Rudimentary empathy in macaques' social decision-making

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 50, 2015, Pages 15516-15521

  Ballesta, Sebastien ^a,b   Duhamel, Jean René ^a,b  

^a INSTITUT DES SCIENCES COGNITIVES   (France)

^b UNIVERSITÉ LYON 1   (France)

Author keywords

Emotions; Eye blink; Prosocial; Social gaze; Social neuroscience

Indexed keywords

ADULT; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANTICIPATION; ARTICLE; DECISION MAKING; EMPATHY; EYELID REFLEX; FEMALE; GAZE; GROOMING; GROUP DYNAMICS; HOME ENVIRONMENT; MACACA FASCICULARIS; MALE; MOTIVATION; NONHUMAN; PRIORITY JOURNAL; REWARD; RHESUS MONKEY; SOCIAL BONDING; SOCIAL INTERACTION; SOCIAL STRUCTURE; VISUAL FIELD; WELFARE; ANIMAL; BLINKING; EYE FIXATION; MACACA; MULTILEVEL ANALYSIS; PHYSIOLOGY; SOCIAL BEHAVIOR; TASK PERFORMANCE; THEORETICAL MODEL;

ANIMALS; BLINKING; CHOICE BEHAVIOR; DECISION MAKING; EMPATHY; FIXATION, OCULAR; MACACA; MALE; MODELS, THEORETICAL; MULTILEVEL ANALYSIS; SOCIAL BEHAVIOR; TASK PERFORMANCE AND ANALYSIS;

EID: 84950291653     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1504454112     Document Type: Article

References (73)

1. Cheney D, Seyfarth R, Smuts B (1986) Social relationships and social cognition in nonhuman primates. Science 234(4782):1361-1366.
2. Ben-Ami Bartal I, Decety J, Mason P (2011) Empathy and pro-social behavior in rats. Science 334(6061):1427-1430.
3. Atsak P, et al. (2011) Experience modulates vicarious freezing in rats: A model for empathy. PLoS One 6(7):e21855.
4. Ben-Ami Bartal I, Rodgers DA, Bernardez Sarria MS, Decety J, Mason P (2014) Prosocial behavior in rats is modulated by social experience. eLife 3:e01385.
5. Ostojić L, Shaw RC, Cheke LG, Clayton NS (2013) Evidence suggesting that desire-state attribution may govern food sharing in Eurasian jays. Proc Natl Acad Sci USA 110(10): 4123-4128.
6. Decety J (2011) The neuroevolution of empathy. Ann N Y Acad Sci 1231(1):35-45.
7. Preston SD, de Waal FB (2002) Empathy: Its ultimate and proximate bases. Behav Brain Sci 25(1):1-20, discussion 20-71.
8. Batson CD (2009) These things called empathy: Eight related but distinct phenomena. The Social Neuroscience of Empathy, eds Decety J, Ickes W (MIT Press, Cambridge, MA), pp 3-15.
9. Insel TR, Young LJ (2001) The neurobiology of attachment. Nat Rev Neurosci 2(2): 129-136.
10. Keverne EB, Martensz ND, Tuite B (1989) Beta-endorphin concentrations in cerebrospinal fluid of monkeys are influenced by grooming relationships. Psychoneuroendocrinology 14(1-2):155-161.
11. Shimada M (2006) Social object play among young Japanese macaques (Macaca fuscata) in Arashiyama, Japan. Primates 47(4):342-349.
12. Shutt K, MacLarnon A, Heistermann M, Semple S (2007) Grooming in Barbary macaques: Better to give than to receive? Biol Lett 3(3):231-233.
13. Masserman JH, Wechkin S, Terris W (1964) "Altruistic" behavior in rhesus monkeys. Am J Psychiatry 121:584-585.
14. Miller RE, Banks JH, Jr, Kuwahara H (1966) The communication of affects in monkeys: Cooperative reward conditioning. J Genet Psychol 108(1st Half):121-134.
15. de Waal FBM, Ferrari PF (2010) Towards a bottom-up perspective on animal and human cognition. Trends Cogn Sci 14(5):201-207.
16. de Waal FB (2008) Putting the altruism back into altruism: The evolution of empathy. Annu Rev Psychol 59(1):279-300.
17. Panksepp J, Panksepp JB (2013) Toward a cross-species understanding of empathy. Trends Neurosci 36(8):489-496.
18. Decety J, Jackson PL (2006) A social-neuroscience perspective on empathy. Curr Dir Psychol Sci 15(2):54-58.
19. Decety J, Svetlova M (2012) Putting together phylogenetic and ontogenetic perspectives on empathy. Dev Cogn Neurosci 2(1):1-24.
20. Gonzalez-Liencres C, Shamay-Tsoory SG, Brüne M (2013) Towards a neuroscience of empathy: Pntogeny, phylogeny, brain mechanisms, context and psychopathology. Neurosci Biobehav Rev 37(8):1537-1548.
21. Evans R, Ferguson E (2014) Defining and measuring blood donor altruism: A theoretical approach from biology, economics and psychology. Vox Sang 106(2):118-126.
22. de Waal FB, Leimgruber K, Greenberg AR (2008) Giving is self-rewarding for monkeys. Proc Natl Acad Sci USA 105(36):13685-13689.
23. 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(3):771-779.
24. Gallese V (2007) Before and below 'theory of mind': Embodied simulation and the neural correlates of social cognition. Philos Trans R Soc Lond B Biol Sci 362(1480): 659-669.
25. Niedenthal PM, Barsalou LW, Winkielman P, Krauth-Gruber S, Ric F (2005) Embodiment in attitudes, social perception, and emotion. Pers Soc Psychol Rev 9(3):184-211.
26. Aarts E, Verhage M, Veenvliet JV, Dolan CV, van der Sluis S (2014) A solution to dependency: Using multilevel analysis to accommodate nested data. Nat Neurosci 17(4): 491-496.
27. Paukner A, Anderson JR, Borelli E, Visalberghi E, Ferrari PF (2005) Macaques (Macaca nemestrina) recognize when they are being imitated. Biol Lett 1(2):219-222.
28. Paukner A, Suomi SJ, Visalberghi E, Ferrari PF (2009) Capuchin monkeys display affiliation toward humans who imitate them. Science 325(5942):880-883.
29. Mandel A, Helokunnas S, Pihko E, Hari R (2015) Brain responds to another person's eye blinks in a natural setting-The more empathetic the viewer the stronger the responses. Eur J Neurosci 42(8):2508-2514.
30. Ballesta S, Reymond G, Pozzobon M, Duhamel J-R (2014) A real-time 3D video tracking system for monitoring primate groups. J Neurosci Methods 234:147-152.
31. Massen JJM, Luyten IJAF, Spruijt BM, Sterck EHM (2011) Benefiting friends or dominants: Prosocial choices mainly depend on rank position in long-tailed macaques (Macaca fascicularis). Primates 52(3):237-247.
32. Massen JJM, van den Berg LM, Spruijt BM, Sterck EHM (2010) Generous leaders and selfish underdogs: Pro-sociality in despotic macaques. PLoS One 5(3):e9734.
33. Chang SWC, Winecoff AA, Platt ML (2011) Vicarious reinforcement in rhesus macaques (macaca mulatta). Front Neurosci 5:27.
34. Sterck EHM, Olesen CU, Massen JJM (2015) No costly prosociality among related longtailed macaques (Macaca fascicularis). J Comp Psychol Wash DC 129(3):275-282.
35. Horner V, Carter JD, Suchak M, de Waal FBM (2011) Spontaneous prosocial choice by chimpanzees. Proc Natl Acad Sci USA 108(33):13847-13851.
36. Burkart JM, Fehr E, Efferson C, van Schaik CP (2007) Other-regarding preferences in a non-human primate: Common marmosets provision food altruistically. Proc Natl Acad Sci USA 104(50):19762-19766.
37. Claidière N, et al. (2015) Selective and contagious prosocial resource donation in capuchin monkeys, chimpanzees and humans. Sci Rep 5:7631.
38. Drayton LA, Santos LR (2014) Insights into Intraspecies Variation in Primate Prosocial Behavior: Capuchins (Cebus apella) Fail to Show Prosociality on a Touchscreen Task. Behav Sci (Basel) 4(2):87-101.
39. Massen JJM, Van Den Berg LM, Spruijt BM, Sterck EHM (2012) Inequity aversion in relation to effort and relationship quality in long-tailed Macaques (Macaca fascicularis). Am J Primatol 74(2):145-156.
40. Aknin LB, Hamlin JK, Dunn EW (2012) Giving leads to happiness in young children. PLoS One 7(6):e39211.
41. Preston SD (2013) The origins of altruism in offspring care. Psychol Bull 139(6): 1305-1341.
42. Dubuc C, Hughes KD, Cascio J, Santos LR (2012) Social tolerance in a despotic primate: Co-feeding between consortship partners in rhesus macaques. Am J Phys Anthropol 148(1):73-80.
43. Sabbatini G, De Bortoli Vizioli A, Visalberghi E, Schino G (2012) Food transfers in capuchin monkeys: An experiment on partner choice. Biol Lett 8(5):757-759.
44. Thomsen CE (1974) Eye contact by non-human primates toward a human observer. Anim Behav 22(1):144-149.
45. Emery NJ (2000) The eyes have it: The neuroethology, function and evolution of social gaze. Neurosci Biobehav Rev 24(6):581-604.
46. Bard KA, et al. (2005) Group differences in the mutual gaze of chimpanzees (Pan troglodytes). Dev Psychol 41(4):616-624.
47. Coss RG, Marks S, Ramakrishnan U (2002) Early environment shapes the development of gaze aversion by wild bonnet macaques (Macaca radiata). Primates 43(3):217-222.
48. Leonard TK, Blumenthal G, Gothard KM, Hoffman KL (2012) How macaques view familiarity and gaze in conspecific faces. Behav Neurosci 126(6):781-791.
49. Mosher CP, Zimmerman PE, Gothard KM (2011) Videos of conspecifics elicit interactive looking patterns and facial expressions in monkeys. Behav Neurosci 125(4): 639-652.
50. Ferrari PF, Paukner A, Ionica C, Suomi SJ (2009) Reciprocal face-to-face communication between rhesus macaque mothers and their newborn infants. Curr Biol 19(20): 1768-1772.
51. Sommer W, Stürmer B, Shmuilovich O, Martin-Loeches M, Schacht A (2013) How about lunch? Consequences of the meal context on cognition and emotion. PLoS One 8(7):e70314.
52. Hare B, Kwetuenda S (2010) Bonobos voluntarily share their own food with others. Curr Biol 20(5):R230-R231.
53. de Waal FBM (2012) The antiquity of empathy. Science 336(6083):874-876.
54. Atsak P, et al. (2011) Experience modulates vicarious freezing in rats: A model for empathy. PLoS One 6(7):e21855.
55. Palagi E, Leone A, Mancini G, Ferrari PF (2009) Contagious yawning in gelada baboons as a possible expression of empathy. Proc Natl Acad Sci USA 106(46):19262-19267.
56. Romero T, Konno A, Hasegawa T (2013) Familiarity bias and physiological responses in contagious yawning by dogs support link to empathy. PLoS One 8(8):e71365.
57. DavisM, Antoniadis EA, Amaral DG, Winslow JT (2008) Acoustic startle reflex in rhesus monkeys: A review. Rev Neurosci 19(2-3):171-185.
58. Anokhin AP, Golosheykin S (2010) Startle modulation by affective faces. Biol Psychol 83(1):37-40.
59. Cords M (1992) Post-conflict reunions and reconciliation in long-tailed macaques. Anim Behav 44(1):57-61.
60. Widdig A, Streich WJ, Tembrock G (2000) Coalition formation among male Barbary macaques (Macaca sylvanus). Am J Primatol 50(1):37-51.
61. Fruteau C, Voelkl B, van Damme E, Noë R (2009) Supply and demand determine the market value of food providers in wild vervet monkeys. Proc Natl Acad Sci USA 106(29):12007-12012.
62. Weiss A, King JE, Murray L (2011) Personality and Temperament in Nonhuman Primates (Springer, New York).
63. De Marco A, Cozzolino R, Dessì-Fulgheri F, Thierry B (2011) Collective arousal when reuniting after temporary separation in Tonkean macaques. Am J Phys Anthropol 146(3):457-464.
64. De Marco A, Sanna A, Cozzolino R, Thierry B (2014) The function of greetings in male Tonkean macaques. Am J Primatol 76(10):989-998.
65. Lehmann J, Korstjens AH, Dunbar RIM (2007) Group size, grooming and social cohesion in primates. Anim Behav 74(6):1617-1629.
66. Nishikawa M, Suzuki M, Sprague DS (2014) Activity and social factors affect cohesion among individuals in female Japanese macaques: A simultaneous focal-follow study. Am J Primatol 76(7):694-703.
67. Kazahari N (2014) Maintaining social cohesion is a more important determinant of patch residence time than maximizing food intake rate in a group-living primate, Japanese macaque (Macaca fuscata) primates. J Primatol 55(2):179-184.
68. Sugiura H, Shimooka Y, Tsuji Y (2014) Japanese macaques depend not only on neighbors but also on more distant members for group cohesion. Ethology 120(1):21-31.
69. McFarland R, Majolo B (2013) Coping with the cold: Predictors of survival in wild Barbary macaques, Macaca sylvanus. Biol Lett 9(4):20130428.
70. Hays A, Richmond B, Optican L (1982) Unix-Based Multiple-Process System, for Real-Time Data Acquisition and Control (Electron Conventions, El Segundo, CA).
71. Ballesta S, Reymond G, Pozzobon M, Duhamel J-R (2014) Compete to play: Trade-off with social contact in long-tailed macaques (Macaca fascicularis). PLoS ONE 9(12): e115965.
72. Varley M, Symmes D (1966) The hierarchy of dominance in a group of macaques. Behaviour 27(1):54-75.
73. Chamove AS (1983) Role or dominance in macaque response to novel objects. Motiv Emot 7(2):213-228.