Empathy as a driver of prosocial behaviour: Highly conserved neurobehavioural mechanisms across species

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 371, Issue 1686, 2016, Pages

  Decety, Jean ^a   Bartal, Inbal Ben Ami ^b   Uzefovsky, Florina ^c   Knafo Noam, Ariel ^d  

^a UNIVERSITY OF CHICAGO   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^d HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

Biological mechanisms; Caring; Development; Empathy; Evolution; Prosocial behaviour

Indexed keywords

DEVELOPMENTAL BIOLOGY; EVOLUTIONARY BIOLOGY; GROUP BEHAVIOR; KINSHIP; NEUROLOGY; PARENTAL CARE; PERCEPTION; PSYCHOLOGY;

ANIMALIA;

ANIMAL; ANIMAL BEHAVIOR; BRAIN; DEVELOPMENTAL PSYCHOLOGY; EMPATHY; EVOLUTION; HUMAN; MENTAL STRESS; PHYSIOLOGY; SOCIAL BEHAVIOR;

ANIMALS; BEHAVIOR, ANIMAL; BIOLOGICAL EVOLUTION; BRAIN; EMPATHY; HUMANS; PSYCHOLOGY, DEVELOPMENTAL; SOCIAL BEHAVIOR; STRESS, PSYCHOLOGICAL;

EID: 84951325669     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2015.0077     Document Type: Review

References (137)

1. Ohtsuki H, Hauert C, Lieberman E, Nowak MA. 2006 A simple rule for the evolution of cooperation on graphs and social networks. Nature 441, 502–505. (doi:10.1038/nature04605)
2. Decety J, Cowell JM. 2015 Empathy, justice, and moral behavior. AJOB Neurosci. 6, 3–14. (doi:10.1080/21507740.2015.1047055)
3. Prinz J. 2011 Is empathy necessary for empathy? In Empathy: philosophical and psychological perspectives (eds A Coplan, P Goldie), pp. 211–229. New York, NY: Oxford University Press.
4. Vasconcelos M, Hollis K, Nowbahari E, Kacelnik A. 2012 Pro-sociality without empathy. Biol. Lett. 8, 910–912. (doi:10.1098/rsbl.2012.0554)
5. Batson CD, Fultz J, Schoenrade PA. 1987 Distress and empathy: two qualitatively distinct vicarious emotions with different motivational consequences. J. Pers. 55, 19–39. (doi:10.1111/j.1467-6494.1987.tb00426.x)
6. Coplan A. 2011 Understanding empathy. In Empathy: philosophical and psychological perspectives (eds A Coplan, P Goldie), pp. 3–18. New York, NY: Oxford University Press.
7. Cuff BMP, Brown SJ, Taylor L, Howat DJ. 2014 Empathy: a review of the concept. Emotion Rev. 7, 1–10. (doi:10.1177/1754073914558466)
8. Decety J, Cowell JM. 2014 Friends or foes: is empathy necessary for moral behaviour? Perspect. Psychol. Sci. 9, 525–537. (doi:10.1177/1745691614545130)
9. Decety J. 2014 The neural pathways, development and functions of empathy. Curr. Opin. Behav. Sci. 3, 1–6. (doi:10.1016/j.cobeha.2014.12.001)
10. Davidov M, Zahn-Waxler C, Roth-Hanania R, Knafo A. 2013 Concern for others in the first year of life: theory, evidence, and avenues for research. Child Dev. Perspect. 7, 126–131. (doi:10.1111/cdep.12028)
11. Gibson JJ. 1979 The ecological approach to visual perception. New York, NY: Houghton Mifflin.
12. Rochat P. 1995 Early objectification of the self. In The self in infancy (ed. P Rochat), pp. 53–71. Amsterdam, The Netherlands: Elsevier Science.
13. Decety J. 2011 The neuroevolution of empathy. Ann. NY Acad. Sci. 1231, 35–45. (doi:10.1111/j.1749-6632.2011.06027.x)
14. Nowak MA. 2006 Five rules for the evolution of cooperation. Science 314, 1560–1563. (doi:10.1126/science.1133755)
15. Plutchick R. 1987 Evolutionary bases of empathy. In Empathy and its development (eds N Eisenberg, J Strayer), pp. 38–46. New York, NY: Cambridge University Press.
