The DOI matches its Crossref record; 51 of the 51 references it cites were found in a registry or an index.
Vicarious Reinforcement in Rhesus Macaques (Macaca Mulatta)
Open accessAbstract
What happens to others profoundly influences our own behavior. Such other-regarding outcomes can drive observational learning, as well as motivate cooperation, charity, empathy, and even spite. Vicarious reinforcement may serve as one of the critical mechanisms mediating the influence of other-regarding outcomes on behavior and decision-making in groups. Here we show that rhesus macaques spontaneously derive vicarious reinforcement from observing rewards given to another monkey, and that this reinforcement can motivate them to subsequently deliver or withhold rewards from the other animal. We exploited Pavlovian and instrumental conditioning to associate rewards to self (M1) and/or rewards to another monkey (M2) with visual cues. M1s made more errors in the instrumental trials when cues predicted reward to M2 compared to when cues predicted reward to M1, but made even more errors when cues predicted reward to no one. In subsequent preference tests between pairs of conditioned cues, M1s preferred cues paired with reward to M2 over cues paired with reward to no one. By contrast, M1s preferred cues paired with reward to self over cues paired with reward to both monkeys simultaneously. Rates of attention to M2 strongly predicted the strength and valence of vicarious reinforcement. These patterns of behavior, which were absent in non-social control trials, are consistent with vicarious reinforcement based upon sensitivity to observed, or counterfactual, outcomes with respect to another individual. Vicarious reward may play a critical role in shaping cooperation and competition, as well as motivating observational learning and group coordination in rhesus macaques, much as it does in humans. We propose that vicarious reinforcement signals mediate these behaviors via homologous neural circuits involved in reinforcement learning and decision-making.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“Critically, rhesus macaques display basic aspects of complex social behaviors that are typically considered ‘uniquely human’ (Frith and Frith, 2007; Saxe, 2006). These include social imitation (Ferrari et al., 2006; Subiaul, 2004), prosocial behaviors (Chang et al., 2011; Masserman et al., 1964), as well as understanding others’ perceptions (Flombaum and Santos, 2005; Santos et al., 2006).”
From Oxytocin and social cognition in rhesus macaques: Implications for understanding and treating human psychopathology (2014) · cites this paper as Chang et al., 2011
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
Two new Later Stone Age sites from the Final Pleistocene in the Falémé Valley, eastern Senegal
Ndiaye, M., Lespez, L., Tribolo, C., Rassé, M., Hadjas, I., Davidoux, S., Huysecom, É., & Douze, K. (2024) · Monash University Research Portal (Monash University) · doi:10.3929/ethz-b-000667478 · Cited by 24,214
Brainard, D. H. (1997) · Spatial Vision · doi:10.1163/156856897x00357 · Cited by 20,012 · cited 1×
“Stimuli were controlled by a computer running Matlab using PsychToolbox (Brainard, 1997; Pelli, 1997).”
MethodThe VideoToolbox software for visual psychophysics: transforming numbers into movies
Pelli, D. G. (1997) · Spatial Vision · doi:10.1163/156856897x00366 · Cited by 11,110 · cited 2×
“Stimuli were controlled by a computer running Matlab using PsychToolbox (Brainard, 1997; Pelli, 1997).”
BackgroundMethodA neural substrate of prediction and reward
Schultz, W., Dayan, P., & Montague, P. R. (1997) · Science · doi:10.1126/science.275.5306.1593 · Cited by 9,388 · cited 2×
“Reinforcement learning provides a powerful mechanism for associating stimuli and actions with the direct experience of reward and punishment (Rescorla and Wagner, 1972; Schultz et al., 1997; Sutton and Barto, 1998).”
BackgroundInfluentialRescorla, R. A. (1972) · Medical Entomology and Zoology · Cited by 7,268
Impure Altruism and Donations to Public Goods: A Theory of Warm-Glow Giving
Andreoni, J. (1990) · The Economic Journal · doi:10.2307/2234133 · Cited by 5,825 · cited 2×
“The “warm glow” hypothesis (Andreoni, 1990) suggests that vicarious reward and punishment motivates individuals to prefer either Edited by: Daeyeol Lee, Yale University School of Medicine, USA Reviewed by: Mehrdad Jazayeri, University of Washington, USA James Rilling, Emory University,…”
BackgroundEmpathy: its ultimate and proximate bases
Preston, S. D., & de Waal, F. B. M. (2002) · Behavioral and Brain Sciences · doi:10.1017/s0140525x02000018 · Cited by 4,126 · cited 1×
“It has been documented that social interaction behaviors increase with familiarity in both humans and monkeys (Preston and de Waal, 2002).”
BackgroundFehr, E., & Fischbacher, U. (2003) · Nature · doi:10.1038/nature02043 · Cited by 3,475 · cited 4×
“Such observations endorse the idea that neural mechanisms supporting vicarious reinforcement are derived specializations of the human brain, which support complex social behavior including observational learning, cooperation, and even altruism (Fehr and Fischbacher, 2003).”
BackgroundInfluentialDoes the chimpanzee have a theory of mind? 30 years later
Call, J., & Tomasello, M. (2008) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2008.02.010 · Cited by 1,592 · cited 2×
“Others have argued that only those species most closely related to humans, namely chimpanzees and bonobos, possess the derived features of human biology and cognition, in particular “theory of mind” (Call and Tomasello, 2008), express other-regarding preferences, but again the evidence for such behavior in apes remain…”
BackgroundThe Functional Theory of Counterfactual Thinking
Epstude, K., & Roese, N. J. (2008) · Personality and Social Psychology Review · doi:10.1177/1088868308316091 · Cited by 905 · cited 1×
“For example, fictive, or counterfactual, learning describes sensitivity to reward outcomes for options that were not chosen, were merely observed, or were even imagined (Byrne, 2002; Lohrenz et al., 2007; Epstude and Roese, 2008).”
Background
Research works printed but not linked: 1
- Sutton R. S. Barto A. G. (1998). Reinforcement Learning: An Introduction. London: MIT Press
Cited by
Sorted by citations
Toward a second-person neuroscience
Schilbach, L., Timmermans, B., Reddy, V., Costall, A., Bente, G., Schlicht, T., & Vogeley, K. (2013) · Behavioral and Brain Sciences · doi:10.1017/s0140525x12000660 · Cited by 1,510
Neuronal Reward and Decision Signals: From Theories to Data
Schultz, W. (2015) · Physiological Reviews · doi:10.1152/physrev.00023.2014 · Cited by 1,126
The neurobiology of rewards and values in social decision making
Ruff, C. C., & Fehr, E. (2014) · Nature reviews. Neuroscience · doi:10.1038/nrn3776 · Cited by 716
Children discard a resource to avoid inequity.
Shaw, A., & Olson, K. R. (2011) · Journal of Experimental Psychology General · doi:10.1037/a0025907 · Cited by 408
Neuronal reference frames for social decisions in primate frontal cortex
Chang, S. W. C., Gariépy, J.-F., & Platt, M. L. (2013) · Nature Neuroscience · doi:10.1038/nn.3287 · Cited by 336
Marmosets: A Neuroscientific Model of Human Social Behavior
Miller, C. T., Freiwald, W. A., Leopold, D. A., Mitchell, J. F., Silva, A. C., & Wang, X. (2016) · Neuron · doi:10.1016/j.neuron.2016.03.018 · Cited by 338
“Such choice behavior depends not only on the stimulus but also on the impact a choice has on another animal observer (Chang et al., 2011).”
BackgroundThe neural and computational systems of social learning
Olsson, A., Knapska, E., & Lindström, B. (2020) · Nature reviews. Neuroscience · doi:10.1038/s41583-020-0276-4 · Cited by 285
“For example, primates are more likely to imitate and learn behaviours demonstrated by a dominant group member 140,141 , and greater perceived similarity with a demonstrator produces stronger threat learning in both mice 142 and humans 104,143 .”
BackgroundChang, S. W. C., Barter, J. W., Ebitz, R. B., Watson, K. K., & Platt, M. L. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1114621109 · Cited by 252
“neither, compared with when self reward is involved (34).”
BackgroundInfluentialChildren develop a veil of fairness.
Shaw, A., Montinari, N., Piovesan, M., Olson, K. R., Gino, F., & Norton, M. I. (2013) · Journal of Experimental Psychology General · doi:10.1037/a0031247 · Cited by 239
Genetic origins of social networks in rhesus macaques
Brent, L. J. N., Heilbronner, S. R., Horvath, J. E., Gonzalez-Martinez, J., Ruiz-Lambides, A., Robinson, A. G., Skene, J. H. P., & Platt, M. L. (2013) · Scientific Reports · doi:10.1038/srep01042 · Cited by 220
A universal role of the ventral striatum in reward-based learning: Evidence from human studies
Daniel, R., & Pollmann, S. (2014) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2014.05.002 · Cited by 225
Prosocial behaviour in animals: the influence of social relationships, communication and rewards
Cronin, K. A. (2012) · Animal Behaviour · doi:10.1016/j.anbehav.2012.08.009 · Cited by 205
“In Chang et al.’s (2011) study of vicarious reward in rhesus macaques described above, prosocial responses were more often directed from dominant towards subordinate individuals.”
BackgroundDecision Making: The Neuroethological Turn
Pearson, J. M., Watson, K. K., & Platt, M. L. (2014) · Neuron · doi:10.1016/j.neuron.2014.04.037 · Cited by 197
Social Fear Learning: from Animal Models to Human Function
Debiec, J., & Olsson, A. (2017) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2017.04.010 · Cited by 186
“For example, primates are more likely to imitate behaviors modeled by a dominant and knowledgeable group member [46, 48].”
