Rudimentary empathy in macaques’ social decision-making

Significance We investigated nonhuman primate prosociality within a decision-making behavioral framework. Our results suggest that macaques have a concept of their peers’ well being. The strength and originality of our experimental design is in challenging monkeys with several decisions involving both pleasant and unpleasant outcomes to self and others, thus allowing us to evaluate social motivation in different contexts. Behavioral measures, such as empathic eye blinking and mutual looking, show that the degrees of empathy and of willingness to interact with peers differ among individuals. These differences were mainly consistent with the preexisting social bonds displayed within our group-housed monkeys. Our results thus provide evidence of partner-dependent behavioral mechanisms shaping primates’ social decisions. Primates live in highly social environments, where prosocial behaviors promote social bonds and cohesion and contribute to group members’ fitness. Despite a growing interest in the biological basis of nonhuman primates’ social interactions, their underlying motivations remain a matter of debate. We report that macaque monkeys take into account the welfare of their peers when making behavioral choices bringing about pleasant or unpleasant outcomes to a monkey partner. Two macaques took turns in making decisions that could impact their own welfare or their partner’s. Most monkeys were inclined to refrain from delivering a mildly aversive airpuff and to grant juice rewards to their partner. Choice consistency between these two types of outcome suggests that monkeys display coherent motivations in different social interactions. Furthermore, spontaneous affilitative group interactions in the home environment were mostly consistent with the measured social decisions, thus emphasizing the impact of preexisting social bonds on decision-making. Interestingly, unique behavioral markers predicted these decisions: benevolence was associated with enhanced mutual gaze and empathic eye blinking, whereas indifference or malevolence was associated with lower or suppressed such responses. Together our results suggest that prosocial decision-making is sustained by an intrinsic motivation for social affiliation and controlled through positive and negative vicarious reinforcements.

[1]  E. Visalberghi,et al.  Capuchin Monkeys Display Affiliation Toward Humans Who Imitate Them , 2009, Science.

[2]  R. Hari,et al.  Brain responds to another person's eye blinks in a natural setting—the more empathetic the viewer the stronger the responses , 2015, The European journal of neuroscience.

[3]  J. Masserman,et al.  "ALTRUISTIC" BEHAVIOR IN RHESUS MONKEYS. , 1964, The American journal of psychiatry.

[4]  V. Gallese Before and below ‘theory of mind’: embodied simulation and the neural correlates of social cognition , 2007, Philosophical Transactions of the Royal Society B: Biological Sciences.

[5]  D. Symmes,et al.  The hierarchy of dominance in a group of macaques. , 1966, Behaviour.

[6]  K. Bard,et al.  Group differences in the mutual gaze of chimpanzees (Pan troglodytes). , 2005, Developmental psychology.

[7]  B. Thierry,et al.  Collective arousal when reuniting after temporary separation in Tonkean macaques. , 2011, American journal of physical anthropology.

[8]  Laurie R Santos,et al.  Insights into Intraspecies Variation in Primate Prosocial Behavior: Capuchins (Cebus apella) Fail to Show Prosociality on a Touchscreen Task , 2014, Behavioral sciences.

[9]  B. Spruijt,et al.  Inequity aversion in relation to effort and relationship quality in long‐tailed Macaques (Macaca fascicularis) , 2012, American journal of primatology.

[10]  Social object play among young Japanese macaques (Macaca fuscata) in Arashiyama, Japan , 2006, Primates.

[11]  C. Batson These things called empathy: Eight related but distinct phenomena. , 2009 .

[12]  J. Duhamel,et al.  A real-time 3D video tracking system for monitoring primate groups , 2014, Journal of Neuroscience Methods.

[13]  W. Streich,et al.  Coalition formation among male Barbary macaques (Macaca sylvanus) , 2000, American journal of primatology.

[14]  Frans B. M. de Waal,et al.  The Antiquity of Empathy , 2012 .

[15]  S. Suomi,et al.  Reciprocal Face-to-Face Communication between Rhesus Macaque Mothers and Their Newborn Infants , 2009, Current Biology.