16. Dulac C, O’Connell LA, Wu Z. 2014 Neural control of maternal and paternal behaviors. Science 345, 765–770. (doi:10.1126/science.1253291)
17. Bell DC, Richard AJ. 2000 Caregiving: the forgotten element in attachment. Psychol. Inq. 11, 69–83. (doi:10.1207/S15327965PLI1102_01)
18. Panksepp J. 1998 Affective neuroscience: the foundations of human and animal emotions. London, UK: Oxford University Press.
19. Tucker DM, Luu P, Derryberry D. 2005 Love hurts: the evolution of empathic concern through the encephalization of nociceptive capacity. Dev. Psychopathol. 17, 699–713. (doi:10.1017/S0954579405050339)
20. Wascher CAF, Scheiber IBR, Kotrschal K. 2008 Heart rate modulation in bystanding geese watching social and non-social events. Proc. R. Soc. B 275, 1653–1659. (doi:10.1098/rspb.2008.0146)
21. Seed AM, Clayton NS, Emery NJ. 2007 Postconflict third-party affiliation in rooks, Corvus frugilegus. Curr. Biol. 17, 152–158. (doi:10.1016/j.cub.2006.11.025)
22. Fraser ON, Bugnyar T. 2010 Do ravens show consolation? Responses to distressed others. PLoS ONE 5, e10605. (doi:10.1371/journal.pone.0010605)
23. Van Kesteren RE, Smit AB, Dirks RW, de With ND, Geraerts WP, Joosse J. 1992 Evolution of the vasopressin/oxytocin superfamily: characterization of a cDNA encoding a vasopressin-related precursor, preproconopressin, from the mollusc Lymnaea stagnalis. Proc. Natl Acad. Sci. USA 89, 4593–4597. (doi:10.1073/pnas.89.10.4593)
24. Lim MM, Young LJ. 2006 Neuropeptidergic regulation of affiliative behavior and social bonding in animals. Horm. Behav. 50, 506–517. (doi:10.1016/j.yhbeh.2006.06.028)
25. Klatt JD, Goodson JL. 2013 Oxytocin-like receptors mediate pair bonding in a socially monogamous songbird. Proc. R. Soc. B 280, 20122396. (doi:10.1098/rspb.2012.2396)
26. Young LJ, Wang Z. 2004 The neurobiology of pair bonding. Nat. Neurosci. 7, 1048–1054. (doi:10.1038/nn1327)
27. Anacker AMJ, Beery AK. 2013 Life in groups: the roles of oxytocin in mammalian sociality. Front. Behav. Neurosci. 7, 185. (doi:10.3389/fnbeh.2013.00185)
28. Crespi BJ. 2015 Oxytocin, testosterone, and human social cognition. Biol. Rev. (doi:10.1111/brv.12175)
29. Domes G, Heinrichs M, Michel A, Berger C, Herpertz SC. 2007 Oxytocin improves ‘mind-reading’ in humans. Biol. Psychiatry 61, 731–733. (doi:10.1016/j.biopsych.2006.07.015)
30. Kosfeld M, Heinrichs M, Zak PJ, Fischbacher U, Fehr E. 2005 Oxytocin increases trust in humans. Nature 435, 673–676. (doi:10.1038/nature03701)
31. Zak PJ, Stanton AA, Ahmadi S. 2007 Oxytocin increases generosity in humans. PLoS ONE 2, e1128. (doi:10.1371/journal.pone.0001128)
32. De Dreu CKW, Greer LL, Handgraaf MJJ, Shalvi S, Van Kleef GA, Baas M, Ten Velden FS, Van Dijk E, Feith SWW. 2010 The neuropeptide oxytocin regulates parochial altruism in intergroup conflict among humans. Science 328, 1408–1411. (doi:10.1126/science.1189047)
33. Rodrigues SM, Saslow LR, Garcia N, John OP, Keltner D. 2009 Oxytocin receptor genetic variation relates to empathy and stress reactivity in humans. Proc. Natl Acad. Sci. USA 106, 21437–21441. (doi:10.1073/pnas.0909579106)
34. Smith KE, Porges EC, Norman GJ, Connelly JJ, Decety J. 2014 Oxytocin receptor gene variation predicts empathic concern and autonomic arousal while perceiving harm to others. Soc. Neurosci. 9, 1–9. (doi:10.1080/17470919.2013.863223)
35. Uzefovsky F, Shalev I, Israel S, Edelman S, Raz Y, Mankuta D, Knafo-Noam A, Ebstein RP. 2015 Oxytocin receptor and vasopressin receptor 1a genes are respectively associated with emotional and cognitive empathy. Horm. Behav. 67, 60–65. (doi:10.1016/j.yhbeh.2014.11.007)
36. Israel S et al. 2009 The oxytocin receptor (OXTR) contributes to prosocial fund allocations in the dictator game and the social value orientations task. PLoS ONE 4, e5535. (doi:10.1371/journal.pone.0005535)
37. Shamay-Tsoory SG, Abu-Akel A, Palgi S, Sulieman R, Fischer-Shofty M, Levkovitz Y, Decety J. 2013 Giving peace a chance: oxytocin increases empathy to pain in the context of the Israeli-Palestinian conflict. Psychoneuroendocrinology 38, 3139–3144. (doi:10.1016/j.psyneuen.2013.09.015)
38. Edgar JL, Lowe JC, Paul ES, Nicol CJ. 2011 Avian maternal response to chick distress. Proc. R. Soc. B 278, 3129–3134. (doi:10.1098/rspb.2010.2701)
39. Church RM. 1959 Emotional reactions of rats to the pain of others. J. Comp. Physiol. Psychol. 52, 132–134. (doi:10.1037/h0043531)
40. Knapska E, Mikosz M, Werka T, Maren S. 2010 Social modulation of learning in rats. Learn. Mem. 17, 35–42. (doi:10.1101/lm.1670910)
41. Bruchey AK, Jones CE, Monfils M-H. 2010 Fear conditioning by-proxy: social transmission of fear during memory retrieval. Behav. Brain Res. 214, 80–84. (doi:10.1016/j.bbr.2010.04.047)
42. Langford DJ, Crager SE, Shehzad Z, Smith SB, Sotocinal SG, Levenstadt JS, Chanda ML, Levitin DJ, Mogil JS. 2006 Social modulation of pain as evidence for empathy in mice. Science 312, 1967–1970. (doi:10.1126/science.1128322)
43. Jeon D, Kim S, Chetana M, Jo D, Ruley HE, Lin S-Y, Rabah D, Kinet J-P, Shin H-S. 2010 Observational fear learning involves affective pain system and Cav1.2 Ca2þ channels in ACC. Nat. Neurosci. 13, 482–488. (doi:10.1038/nn.2504)
44. Langford DJ et al. 2010 Social approach to pain in laboratory mice. Soc. Neurosci. 5, 163–170. (doi:10.1080/17470910903216609)
45. Hostinar CE, Gunnar MR. 2015 Social support can buffer against stress and shape brain activity. AJOB Neurosci. 6, 34–42. (doi:10.1080/21507740.2015.1047054)
46. Norman GJ, Karelina K, Morris J, Zhang N, Cochran M, DeVries A. 2010 Social interaction prevents the development of depressivelike behavior post nerve injury in mice: a potential role for oxytocin. Psychosom. Med. 72, 519–526. (doi:10.1097/PSY.0b013e3181de8678)
47. Cheng Y, Chen C, Decety J. 2014 An EEG/ERP investigation of the development of empathy in early and middle childhood. Dev. Cogn. Neurosci. 10, 160–169. (doi:10.1016/j.dcn.2014.08.012)
48. Decety J, Michalska KJ. 2010 Neurodevelopmental changes in the circuits underlying empathy and sympathy from childhood to adulthood. Dev. Sci. 13, 886–899. (doi:10.1111/j.1467-7687.2009.00940.x)
49. Decety J, Michalska KJ, Kinzler KD. 2012 The contribution of emotion and cognition to moral sensitivity: a neurodevelopmental study. Cereb. Cortex 22, 209–220. (doi:10.1093/cercor/bhr111)
50. Jackson PL, Meltzoff AN, Decety J. 2006 To what extent do we share the pain of others? Insight from the neural bases of pain empathy. Pain 125, 5–9. (doi:10.1016/j.pain.2006.09.013)
51. Jackson PL, Meltzoff AN, Decety J. 2005 How do we perceive the pain of others? A window into the neural processes involved in empathy. Neuroimage 24, 771–779. (doi:10.1016/j.neuroimage.2004.09.006)
52. Lamm C, Nusbaum HC, Meltzoff AN, Decety J. 2007 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. (doi:10.1371/journal.pone.0001292)
53. Lamm C, Decety J, Singer T. 2011 Meta-analytic evidence for common and distinct neural networks associated with directly experienced pain and empathy for pain. Neuroimage 54, 2492–2502. (doi:10.1016/j.neuroimage.2010.10.014)
54. Decety J. 2011 Dissecting the neural mechanisms mediating empathy. Emot. Rev. 3, 92–108. (doi:10.1177/1754073910374662)
55. Decety J, Cowell JM. 2014 The complex relation between morality and empathy. Trends Cogn. Sci. 18, 337–339. (doi:10.1016/j.tics.2014.04.008)
56. Parsons CE, Stark EA, Young KS, Stein A, Kringelbach ML. 2013 Understanding the human parental brain: a critical role of the orbitofrontal cortex. Soc. Neurosci. 8, 525–543. (doi:10.1080/17470919.2013.842610)
57. Ruff CC, Fehr E. 2014 The neurobiology of rewards and values in social decision making. Nat. Rev. Neurosci. 15, 549–562. (doi:10.1038/nrn3776)
58. FeldmanHall O, Dalgleish T, Evans D, Mobbs D. 2015 Empathic concern drives costly altruism. Neuroimage 105, 347–356. (doi:10.1016/j.neuroimage.2014.10.043)
59. Blair R. 1995 A cognitive developmental approach to morality: investigating the psychopath. Cognition 57, 1–29. (doi:10.1016/0010-0277(95)00676-P)
60. Rhee SH et al. 2013 Early concern and disregard for others as predictors of antisocial behavior. J. Child Psychol. Psychiatry Allied Discip. 54, 157–166. (doi:10.1111/j.1469-7610.2012.02574.x)
61. Cheng Y, Hung A, Decety J. 2012 Dissociation between affective sharing and emotion understanding in juvenile psychopaths. Dev. Psychopathol. 24, 623–636. (doi:10.1017/S095457941200020X)
62. Lockwood PL, Sebastian CL, McCrory EJ, Hyde ZH, Gu X, De Brito SA, Viding E. 2013 Association of callous traits with reduced neural response to others’ pain in children with conduct problems. Curr. Biol. 23, 901–905. (doi:10.1016/j.cub.2013.04.018)
63. Marsh AA, Finger EC, Fowler KA, Adalio CJ, Jurkowitz ITN, Schechter JC, Pine DS, Decety J, Blair RJR. 2013 Empathic responsiveness in amygdala and anterior cingulate cortex in youths with psychopathic traits. J. Child Psychol. Psychiatry Allied Discip. 54, 900–910. (doi:10.1111/jcpp.12063)
64. Anderson NE, Kiehl KA. 2012 The psychopath magnetized: insights from brain imaging. Trends Cogn. Sci. 16, 52–60. (doi:10.1016/j.tics.2011.11.008)
65. Hare RD, Neumann CS. 2008 Psychopathy as a clinical and empirical construct. Annu. Rev. Clin. Psychol. 4, 217–246. (doi:10.1146/annurev.clinpsy.3.022806.091452)
66. Decety J, Chen C, Harenski C, Kiehl KA. 2013 An fMRI study of affective perspective taking in individuals with psychopathy: imagining another in pain does not evoke empathy. Front. Hum. Neurosci. 7, 489. (doi:10.3389/fnhum.2013.00489)
67. Decety J, Skelly LR, Kiehl KA. 2013 Brain response to empathy-eliciting scenarios involving pain in incarcerated individuals with psychopathy. JAMA Psychiatry 70, 638–645. (doi:10.1001/jamapsychiatry.2013.27)
68. Kiehl KA. 2014 The psychopath whisperer: inside the minds of those without a conscience. New York, NY: Crown Publishers.
69. Wolf RC, Pujara MS, Motzkin JC, Newman JP, Kiehl KA, Decety J, Kosson DS, Koenigs M. 2015 Interpersonal traits of psychopathy linked to reduced integrity of the uncinate fasciculus. Hum. Brain Mapp. 36, 4202–4209. (doi:10.1002/hbm.22911)
70. Yoder KJ, Porges EC, Decety J. 2014 Amygdala subnuclei connectivity in response to violence reveals unique influences of individual differences in psychopathic traits in a nonforensic sample. Hum. Brain Mapp. 36, 1417–1428. (doi:10.1002/hbm.22712)
71. Barnett M, Thompson S. 2001 The role of perspective taking and empathy in children’s machiavellianism, prosocial behavior, and motive for helping. J. Genet. Psychol. 146, 295–305. (doi:10.1080/00221325.1985.9914459)
72. Cronin KA. 2012 Prosocial behaviour in animals: the influence of social relationships, communication and rewards. Anim. Behav. 84, 1085–1093. (doi:10.1016/j.anbehav.2012.08.009)
73. Nowbahari E, Scohier A, Durand J-L, Hollis KL. 2009 Ants, Cataglyphis cursor, use precisely directed rescue behavior to free entrapped relatives. PLoS ONE 4, e6573. (doi:10.1371/journal.pone.0006573)
74. De Waal FBM. 2008 Putting the altruism back into altruism: the evolution of empathy. Annu. Rev. Psychol. 59, 279–300. (doi:10.1146/annurev.psych.59.103006.093625)
75. Dugatkin L. 1997 Cooperation among animals: an evolutionary perspective. New York, NY: Oxford University Press.
76. West SA, Gardner A, Griffin AS. 2006 Altruism. Curr. Biol. 16, R482–R483. (doi:10.1016/j.cub.2006.06.014)
77. Cowell JM, Decety J. 2015 The neuroscience of implicit moral evaluation and its relation to generosity in early childhood. Curr. Biol. 25, 93–97. (doi:10.1016/j.cub.2014.11.002)
78. Paulus M. 2014 The emergence of prosocial behavior: why do infants and toddlers help, comfort, and share? Child Dev. Perspect. 8, 77–81. (doi:10.1111/cdep.12066)
79. Tomasello M, Vaish A. 2011 Origins of human cooperation and morality. Annu. Rev. Psychol. 64, 231–255. (doi:10.1146/annurev-psych-113011-143812)
80. Prétôt L, Brosnan S. 2015 The evolution of morality: a comparative approach. In The moral brain: a multidisciplinary perspective (eds J Decety, T Wheatley), pp. 3–18. Cambridge, MA: MIT Press.
81. Dunfield K, Kuhlmeier VA, O’Connell L, Kelley E. 2011 Examining the diversity of prosocial behavior: helping, sharing, and comforting in infancy. Infancy 16, 227–247. (doi:10.1111/j.1532-7078.2010.00041.x)
82. Hay DF, Nash A, Pedersen J. 1981 Responses of sixmonth- olds to the distress of their peers. Child Dev. 52, 1071–1075. (doi:10.2307/1129114)
83. Geangu E, Hauf P, Bhardwaj R, Bentz W. 2011 Infant pupil diameter changes in response to others’ positive and negative emotions. PLoS ONE 6, e27132. (doi:10.1371/journal.pone.0027132)
84. Roth-Hanania R, Davidov M, Zahn-Waxler C. 2011 Empathy development from 8 to 16 months: early signs of concern for others. Infant Behav. Dev. 34, 447–458. (doi:10.1016/j.infbeh.2011.04.007)
85. Kanakogi Y, Okumura Y, Inoue Y, Kitazaki M, Itakura S. 2013 Rudimentary sympathy in preverbal infants: preference for others in distress. PLoS ONE, 8, e65292. (doi:10.1371/journal.pone.0065292)
86. Knafo A, Zahn-Waxler C, Van Hulle C, Robinson JL, Rhee SH. 2008 The developmental origins of a disposition toward empathy: genetic and environmental contributions. Emotion 8, 737–752. (doi:10.1037/a0014179)
87. Decety J, Howard LH. 2013 The role of affect in the neurodevelopment of morality. Child Dev. Perspect. 7, 49–54. (doi:10.1111/cdep.12020)
88. Hamlin J. 2015 The infantile origins of our moral brains. In The moral brain—a multidisciplinary perspective (eds J Decety, T Wheatley), pp. 105–122. Cambridge, MA: MIT Press.
89. Hepach R, Vaish A, Tomasello M. 2012 Young children are intrinsically motivated to see others helped. Psychol. Sci. 23, 967–972. (doi:10.1177/0956797612440571)
90. Zahn-Waxler C, Radke-Yarrow M, Wagner E, Chapman M. 1992 Development of concern for others. Dev. Psychol. 28, 126–136. (doi:10.1037/0012-1649.28.1.126)
91. Williams A, O’Driscoll K, Moore C. 2014 The influence of empathic concern on prosocial behavior in children. Front. Psychol. 5, 1–8. (doi:10.3389/fpsyg.2014.00425)
92. Benenson JF, Pascoe J, Radmore N. 2007 Children’s altruistic behavior in the dictator game. Evol. Hum. Behav. 28, 168–175. (doi:10.1016/j.evolhumbehav.2006.10.003)
93. Li Y, Li H, Decety J, Lee K. 2013 Experiencing a natural disaster alters children’s altruistic giving. Psychol. Sci. 24, 1686–1695. (doi:10.1177/0956797613479975)
94. Knafo A, Uzefovsky F. 2013 Variation in empathy: the interplay of genetic and environmental factors. In The infant mind: origins of the social brain (eds M Legerstee, DW Haley, MH Bornstein), pp. 97–122. New York, NY: Guilford.
95. Gregory AM, Light-Häusermann JH, Rijsdijk F, Eley TC. 2009 Behavioral genetic analyses of prosocial behavior in adolescents. Dev. Sci. 12, 165–174. (doi:10.1111/j.1467-7687.2008.00739.x)
96. Knafo A, Plomin R. 2006 Prosocial behavior from early to middle childhood: genetic and environmental influences on stability and change. Dev. Psychol. 42, 771–786. (doi:10.1037/0012-1649.42.5.771)
97. Christ CC, Carlo G, Stoltenberg SF. 2015 Oxytocin receptor (OXTR) single nucleotide polymorphisms indirectly predict prosocial behavior through perspective taking and empathic concern. J. Pers. (doi:10.1111/jopy.12152)
98. Wade M, Hoffmann TJ, Wigg K, Jenkins JM. 2014 Association between the oxytocin receptor (OXTR) gene and children’s social cognition at 18 months. Genes Brain Behav. 13, 603–610. (doi:10.1111/gbb.12148)
99. Wu N, Su Y. 2013 Oxytocin receptor gene relates to theory of mind and prosocial behavior in children. J. Cogn. Dev. 16, 302–313. (doi:10.1080/15248372.2013.858042)
100. Darley J, Latane B. 1970 Norms and normative behavior: field studies of social interdependence. In Altruism and helping behavior (eds J Macauley, L Berkowitz), pp. 83–102. New York, NY: Academic Press.
101. Hull C. 1943 Principles of behavior. Englewood Cliffs, NJ: Prentice Hall.
102. Shaun Ho S, Konrath S, Brown S, Swain JE. 2014 Empathy and stress related neural responses in maternal decision making. Front. Neurosci. 8, 1–9. (doi:10.3389/fnins.2014.00152)
103. Rutgen M, Seidel E-M, Riecˇansky´ I, Lamm C. 2015 Reduction of empathy for pain by placebo analgesia suggests functional equivalence of empathy and first-hand emotion experience. J. Neurosci. 35, 8938–8947. (doi:10.1523/JNEUROSCI.3936-14.2015)
104. Perkins AM, Leonard AM, Weaver K, Dalton JA, Mehta MA, Kumari V, Williams SCR, Ettinger U. 2012 A dose of ruthlessness: interpersonal moral judgment is hardened by the anti-anxiety drug Lorazepam. J. Exp. Psychol. Gen. 142, 612–620. (doi:10.1037/a0030256)
105. Terbeck S, Kahane G, McTavish S, Savulescu J, Cowen PJ, Hewstone M. 2012 Propranolol reduces implicit negative racial bias. Psychopharmacology (Berl). 222, 419–424. (doi:10.1007/s00213-012-2657-5)
106. Welt T, Engelmann M, Renner U, Erhardt A, Müller MB, Landgraf R, Holsboer F, Keck ME. 2006 Temazepam triggers the release of vasopressin into the rat hypothalamic paraventricular nucleus: novel insight into benzodiazepine action on hypothalamic-pituitary-adrenocortical system activity during stress. Neuropsychopharmacology 31, 2573–2579. (doi:10.1038/sj.npp.1301006)
107. Yagi K, Onaka T. 1996 A benzodiazepine, chlordiazepoxide, blocks vasopressin and oxytocin release after footshocks but not osmotic stimulus in the rat. Neurosci. Lett. 203, 49–52. (doi:10.1016/0304-3940(95)12262-1)
108. Moll J, Krueger F, Zahn R, Pardini M, de Oliveira- Souza R, Grafman J. 2006 Human fronto-mesolimbic networks guide decisions about charitable donation. Proc. Natl Acad. Sci. USA 103, 15623–15628. (doi:10.1073/pnas.0604475103)
109. Harbaugh W, Mayr U, Burghart D. 2007 Neural responses to taxation and voluntary giving reveal motives for charitable donations. Science 316, 1622–1625. (doi:10.1126/science.1140738)
110. Jablonka E, Lamb M. 2005 Evolution in four dimensions. Cambridge, MA: MIT Press.
111. Clay Z, de Waal FBM. 2013 Bonobos respond to distress in others: consolation across the age spectrum. PLoS ONE 8, e55206. (doi:10.1371/journal.pone.0055206)
112. McGraw LA, Young LJ. 2010 The prairie vole: an emerging model organism for understanding the social brain. Trends Neurosci. 33, 103–109. (doi:10.1016/j.tins.2009.11.006)
113. Dölen G, Darvishzadeh A, Huang KW, Malenka RC. 2013 Social reward requires coordinated activity of nucleus accumbens oxytocin and serotonin. Nature 501, 179–184. (doi:10.1038/nature12518)
114. Kendrick K. 2013 Oxytocin regulation of sheep social. In Oxytocin, vasopressin and related peptides in the regulation of behavior (eds E Choleris, DW Pfaff, M Kavaliers), pp. 183–192. New York, NY: Cambridge University Press.