BackgroundNeural mechanisms of social decision-making in the primate amygdala
Chang, S. W. C., Fagan, N. A., Toda, K., Utevsky, A. V., Pearson, J. M., & Platt, M. L. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1514761112 · Cited by 157
“Reaction times, the time from the onset of decisions to movement onset, were computed using a 20 °/s velocity threshold criterion (7, 33, 34).”
InfluentialAffiliation, empathy, and the origins of theory of mind
Seyfarth, R. M., & Cheney, D. L. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1301223110 · Cited by 164
“This preference was especially true if the partner was familiar (39).”
BackgroundNeuroethology of primate social behavior
Chang, S. W. C., Brent, L. J. N., Adams, G. K., Klein, J. T., Pearson, J. M., Watson, K. K., & Platt, M. L. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1301213110 · Cited by 157
“In this social reward-allocation task, monkeys tend to prefer to reward someone over no one, and this prosocial preference is magnified by familiarity and dominance status (96) and significantly modulated by neuropeptide OT (97).”
BackgroundKumaran, D., Banino, A., Blundell, C., Hassabis, D., & Dayan, P. (2016) · Neuron · doi:10.1016/j.neuron.2016.10.052 · Cited by 163
“…(Apps et al., 2016), but also incorporates rank information, particularly within one’s own social group, dovetailing with behavioral evidence concerning the influence of social dominance and familiarity on cooperative behavior (Chang et al., 2011; Molenberghs, 2013; Seyfarth and Cheney, 2012).”
BackgroundInfluentialSocial learning through prediction error in the brain
Joiner, J. A., Piva, M., Turrin, C., & Chang, S. W. C. (2017) · npj Science of Learning · doi:10.1038/s41539-017-0009-2 · Cited by 147
The neuroethology of friendship
Brent, L. J. N., Chang, S. W. C., Gariépy, J., & Platt, M. L. (2014) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.12315 · Cited by 138
The anterior cingulate cortex: an integrative hub for human socially-driven interactions
Lavín, C., Melis, C., Mikulan, E., Gelormini‐Lezama, C., Huepe, D., & Ibáñez, A. M. (2013) · Frontiers in Neuroscience · doi:10.3389/fnins.2013.00064 · Cited by 145
“This evidence is in line with the idea that social cognition involves the integration of flexible and contextdependent information (Chang et al., 2011; Ibanez and Manes, 2012).”
ResultModulation of value representation by social context in the primate orbitofrontal cortex
Azzi, J. C. B., Angela Sirigu, B., & Duhamel, J. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1111715109 · Cited by 129
“A behavioral experiment related to our own, but using a direct preference response, also found that monkeys more often choose a reward to self-only than a reward to both self and another monkey (27).”
BackgroundResultSocial rewards and social networks in the human brain
Fareri, D. S., & Delgado, M. R. (2014) · The Neuroscientist · doi:10.1177/1073858414521869 · Cited by 124
Social learning in humans and other animals
Gariépy, J., Watson, K. K., Du, E., Xie, D. L., Erb, J., Amasino, D. R., & Platt, M. L. (2014) · Frontiers in Neuroscience · doi:10.3389/fnins.2014.00058 · Cited by 133
“Masaki Isoda, Kansai Medical University, Japan Steve W. C. Chang, Duke University, USA”
BackgroundProsocial Choice in Rats Depends on Food-Seeking Behavior Displayed by Recipients
Márquez, C., Rennie, S. M., Costa, D. F., & Moita, M. A. P. (2015) · Current Biology · doi:10.1016/j.cub.2015.05.018 · Cited by 100
“Vicarious reward signals have been shown in the brain of human and non-human primates [44–46].”
Specialized medial prefrontal–amygdala coordination in other-regarding decision preference
Monte, O. D., Chu, C.-C. J., Fagan, N. A., & Chang, S. W. C. (2020) · Nature Neuroscience · doi:10.1038/s41593-020-0593-y · Cited by 101
Nihonsugi, T., Ihara, A. S., & Haruno, M. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.3885-14.2015 · Cited by 93
“…revealed that the insula, supplementary motor area, dorsolateral prefrontal cortex (DLPFC), and temporal parietal junction are involved (L.J. Chang et al., 2011), while studies of inequity aversion (Sanfey et al., 2003; Hsu Received Sept. 18, 2014; revised Jan. 1, 2015; accepted Jan. 6,…”
BackgroundInfluentialCritical issues in experimental studies of prosociality in non-human species
Marshall‐Pescini, S., Dale, R., Quervel-Chaumette, M., & Range, F. (2016) · Animal Cognition · doi:10.1007/s10071-016-0973-6 · Cited by 97
“Examples include Chang et al. (2011), who used eye tracking, and de Waal et al. (2008), using token exchange.”
Adaptations for social cognition in the primate brain
Platt, M. L., Seyfarth, R. M., & Cheney, D. L. (2016) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2015.0096 · Cited by 95
“Subjects were significantly more likely to choose the reward than the withhold option, and this prosocial tendency was enhanced by familiarity [105].”
BackgroundOxytocin enhances attention to the eye region in rhesus monkeys
Dal Monte, O., Noble, P. L., Costa, V. D., & Averbeck, B. B. (2014) · Frontiers in Neuroscience · doi:10.3389/fnins.2014.00041 · Cited by 80
“This is similar to the dose previously found to affect socially relevant behaviors in monkeys (Chang et al., 2011) and humans (Kirsch et al., 2005; Guastella et al., 2008b; Rimmele et al., 2009; Evans et al., 2010).”
ResultNeural mechanisms necessary for empathy-related phenomena across species
Paradiso, E., Gazzola, V., & Keysers, C. (2021) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2021.02.005 · Cited by 78
Activity of striatal neurons reflects social action and own reward
Báez-Mendoza, R., Harris, C., & Schultz, W. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1211342110 · Cited by 83
“1 E and F), confirming previous observations during social interaction of nonhuman primates (3, 8, 19).”
ResultChang, S. W. C., & Platt, M. L. (2014) · Brain Research · doi:10.1016/j.brainres.2013.11.006 · Cited by 71
“These include social imitation (Ferrari et al., 2006; Subiaul, 2004), prosocial behaviors (Chang et al., 2011; Masserman et al., 1964), as well as understanding others' perceptions (Flombaum and Santos, 2005; Santos et al., 2006).”
BackgroundInfluentialLevels of naturalism in social neuroscience research
Fan, S., Monte, O. D., & Chang, S. W. C. (2021) · iScience · doi:10.1016/j.isci.2021.102702 · Cited by 71
“Notably, studies using real-life paradigms have revealed distinct social behaviors as well as specific neural activity that are not observed when the social partners are absent or display non-contingent behaviors (Chang et al., 2011; Azzi et al., 2012; Hosokawa andWatanabe, 2012; Haroush andWilliams, 2015; Noritake et…”
BackgroundAmici, F., Visalberghi, E. M., & Call, J. (2014) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2014.1699 · Cited by 71
“distribution have produced mixed results [14-29].”
BackgroundBasile, B. M., Schafroth, J. L., Karaskiewicz, C. L., Chang, S. W. C., & Murray, E. A. (2020) · PLoS Biology · doi:10.1371/journal.pbio.3000677 · Cited by 68
Prefrontal cortex interactions with the amygdala in primates
Murray, E. A., & Fellows, L. K. (2021) · Neuropsychopharmacology · doi:10.1038/s41386-021-01128-w · Cited by 66
“Another task evaluates the prosocial tendencies of macaques by measuring the amount of reward obtained by conspecifics [221].”
BackgroundDynamic influences on the neural encoding of social valence
Padilla-Coreano, N., Tye, K. M., & Zelikowsky, M. (2022) · Nature reviews. Neuroscience · doi:10.1038/s41583-022-00609-1 · Cited by 59
Neuronal correlates of strategic cooperation in monkeys
Ong, W. S., Madlon‐Kay, S., & Platt, M. L. (2020) · Nature Neuroscience · doi:10.1038/s41593-020-00746-9 · Cited by 61
Do marmosets care to share? Oxytocin treatment reduces prosocial behavior toward strangers
Mustoe, A. C., Cavanaugh, J., Harnisch, A. M., Thompson, B. E., & French, J. A. (2015) · Hormones and Behavior · doi:10.1016/j.yhbeh.2015.04.015 · Cited by 59
“, 2008), OldWorld monkeys (OWM) (Chang et al., 2011; Massen et al., 2010), and New-World monkeys (NWM) (Burkart et al.”
BackgroundSocial and Non-social Mechanisms of Inequity Aversion in Non-human Animals
Oberließen, L., & Kalenscher, T. (2019) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2019.00133 · Cited by 59
Rudimentary empathy in macaques’ social decision-making
Ballesta, S., & Duhamel, J. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1504454112 · Cited by 57
“Are Social Stimuli Vicarious Reinforcers? The quest for proximal mechanisms of prosociality has led authors to hypothesize that prosocial behavior is shaped by the reinforcing value of certain social events (33).”
BackgroundInfluentialSocial tolerance in a despotic primate: Co‐feeding between consortship partners in rhesus macaques
Dubuc, C., Hughes, K. D., Cascio, J., & Santos, L. R. (2012) · American Journal of Physical Anthropology · doi:10.1002/ajpa.22043 · Cited by 53
“…(e.g., strict dominance hierarchy, low reconciliation tendencies), like chimpanzees (Pan troglodytes) and rhesus macaques (Macaca mulatta), fail to do so, even when such donations pose no cost to the actor (Silk et al., 2005; Hare et al., 2007; Vonk et al., 2008; Chang et al., 2011; but see below).”
