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Neuronal reference frames for social decisions in primate frontal cortex
Open accessAbstract
Social decisions are crucial for the success of individuals and the groups that they comprise. Group members respond vicariously to benefits obtained by others, and impairments in this capacity contribute to neuropsychiatric disorders such as autism and sociopathy. We examined the manner in which neurons in three frontal cortical areas encoded the outcomes of social decisions as monkeys performed a reward-allocation task. Neurons in the orbitofrontal cortex (OFC) predominantly encoded rewards that were delivered to oneself. Neurons in the anterior cingulate gyrus (ACCg) encoded reward allocations to the other monkey, to oneself or to both. Neurons in the anterior cingulate sulcus (ACCs) signaled reward allocations to the other monkey or to no one. In this network of received (OFC) and foregone (ACCs) reward signaling, ACCg emerged as an important nexus for the computation of shared experience and social reward. Individual and species-specific variations in social decision-making might result from the relative activation and influence of these areas.
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“Prior investigations in rodents and primates, for example, have provided evidence for the presence of neurons that encode information about other individuals, demonstrating changes in activity when the animals observe another’s appetitive or aversive experiences 1–11.”
From Reduced sociability and social agency encoding in adult Shank3-mutant mice are restored through gene re-expression in real time (2021) · cites this paper as [2]
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“Previous investigations have provided insight into how discrete aspects of another animal’s experience, such as receipt of reward, may be encoded by cells 1–7,9.”
From Reduced sociability and social agency encoding in adult Shank3-mutant mice are restored through gene re-expression in real time (2021) · cites this paper as [2]
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“We have previously shown that videos promote interactive looking behaviors, e.g., eye contact, gaze-following, gaze-avoidance, and the reciprocation of facial expressions [12-17] as they better approximate natural interactions [18-20].”
From Neurons in the Monkey Amygdala Detect Eye Contact during Naturalistic Social Interactions (2014) · cites this paper as [18]
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Báez-Mendoza, R., Vázquez, Y., Mastrobattista, E. P., & Williams, Z. M. (2021) · Frontiers in Neuroscience · doi:10.3389/fnins.2021.720294 · Cited by 34
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“…learning (Etkin et al., 2011; Neubert et al., 2015), is active during social approach behaviors in rodents (Lee et al., 2016) and during prosocial preference behaviors and viewing of social interactions between conspecifics in nonhuman primates (Chang et al., 2013a; Sliwa and Freiwald, 2017).”
BackgroundSelf-citationCoordinate transformation approach to social interactions
Chang, S. W. C. (2013) · Frontiers in Neuroscience · doi:10.3389/fnins.2013.00147 · Cited by 31
“…(KingCasas et al., 2005; Moll et al., 2006; Behrens et al., 2008, 2009; Mobbs et al., 2009; Jeon et al., 2010; Yoshida et al., 2011, 2012; Azzi et al., 2012; Carter et al., 2012; Hillman and Bilkey, 2012; Kishida and Montague, 2012; Nicolle et al., 2012; Watson and Platt, 2012; Chang et al., 2013).”
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Gabay, A. S., & Apps, M. A. J. (2020) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsaa037 · Cited by 26
“Indeed, there is considerable evidence that there is overlap in the mechanisms that guide self-benefitting and other-oriented decisions, even if there are some dissociations (Zaki and Mitchell, 2011; Chang et al., 2013; Wittmann et al., 2018; Piva et al., 2019).”
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MethodSelf-citationProsocial behaviors in rodents
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“…error signals specifically when subjects learn to benefit others (Lockwood et al., 2016), and single-neuron recordings in rhesus macaques, Macaca mulatta , revealed that a high proportion of neurons in the ACCg exclusively responded to reward delivered to a conspecific (Chang et al., 2013).”
BackgroundSocial monitoring of actions in the macaque frontopolar cortex
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BackgroundMethodSickness and the Social Brain: How the Immune System Regulates Behavior across Species
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Entorhinal transformations in abstract frames of reference
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Neural responses underlying extraordinary altruists’ generosity for socially distant others
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BackgroundFairness influences early signatures of reward-related neural processing
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“ACCg activity, on the other hand, is linked to shared experience and social reward, since neurons in the ACCg encoded reward allocations to another monkey, to oneself or to both (Chang et al., 2013).”
BackgroundMethodInfluentialZhang, X., Yan, X., Stylli, J., & Platt, M. L. (2021) · Transportation Research Part F Traffic Psychology and Behaviour · doi:10.1016/j.trf.2021.05.010 · Cited by 20
Self-citationDeng, S., Tan, S., Guo, C., Liu, Y., & Li, X. (2024) · Frontiers in Neuroscience · doi:10.3389/fnins.2024.1391191 · