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.
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“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
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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
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BackgroundMethodA neural substrate of prediction and reward
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“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).”
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“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,…”
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“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).”
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“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
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Research works printed but not linked: 1
- Sutton R. S. Barto A. G. (1998). Reinforcement Learning: An Introduction. London: MIT Press
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Joiner, J. A., Nair, A. R., Fagan, N. A., & Chang, S. W. C. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.11.15.516657 · Cited by 3
“Similarly, though it does not impact their own reward values or outcomes, animals find watching another animal receive rewards to be reinforcing as well, which is an example of vicarious reward (Bandura et al., 1963; Mobbs et al., 2009; Chang et al., 2011).”
Prefrontal–Amygdala Pathways for Object and Social Value Representation
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Neuroetología del comportamiento social de los primates
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Esteve-Agraz, J., Rodríguez-Milan, V. J., & Márquez, C. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.02.21.639526 · Cited by 1
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Functional Significance of Default Brain Activity Observed in Nonhuman Animals
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Jovanovic, V., Fishbein, A. R., de la Mothe, L. A., Lee, K., & Miller, C. T. (2021) · SSRN Electronic Journal · doi:10.2139/ssrn.3956813
Neural Basis of Empathy and Its Dysfunction in Autism Spectrum Disorders (ASD)
Platt, M. L. (2014) · Defense Technical Information Center (DTIC) · doi:10.21236/ada612863
A multi-brain mechanism for observational threat learningPreprint
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Anterior cingulate cortex neurons in macaques encode social image identitiesPreprint
Simon, J., & Rich, E. L. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.11.10.566537
“Gaze following can impact future decisions related to the information in the focus of shared attention 18,19 , and is a conserved trait across primate species, being found in both adult and infant humans as well as monkeys 17,20–22 .”
BackgroundInfluentialWhat’s Next if Reward is Enough? Insights for AGI from Animal Reinforcement Learning
Rajagopal, S. (2023) · Journal of Artificial General Intelligence · doi:10.2478/jagi-2023-0002
Comparative Game Theory: Bringing Ethology Back into Social Decision Neuroscience
Shi, W., Meisner, O. C., Jadi, M. P., Nandy, A. S., & Chang, S. W. C. (2026) · Springer eBooks · doi:10.1007/978-3-032-02925-6_27
The Anterior Cingulate Cortex and Prosocial Behavior toward Others in Negative State
Zhang, M., Rigney, N., Chang, S. W. C., & Hong, W. (2026) · Journal of Neuroscience · doi:10.1523/jneurosci.1105-25.2025 · Cited by 1
A Neurocomputational Model of Observation-Based Decision Making with a Focus on Trust
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“Reviewing these perspectives provides a basis for introducing a neurocomputational framework that links these two levels of analysis through a computational model.”
Bromberg-Martin, E. S., Merel, J., & Monosov, I. E. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.06.09.731206 · Cited by 1
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
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