BackgroundVicarious Neural Processing of Outcomes during Observational Learning
Monfardini, E., Gazzola, V., Boussaoud, D., Brovelli, A., Keysers, C., & Wicker, B. (2013) · PLoS ONE · doi:10.1371/journal.pone.0073879 · Cited by 61
“Learning-by-observation (LeO) plays a crucial role in many adaptive behaviours such as foraging and predator avoidance [4] and it has been observed in several animal species including rats [5], dogs [6], pigeons [7] and monkeys [8–11].”
BackgroundBasolateral amygdala lesions abolish mutual reward preferences in rats
Hernandez-Lallement, J., van Wingerden, M., Schäble, S., & Kalenscher, T. (2015) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2015.11.004 · Cited by 53
Jovanovic, V., Fishbein, A. R., de la Mothe, L. A., Lee, K., & Miller, C. T. (2022) · Neuron · doi:10.1016/j.neuron.2022.01.020 · Cited by 53
Resource allocation to kin, friends, and strangers by 3- to 6-year-old children
Lu, H. J., & Chang, L. (2016) · Journal of Experimental Child Psychology · doi:10.1016/j.jecp.2016.05.018 · Cited by 45
The psychology of cooperation in animals: an ecological approach
McAuliffe, K., & Thornton, A. (2015) · Journal of Zoology · doi:10.1111/jzo.12204 · Cited by 47
Neural basis of learning and preference during social decision-making
Seo, H., & Lee, D. (2012) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2012.05.010 · Cited by 45
Mustoe, A. C., Harnisch, A. M., Hochfelder, B., Cavanaugh, J., & French, J. A. (2016) · Animal Behaviour · doi:10.1016/j.anbehav.2016.01.025 · Cited by 40
Ninomiya, T., Noritake, A., Ullsperger, M., & Isoda, M. (2018) · Neuroscience Research · doi:10.1016/j.neures.2018.04.004 · Cited by 45
An integrated framework for the role of oxytocin in multistage social decision‐making
Piva, M., & Chang, S. W. C. (2018) · American Journal of Primatology · doi:10.1002/ajp.22735 · Cited by 38
Falcone, R., Brunamonti, E., Ferraina, S., & Genovesio, A. (2015) · Cerebral Cortex · doi:10.1093/cercor/bhv224 · Cited by 40
“It emerges from these studies that monkeys are able to monitor other agents’ choices and their outcome and to use this knowledge to guide their own decisions (Chang et al. 2011; Falcone, Brunamonti, Ferraina et al. 2012; Falcone, Brunamonti, and Genovesio 2012; Bevacqua et al. 2013; Falcone et al. 2013).”
BackgroundCapuchins’ (Cebus apella) sensitivity to others’ goal-directed actions in a helping context
Drayton, L. A., & Santos, L. R. (2013) · Animal Cognition · doi:10.1007/s10071-013-0700-5 · Cited by 40
“…longtailed macaques (Macaca fuscicularis): Massen et al. 2010, 2011; ravens (Corvus corax): Di Lascio et al. 2013; rhesus macaques (Macaca mulatta): Chang et al. 2011], comparative psychologists have looked primarily to two primate species—chimpanzees and brown capuchin monkeys—to more carefully…”
BackgroundIsoda, M. (2021) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-101420-011820 · Cited by 38
Capuchin monkeys, Cebus apella, show no evidence for inequity aversion in a costly choice task
McAuliffe, K., Chang, L. W., Leimgruber, K. L., Spaulding, R., Blake, P. R., & Santos, L. R. (2015) · Animal Behaviour · doi:10.1016/j.anbehav.2015.02.014 · Cited by 38
Animal Cognition: Monkeys Pass the Mirror Test
Toda, K., & Platt, M. L. (2015) · Current Biology · doi:10.1016/j.cub.2014.12.005 · Cited by 35
Multimodal cues displayed by submissive rats promote prosocial choices by dominants
Gachomba, M. J. M., Esteve-Agraz, J., Caref, K., Maroto, A. S., Bortolozzo-Gleich, M. H., Laplagne, D. A., & Márquez, C. (2022) · Current Biology · doi:10.1016/j.cub.2022.06.026 · Cited by 35
Interplay between the oxytocin and opioid systems in regulating social behaviour
Putnam, P. T., & Chang, S. W. C. (2022) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2021.0050 · Cited by 33
“In non-human primates, oxytocin increases time spent looking at faces [35,36], improves socially reinforced learning [37], increases the frequency of gaze following behaviours [38] and promotes the donation of rewards to social partners [39,40].”
