 513, 414–417 (2014).

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  89. 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).

    Article  Google Scholar 

  90. 90

    Prinz, W. Perception and action planning. Eur. J. Cogn. Psychol. 9, 129–154 (1997).

    Article  Google Scholar 

  91. 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). This study reports the discovery of mirror neurons, which are a subclass of cells that activate similarly when a macaque or the experimenter performs a goal-directed motor action.

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  92. 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).

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  93. 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). This study offers early support for the PAM by showing that damage to the somatosensory cortex (where the body is represented) impairs an individual's ability to recognize the facial emotions of others.

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  94. 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).

    PubMed  PubMed Central  Article  Google Scholar 

  95. 95

    Singer, T. & Lamm, C. The social neuroscience of empathy. Ann. NY Acad. Sci. 1156, 81–96 (2009).

    PubMed  PubMed Central  Article  Google Scholar 

  96. 96

    Zaki, J. & Ochsner, K. N. The neuroscience of empathy: progress, pitfalls and promise. Nat. Neurosci. 15, 675–680 (2012).

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  97. 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).

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  98. 98

    Preston, S. D. et al. The neural substrates of cognitive empathy. Soc. Neurosci. 2, 254–275 (2007).

    PubMed  PubMed Central  Article  Google Scholar 

  99. 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).

    PubMed  PubMed Central  Article  Google Scholar 

  100. 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).

    PubMed  PubMed Central  Article  Google Scholar 

  101. 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).

    Article  Google Scholar 

  102. 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).

    PubMed  PubMed Central  Article  Google Scholar 

  103. 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).

    PubMed  PubMed Central  Article  Google Scholar 

  104. 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).

    PubMed  PubMed Central  Article  Google Scholar 

  105. 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).

    PubMed  PubMed Central  Article  Google Scholar 

  106. 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).

    PubMed  PubMed Central  Article  Google Scholar 

  107. 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).

    CAS  Article  PubMed  Google Scholar 

  108. 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).

    PubMed  PubMed Central  Article  Google Scholar 

  109. 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).

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  110. 110

    Saxe, R. & Wexler, A. Making sense of another mind: the role of the right temporo-parietal junction. Neuropsychologia 43, 1391–1399 (2005).

    PubMed  PubMed Central  Article  Google Scholar 

  111. 111

    Adolphs, R., Baron-Cohen, S. & Tranel, D. Impaired recognition of social emotions following amygdala damage. J. Cogn. Neurosci. 14, 1264–1274 (2002).

    PubMed  PubMed Central  Article  Google Scholar 

  112. 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).

    CAS  Article  Google Scholar 

  113. 113

    Marsh, A. A. Neural, cognitive, and evolutionary foundations of human altruism. Wiley Interdiscip. Rev. Cogn. Sci. 7, 59–71 (2016).

    PubMed  PubMed Central  Article  Google Scholar 

  114. 114

    Singer, T. et al. Empathy for pain involves the affective but not sensory components of pain. Science 303, 1157–1162 (2004).

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  115. 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).

    PubMed  PubMed Central  Article  Google Scholar 

  116. 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).

    PubMed  PubMed Central  Article  Google Scholar 

  117. 117

    Morrison, I. & Downing, P. E. Organization of felt and seen pain responses in anterior cingulate cortex. Neuroimage 37, 642–651 (2007).

    PubMed  PubMed Central  Article  Google Scholar 

  118. 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).

    PubMed  PubMed Central  Article  Google Scholar 

  119. 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).

    PubMed  PubMed Central  Article  Google Scholar 

  120. 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).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  121. 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).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  122. 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).

    PubMed  PubMed Central  Article  Google Scholar 

  123. 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).

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  124. 124

    Krishnan, A. et al. Somatic and vicarious pain are represented by dissociable multivariate brain patterns. eLife 5, e15166 (2016).

    PubMed  PubMed Central  Article  Google Scholar 

  125. 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). This paper offers a meta-analysis of the role of the dACC–aMCC–SMA and the bilateral anterior insula across empathy tasks, demonstrating a domain-general role with similar recruitment for self and other experiences.

    PubMed  PubMed Central  Article  Google Scholar 

  126. 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). In this study, the anterior insula and aMCC are engaged across pain, disgust and unfairness, showing that these regions are not pain specific but participate in various negative self and other experiences.

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  127. 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).

    Article  CAS  Google Scholar 

  128. 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).

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  129. 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).

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  130. 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).

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  131. 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).

    PubMed  PubMed Central  Article  Google Scholar 

  132. 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).

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  133. 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).