115. Kelly AM, Goodson JL. 2014 Hypothalamic oxytocin and vasopressin neurons exert sex-specific effects on pair bonding, gregariousness, and aggression in finches. Proc. Natl Acad. Sci. USA 111, 6069–6074. (doi:10.1073/pnas.1322554111)
116. Braida D, Donzelli A, Martucci R, Capurro V, Busnelli M, Chini B, Sala M. 2012 Neurohypophyseal hormones manipulation modulate social and anxiety-related behavior in zebrafish. Psychopharmacology (Berl.) 220, 319–330. (doi:10.1007/s00213-011-2482-2)
117. Beery AK, Kaufer D. 2015 Stress, social behavior, and resilience: insights from rodents. Neurobiol. Stress 1, 116–127. (doi:10.1016/j.ynstr.2014.10.004)
118. Rice G, Gainer P. 1962 ‘Altruism’ in the albino rat. J. Comp. Physiol. Psychol. 55, 123–125. (doi:10.1037/h0042276)
119. Sato N, Tan L, Tate K, Okada M. 2015 Rats demonstrate helping behavior toward a soaked conspecific. Anim. Cogn. 18, 1039–1047. (doi:10.1007/s10071-015-0872-2)
120. Silberberg A, Allouch C, Sandfort S, Kearns D, Karpel H, Slotnick B. 2014 Desire for social contact, not empathy, may explain ‘rescue’ behavior in rats. Anim. Cogn. 17, 609–618. (doi:10.1007/s10071-013-0692-1)
121. Hernandez-Lallement J, van Wingerden M, Marx C, Srejic M, Kalenscher T. 2015 Rats prefer mutual rewards in a prosocial choice task. Front. Neurosci. 8, 1–9. (doi:10.3389/fnins.2014.00443)
122. Márquez C, Rennie SM, Costa DF, Moita MA. 2015 Prosocial choice in rats depends on food-seeking behavior displayed by recipients. Curr. Biol. 25, 1736–1745. (doi:10.1016/j.cub.2015.05.018)
123. Bartal I, Decety J, Mason P. 2011 Empathy and pro-social behavior in rats. Science (80-.) 334, 1427–1431. (doi:10.1126/science.1210789)
124. Ben-Ami Bartal I, Murray T, Bernardez Sarria MS, Decety J, Mason P. 2013 Emotional contagion is required for prosocial behavior in rats. Poster presented at Neuroscience 2013, 43rd Annu. Meet. Society for Neuroscience, San Diego, CA.
125. Martin LJ et al. 2015 Reducing social stress elicits emotional contagion of pain in mouse and human strangers. Curr. Biol. 25, 326–332. (doi:10.1016/j.cub.2014.11.028)
126. Melloni M, Lopez V, Ibanez A. 2014 Empathy and contextual social cognition. Cogn. Affect. Behav. Neurosci. 14, 407–425. (doi:10.3758/s13415-013-0205-3)
127. Cheng Y, Chen C, Lin C-P, Chou K-H, Decety J. 2010 Love hurts: an fMRI study. Neuroimage 51, 923–929. (doi:10.1016/j.neuroimage.2010.02.047)
128. Decety J, Echols S, Correll J. 2010 The blame game: the effect of responsibility and social stigma on empathy for pain. J. Cogn. Neurosci. 22, 985–997. (doi:10.1162/jocn.2009.21266)
129. Xu X, Zuo X, Wang X, Han S. 2009 Do you feel my pain? Racial group membership modulates empathic neural responses. J. Neurosci. 29, 8525–8529. (doi:10.1523/JNEUROSCI.2418-09.2009)
130. Forgiarini M, Gallucci M, Maravita A. 2011 Racism and the empathy for pain on our skin. Front. Psychol. 2, 1–7. (doi:10.3389/fpsyg.2011.00108)
131. Contreras-Huerta LS, Hielscher E, Sherwell CS, Rens N, Cunnington R. 2014 Intergroup relationships do not reduce racial bias in empathic neural responses to pain. Neuropsychologia 64C, 263–270. (doi:10.1016/j.neuropsychologia.2014.09.045)
132. Cikara M, Botvinick M, Fiske S. 2011 Us versus them: social identity shapes neural responses to intergroup competition and harm. Psychol. Sci. 22, 306–313. (doi:10.1177/0956797610397667)
133. Ben-Ami Bartal I, Rodgers DA, Bernardez Sarria MS, Decety J, Mason P. 2014 Pro-social behavior in rats is modulated by social experience. Elife 3, e01385. (doi:10.7554/eLife.01385)
134. Zuo X, Han S. 2013 Cultural experiences reduce racial bias in neural responses to others’ suffering. Cult. Brain 1, 34–46. (doi:10.1007/s40167-013-0002-4)
135. Telzer EH, Humphreys KL, Shapiro M, Tottenham N. 2012 Amygdala sensitivity to race is not present in childhood but emerges over adolescence. J. Cogn. Neurosci. 25, 234–244. (doi:10.1162/jocn_a_00311)
136. Cao Y, Contreras-Huerta LS, McFadyen J, Cunnington R. 2015 Racial bias in neural response to others’ pain is reduced with other-race contact. Cortex 70, 68–78. (doi:10.1016/j.cortex.2015.02.010)
137. Darwin C. 1871 The descent of man. London, UK: Watts & Co.