BackgroundAnimal Paradigms to Assess Cognition with Translation to Humans
Wallace, T. L., Ballard, T. M., & Glavis-Bloom, C. (2015) · Handbook of Experimental Pharmacology · doi:10.1007/978-3-319-16522-6_2 · Cited by 26
A neuronal reward inequity signal in primate striatum
Báez-Mendoza, R., van Coeverden, C., & Schultz, W. (2015) · Journal of Neurophysiology · doi:10.1152/jn.00321.2015 · Cited by 25
“Previous and present behavioral results suggest that rhesus monkeys may be sensitive to reward for other monkeys (Azzi et al. 2012; Chang et al. 2011).”
ResultModel-Observer Similarity, Error Modeling and Social Learning in Rhesus Macaques
Monfardini, E., Hadj‐Bouziane, F., & Meunier, M. (2014) · PLoS ONE · doi:10.1371/journal.pone.0089825 · Cited by 24
“Reward consumption may help simply by providing vicarious reinforcement, the processing of others’ gains known to influence decision in monkeys [15,65,66].”
BackgroundA Social Reinforcement Learning Hypothesis of Mutual Reward Preferences in Rats
Hernandez-Lallement, J., van Wingerden, M., Schäble, S., & Kalenscher, T. (2016) · Current topics in behavioral neurosciences · doi:10.1007/7854_2016_436 · Cited by 23
Mason, S. A., Premereur, E., Pelekanos, V., Emberton, A., Honess, P. E., & Mitchell, A. S. (2019) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2019.02.001 · Cited by 24
“Previous evidence shows that monkeys and other primates will benefit from vicarious learning about the positive experiences of their fellow cagemates and from humans (Chang et al., 2011; Darby and Riopelle, 1959; Falcone et al., 2012a, 2012b; Fogassi et al., 2005; Meunier et al., 2007; Myers, 1970; Snowdon and Boe, 20…”
BackgroundCoding of Self and Other’s Future Choices in Dorsal Premotor Cortex during Social Interaction
Cirillo, R., Ferrucci, L., Marcos, E., Ferraina, S., & Genovesio, A. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.07.030 · Cited by 23
“, 2014), and show altruistic behaviors (Chang et al., 2011).”
Vicarious Learning from Human Models in Monkeys
Falcone, R., Brunamonti, E., & Genovesio, A. (2012) · PLoS ONE · doi:10.1371/journal.pone.0040283 · Cited by 23
“Several researchers have begun to study social adaptation [20], vicarious rewards [21] and behaviors regarding self vs.”
BackgroundFerrucci, L., Nougaret, S., & Genovesio, A. (2019) · Scientific Reports · doi:10.1038/s41598-018-36803-4 · Cited by 21
Balint, Z. K., Raper, J., Michopoulos, V., Howell, L. H., Gunter, C., Bachevalier, J., & Sánchez, M. M. (2021) · PLoS ONE · doi:10.1371/journal.pone.0235946 · Cited by 18
“as mother-offspring bonds, social play, reciprocal prosocial interactions, strong family alliances that preserve the status in the social hierarchy, as well as social awareness (15-18).”
BackgroundDevelopment of social systems neuroscience using macaques
Isoda, M., Noritake, A., & Ninomiya, T. (2018) · Proceedings of the Japan Academy Series B · doi:10.2183/pjab.94.020 · Cited by 19
Neurons in primate prefrontal cortex signal valuable social information during natural viewing
Adams, G. K., Ong, W. S., Pearson, J. M., Watson, K. K., & Platt, M. L. (2021) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2019.0666 · Cited by 17
“Among the foraging behaviours, ‘group foraging’, ‘hold food in mouth’ and ‘retrieve from cheek pouch’ were particularly effective at attracting gaze to the video, consistent with the phenomenon of vicarious reinforcement [34].”
BackgroundA Brain‐To‐Brain Mechanism for Social Transmission of Threat Learning
Pan, Y., Vinding, M. C., Zhang, L., Lundqvist, D., & Olsson, A. (2023) · Advanced Science · doi:10.1002/advs.202304037 · Cited by 17
Leveraging Social Learning to Enhance Captive Animal Care and Welfare
Hopper, L. M. (2021) · Journal of Zoological and Botanical Gardens · doi:10.3390/jzbg2010003 · Cited by 17
Ferrucci, L., Nougaret, S., Falcone, R., Cirillo, R., Ceccarelli, F., & Genovesio, A. (2021) · Cerebral Cortex · doi:10.1093/cercor/bhab253 · Cited by 15
“For example, when 2 monkeys are sitting next to each other’s and the actor’s choice can lead to a different contingency of reward delivery, the choice of the actor monkey is shaped by the future recipient of the reward (Chang et al. 2011; Noritake et al. 2018).”