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  134. 134

    Bechara, A., Damasio, H. & Damasio, A. R. Emotion, decision making and the orbitofrontal cortex. Cereb. Cortex 10, 295–307 (2000). This paper shows how the orbitofrontal cortex informs decisions from one's own simulated affective state, allowing humans to imagine how another person feels and how they would feel as a result of possible decision outcomes.

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  135. 135

    Gallese, V., Keysers, C. & Rizzolatti, G. A unifying view of the basis of social cognition. Trends Cogn. Sci. 8, 396–403 (2004).

    PubMed  PubMed Central  Article  Google Scholar 

  136. 136

    Iacoboni, M. Imitation, empathy, and mirror neurons. Annu. Rev. Psychol. 60, 653–670 (2008).

    Article  Google Scholar 

  137. 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).

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  138. 138

    Keysers, C. & Gazzola, V. Social neuroscience: mirror neurons recorded in humans. Curr. Biol. 20, R353–R354 (2010).

    PubMed  PubMed Central  CAS  Article  Google Scholar 

  139. 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).

    PubMed  PubMed Central  Article  Google Scholar 

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Acknowledgements

The authors thank their sources of funding during the preparation of this manuscript, including support for the Living Links Center from Emory College, Georgia, USA (to F.B.M.d.W.) and a grant from Rackham Graduate School at the University of Michigan, USA (to S.D.P.). The authors also thank Y. Lei for assistance with manuscript preparation, and L. Bickel for creating the original brain figures.

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Glossary

Empathy

Any process that emerges from the fact that observers understand others' states by activating personal, neural and mental representations of that state, including the capacity to be affected by and share the emotional state of another; assess the reasons for the other's state; and identify with the other, adopting his or her perspective.

Theory-of-mind

The ability to attribute mental states to others, such as knowledge, intentions and beliefs.

Affective empathy

Also known as emotional empathy. Empathy that is directly affected by the emotional state of another by matching or 'feeling with' it, as a result of perceiving this state.

Cognitive empathy

Empathy derived from a top-down process in which the observer imagines how the target feels, even if the target is not present or their feelings cannot be directly observed.

Empathic perspective-taking

The capacity to take another's affective perspective: for example, understanding their specific situation and needs, separate from one's own, which still requires access to personal representations of the other's state.

False-belief task

A crucial theory-of-mind task that determines whether an observer knows what another knows, even if this knowledge is incongruent with the observer's own.

Targeted helping

Assistance and care based on a cognitive appreciation of the other's specific need or circumstances.

Tinbergian framework

A series of 'why' questions that we may ask about any observed behaviour, as proposed by Niko Tinbergen. The questions concern different levels of causation: for example, why did a behaviour evolve (what are its benefits), why does the behaviour occur (what caused it) and what is the behaviour's phylogenetic origin?

Emotional contagion

Emotional state matching between a target and an observer.

Consolation behaviour

Reassurance behaviour directed at a distressed party, such as a victim of aggression (also see the definition of 'empathic concern').

Empathic concern

Also known as sympathetic concern. Concern about another's state, and attempts to ameliorate this state (also see the definition of 'consolation behaviour').

Perception–action mechanism

Spontaneous activation of an individual's own personal representations for a target, their state and their situation when perceiving the target's state.

Emotion self-regulation

Control over one's own emotions to promote adaptive responding, including response delay, recovery from upsets and selective attention.

Directed altruism

Helping or comforting behaviour directed at an individual in need, pain or distress.

Convergent evolution

A process in which unrelated species independently evolve similar traits or capacities in response to similar environmental pressures.

Ideomotor action

An action that is covertly mimicked when another's action or movement of an object is being observed, such as moving your arm when you watch someone bowl or tilting your head in synchrony with a pendulum swing.

Motor imitation

Re-enactment by the observer of a target's motor movements or facial expressions.

Affordances

Motor or action properties of objects that are activated by their percepts, which are intrinsic to the mental representation of the object.

Simon effect

A behavioural effect in which motor actions are facilitated when they are consistent with the spatial location of the stimulus, and slowed when they are inconsistent or opposing the location.

Bottom-up

Describes a neural and mental process that is stimulus-driven on the basis of directly observed information without requiring explicit cognitive processes or capacities. Empathy arises from bottom-up processes that are shared across species such as motor mimicry, emotional contagion and state matching.

Top-down

Describes a neural and mental process that requires a conscious, cognitive evaluation to take into account information that is not directly observable, such as taking another's perspective or reasoning about their state on the basis of conceptual knowledge. These processes participate in more advanced forms of empathy that are more sophisticated in humans and with age, but they are not required to simply understand how someone feels.

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de Waal, F., Preston, S. Mammalian empathy: behavioural manifestations and neural basis. Nat Rev Neurosci 18, 498–509 (2017). https://doi.org/10.1038/nrn.2017.72

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