[16]  Elizabeth W. Dunn,et al.  Giving Leads to Happiness in Young Children , 2012, PloS one.

[17]  Robin I. M. Dunbar,et al.  Group size, grooming and social cohesion in primates , 2007, Animal Behaviour.

[18]  Matthijs Verhage,et al.  A solution to dependency: using multilevel analysis to accommodate nested data , 2014, Nature Neuroscience.

[19]  S. Preston,et al.  Empathy: Its ultimate and proximate bases. , 2001, The Behavioral and brain sciences.

[20]  N. Kazahari 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) , 2014, Primates.

[21]  J. King,et al.  Personality from the Perspective of a Primatologist , 2011 .

[22]  Kelly D. Hughes,et al.  Social tolerance in a despotic primate: co-feeding between consortship partners in rhesus macaques. , 2012, American journal of physical anthropology.

[23]  B. Spruijt,et al.  Benefiting friends or dominants: prosocial choices mainly depend on rank position in long-tailed macaques (Macaca fascicularis) , 2011, Primates.

[24]  Judith M Burkart,et al.  Other-regarding preferences in a non-human primate: Common marmosets provision food altruistically , 2007, Proceedings of the National Academy of Sciences.

[25]  Lydia M. Hopper,et al.  Selective and contagious prosocial resource donation in capuchin monkeys, chimpanzees and humans , 2015, Scientific Reports.

[26]  B. Majolo,et al.  Coping with the cold: predictors of survival in wild Barbary macaques, Macaca sylvanus , 2013, Biology Letters.

[27]  J. Massen,et al.  No costly prosociality among related long-tailed macaques (Macaca fascicularis). , 2015, Journal of comparative psychology.

[28]  D. Sprague,et al.  Activity and social factors affect cohesion among individuals in female Japanese macaques: A simultaneous focal‐follow study , 2014, American journal of primatology.

[29]  P. Ferrari,et al.  Contagious yawning in gelada baboons as a possible expression of empathy , 2009, Proceedings of the National Academy of Sciences.

[30]  Shayna Marks,et al.  Early environment shapes the development of gaze aversion by wild bonnet macaques (Macaca radiata) , 2002, Primates.

[31]  Pier Francesco Ferrari,et al.  Towards a bottom-up perspective on animal and human cognition , 2010, Trends in Cognitive Sciences.

[32]  Steve W. C. Chang,et al.  Vicarious Reinforcement in Rhesus Macaques (Macaca Mulatta) , 2011, Front. Neurosci..

[33]  Eric B. Keverne,et al.  Beta-endorphin concentrations in cerebrospinal fluid of monkeys are influenced by grooming relationships , 1989, Psychoneuroendocrinology.

[34]  Berry M. Spruijt,et al.  Generous Leaders and Selfish Underdogs: Pro-Sociality in Despotic Macaques , 2010, PloS one.

[35]  W. Sommer,et al.  How about Lunch? Consequences of the Meal Context on Cognition and Emotion , 2013, PloS one.

[36]  J. Banks,et al.  The communication of affects in monkeys: cooperative reward conditioning. , 1966, The Journal of genetic psychology.

[37]  Andrew N. Meltzoff,et al.  How do we perceive the pain of others? A window into the neural processes involved in empathy , 2005, NeuroImage.

[38]  N. Emery,et al.  The eyes have it: the neuroethology, function and evolution of social gaze , 2000, Neuroscience & Biobehavioral Reviews.

[39]  Elisabetta Visalberghi,et al.  Macaques (Macaca nemestrina) recognize when they are being imitated , 2005, Biology Letters.

[40]  N. Clayton,et al.  Evidence suggesting that desire-state attribution may govern food sharing in Eurasian jays , 2013, Proceedings of the National Academy of Sciences.

[41]  F. D. de Waal Putting the altruism back into altruism: the evolution of empathy. , 2008, Annual review of psychology.

[42]  T. Insel,et al.  The neurobiology of attachment , 2001, Nature Reviews Neuroscience.

[43]  J. Decety,et al.  Putting together phylogenetic and ontogenetic perspectives on empathy , 2012, Developmental Cognitive Neuroscience.

[44]  B. Voelkl,et al.  Supply and demand determine the market value of food providers in wild vervet monkeys , 2009, Proceedings of the National Academy of Sciences.

[45]  J. Decety,et al.  A Social-Neuroscience Perspective on Empathy , 2006 .

[46]  L. Barsalou,et al.  Embodiment in Attitudes, Social Perception, and Emotion , 2005, Personality and social psychology review : an official journal of the Society for Personality and Social Psychology, Inc.

[47]  Jean Decety,et al.  Empathy and Pro-Social Behavior in Rats , 2011, Science.

[48]  Timothy K. Leonard,et al.  How macaques view familiarity and gaze in conspecific faces. , 2012, Behavioral neuroscience.

[49]  E. Visalberghi,et al.  Food transfers in capuchin monkeys: an experiment on partner choice , 2012, Biology Letters.

[50]  T. Hasegawa,et al.  Familiarity Bias and Physiological Responses in Contagious Yawning by Dogs Support Link to Empathy , 2013, PloS one.

[51]  Jean Decety,et al.  Annals of the New York Academy of Sciences the Neuroevolution of Empathy , 2022 .

[52]  Lance M. Optican,et al.  Unix-based multiple-process system, for real-time data acquisition and control , 1982 .

[53]  V. Horner,et al.  Spontaneous prosocial choice by chimpanzees , 2011, Proceedings of the National Academy of Sciences.

[54]  H. Sugiura,et al.  Japanese Macaques Depend not Only on Neighbours but also on More Distant Members for Group Cohesion , 2014 .

[55]  A. Anokhin,et al.  Startle modulation by affective faces , 2010, Biological Psychology.

[56]  A. Chamove Role or dominance in macaque response to novel objects , 1983 .

[57]  R. Seyfarth,et al.  Social relationships and social cognition in nonhuman primates. , 1986, Science.

[58]  E. Ferguson,et al.  Defining and measuring blood donor altruism: a theoretical approach from biology, economics and psychology , 2013, Vox sanguinis.

[59]  B. Hare,et al.  Bonobos voluntarily share their own food with others , 2010, Current Biology.

[60]  Curtis E. Thomsen,et al.  Eye contact by non-human primates toward a human observer , 1974 .

[61]  K. Gothard,et al.  Videos of conspecifics elicit interactive looking patterns and facial expressions in monkeys. , 2011, Behavioral neuroscience.

[62]  F. D. de Waal,et al.  Giving is self-rewarding for monkeys , 2008, Proceedings of the National Academy of Sciences.

[63]  Christian Keysers,et al.  Experience Modulates Vicarious Freezing in Rats: A Model for Empathy , 2011, PloS one.

[64]  D. Amaral,et al.  Acoustic Startle Reflex in Rhesus Monkeys: A Review , 2008, Reviews in the neurosciences.

[65]  J. Duhamel,et al.  Compete to Play: Trade-Off with Social Contact in Long-Tailed Macaques (Macaca fascicularis) , 2014, PloS one.

[66]  B. Thierry,et al.  The function of greetings in male Tonkean macaques , 2014, American journal of primatology.

[67]  J. Panksepp,et al.  Toward a cross-species understanding of empathy , 2013, Trends in Neurosciences.

[68]  Solomon Diamond,et al.  Personality and temperament , 1957 .

[69]  Stuart Semple,et al.  Grooming in Barbary macaques: better to give than to receive? , 2007, Biology Letters.

[70]  J. Decety,et al.  Pro-social behavior in rats is modulated by social experience , 2014, eLife.

[71]  M. Cords Post-conflict reunions and reconciliation in long-tailed macaques , 1992, Animal Behaviour.

[72]  S. Preston,et al.  The origins of altruism in offspring care. , 2013, Psychological bulletin.

[73]  M. Brüne,et al.  Towards a neuroscience of empathy: Ontogeny, phylogeny, brain mechanisms, context and psychopathology , 2013, Neuroscience & Biobehavioral Reviews.