BackgroundSocial processing by the primate medial frontal cortex
Putnam, P. T., & Chang, S. W. C. (2021) · International review of neurobiology · doi:10.1016/bs.irn.2020.12.003 · Cited by 19
Monkeys Monitor Human Goals in a Nonmatch-to-Goal Interactive Task
Falcone, R., Brunamonti, E., Ferraina, S., & Genovesio, A. (2012) · PLoS ONE · doi:10.1371/journal.pone.0032209 · Cited by 15
“Nevertheless, M–M paradigm can be more adapted to study aspects such as the vicarious reinforcement [32] or the influence of social hierarchy on social interactions but new experimental designs should be developed and tested within the paradigm to investigate these topics.”
BackgroundRole of the social actor during social interaction and learning in human-monkey paradigms
Nougaret, S., Ferrucci, L., & Genovesio, A. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.05.004 · Cited by 14
Lu, H. J., & Chang, L. (2018) · Evolutionary Psychology · doi:10.1177/1474704918797031 · Cited by 13
Putnam, P. T., Chu, C.-C. J., Fagan, N. A., Monte, O. D., & Chang, S. W. C. (2023) · Neuron · doi:10.1016/j.neuron.2023.05.020 · Cited by 12
“To quantify social decision preferences, we constructed a choice preference index as contrast ratios 27,35,38,44,45 (Equation 1).”
InfluentialPutnam, P. T., & Chang, S. W. C. (2021) · Behavioural Brain Research · doi:10.1016/j.bbr.2021.113356 · Cited by 11
The Vicarious Brain: Integrating Empathy and Emotional Learning
Olsson, A., & Spring, V. L. (2018) · Elsevier eBooks · doi:10.1016/b978-0-12-805397-3.00002-4 · Cited by 13
From affective to cognitive processing: Functional organization of the medial frontal cortex
Simon, J., Rudebeck, P. H., & Rich, E. L. (2021) · International review of neurobiology · doi:10.1016/bs.irn.2020.11.011 · Cited by 14
Egalitarian reward contingency in competitive games and primate prefrontal neuronal activity
Hosokawa, T., & Watanabe, M. (2015) · Frontiers in Neuroscience · doi:10.3389/fnins.2015.00165 · Cited by 9
“…behavioral studies indicating that non-human primates care about what the other subject obtained (Brosnan and De Waal, 2003; Brosnan et al., 2005; Chang et al., 2011; Azzi et al., 2012), monkeys in the present study appeared to be interested in whether or not the opponent obtained a reward.”
BackgroundVicarious reward unblocks associative learning about novel cues in male rats
van Gurp, S., Hoog, J., Kalenscher, T., & van Wingerden, M. (2020) · eLife · doi:10.7554/elife.60755 · Cited by 10
“In monkeys it was furthermore found that cues that are associated with reward delivery to another monkey were preferred over cues that were associated with juice delivery to a chair with no monkey in it and this preference was absent, in the non-social condition, when there was only a juice bottle present (Chang et al…”
Prosociality and reciprocity in capybaras (Hydrochoerus hydrochaeris) in a non-reproductive context
Lalot, M., Liévin‐Bazin, A., Bourgeois, A., Jalme, M. S., & Bovet, D. (2021) · Behavioural Processes · doi:10.1016/j.beproc.2021.104407 · Cited by 8
Neural populations in macaque anterior cingulate cortex encode social image identities
Simon, J., & Rich, E. L. (2024) · Nature Communications · doi:10.1038/s41467-024-51825-5 · Cited by 6
“Gaze following can impact future decisions related to the information in the focus of shared attention 18,19 , and is a conserved tendency across primate species found in both adult and infant humans as well as monkeys 17,20 – 22 .”
How dopamine guides our social world
Padilla-Coreano, N., & Martínez-Rivera, F. J. (2025) · Pharmacological Reviews · doi:10.1016/j.pharmr.2025.100085 · Cited by 6
Autonomic arousal tracks outcome salience not valence in monkeys making social decisions.
Basile, B. M., Joiner, J. A., Monte, O. D., Fagan, N. A., Karaskiewicz, C. L., Lucas, D. R., Chang, S. W. C., & Murray, E. A. (2021) · Behavioral Neuroscience · doi:10.1037/bne0000424 · Cited by 6
Brain games: Toward a neuroecology of social behavior
Gariépy, J., Chang, S. W. C., & Platt, M. L. (2013) · Behavioral and Brain Sciences · doi:10.1017/s0140525x12001938 · Cited by 5
Evolutionary Perspective on Prosocial Behaviors in Nonhuman Animals
Takimoto-Inose, A. (2021) · Springer eBooks · doi:10.1007/978-981-16-2028-7_12 · Cited by 5
Short-Term Reciprocity in Macaque’s Social Decision-Making
Ballesta, S., Reymond, G., & Duhamel, J. (2019) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2019.00225 · Cited by 4
“In fact, in many other ethically accepted social neuroscience studies, non-human primates has already proven their ability to express coherent socio-cognitive behaviors (Chang et al., 2011; Haroush and Williams, 2015; Yoshida et al., 2011) that were consistent with naturally occurring social behaviors (Ballesta and Du…”
BackgroundSpecialized medial prefrontal-amygdala coordination in other-regarding decision preferencePreprint
Monte, O. D., Chu, C.-C. J., Fagan, N. A., & Chang, S. W. C. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/640292 · Cited by 7
Meisner, O. C., Monte, O. D., Fagan, N., Nandy, A. S., & Chang, S. W. C. (2025) · Journal of Neuroscience · doi:10.1523/jneurosci.2416-24.2025 · Cited by 4
Horn, L., Bugnyar, T., & Massen, J. J. M. (2023) · Ethology · doi:10.1111/eth.13420 · Cited by 5
Emotional Learning and Regulation in Social Situations
Olsson, A., Undeger, I., & Yi, J. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-800935-2.00012-9 · Cited by 4
Jovanovic, V., Fishbein, A. R., de la Mothe, L. A., Lee, K., & Miller, C. T. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.11.01.466818 · Cited by 4
“Indeed, the mere presence of conspecifics can affect primate decision-making (Chang et al., 2011, 2013), while simply watching conspecific social interactions as a third-party observer has been shown to change the response properties of face cells (McMahon et al., 2015).”
Oxytocin and opioid antagonists: A dual approach to improving social behavior
Monte, O. D., Gangopadhyay, P., Putnam, P. T., & Chang, S. W. C. (2025) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.15376 · Cited by 3
“96 Moreover, OT can improve socially reinforced learning, 97 modulate prosocial preferences, 98,99 and affect social hierarchy.”
Ventromedial prefrontal cortex lesions disrupt learning to reward others
Gueguen, M., Cutler, J., Drew, D., Apps, M. A. J., Jeyaretna, D. S., Husain, M., Manohar, S., & Lockwood, P. L. (2025) · Brain · doi:10.1093/brain/awaf056 · Cited by 4
“Employing prosocial reinforcement learning paradigms similar to the one used here, further studies have shown that monkey ACCg neurons selectively activate for pro-social rewards 77,78 and that ACC lesions cause animals to become unable to learn to benefit another monkey over no one.”
In mixed company: two macaws are self-regarding in a symbolic prosocial choice task
Leete, J., & Vonk, J. M. (2022) · Behavioral Ecology and Sociobiology · doi:10.1007/s00265-021-03123-z · Cited by 3
Vicarious reward unblocks associative learning about novel cues in male ratsPreprint
van Gurp, S., Hoog, J., Tobias Kalenscher, A., & van Wingerden, M. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/612697 · Cited by 3
“Monkeys, for example, prefer cues that are associated with reward delivery to another 579 monkey over cues that were associated with juice delivery to a chair with no monkey in it and this preference was 580 absent, in the non-social condition, when there was only a juice bottle present (Chang et al., 2011).”
InfluentialSocial Value Unblocks Pavlovian Reinforcement Learning in Male RatsPreprint
van Gurp, S., Hoog, J., Kalenscher, T., & van Wingerden, M. (2019) · SSRN Electronic Journal · doi:10.2139/ssrn.3382553 · Cited by 3
“Humans for example learn to respond faster to stimuli that become associated with positive social reinforcement [11] and monkeys choose stimuli that predicted a reward delivery to a conspecific more than the stimuli that predicted no reward delivery [12].”
Metadata
- Authors
- Chang, S. W. C., Winecoff, A. A., & Platt, M. L.
- Affiliations
- Duke University (US)
- Corresponding author
- Chang, Steve W. C.
- Venue
- Frontiers in Neuroscience
- Publisher
- Frontiers Media SA
- Published
- 2011
- Volume
- 5
- Pages
- 27-27
- ISSN
- 1662-453X (ISSN-L)
- 1662-4548
- PMC
- PMC3080185
- OpenAlex
- W2088134342
- Cited by
- 124
- References
- 51
- Citations by year
- 2026: 4 · 2025: 5 · 2024: 2 · 2023: 7 · 2022: 7 · 2021: 17 · 2020: 5 · 2019: 10 · 2018: 6 · 2017: 3 · 2016: 11 · 2015: 15 · 2014: 9 · 2013: 14 · 2012: 8
- FWCI
- 13.92
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- cc-by
- Locations
- Frontiers in Neuroscience (publishedVersion, cc-by)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- National Institute of Mental Health (R01MH086712, R01MH095894)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Primate Behavior and Ecology
- Social Sciences › Psychology › Developmental and Educational Psychology › Child and Animal Learning Development
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Keywords
- vicarious reinforcement, rhesus monkeys, social learning, potential outcomes, observational learning, cooperation, attention to others, classical conditioning, operant conditioning, reward valuation, group decision making
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
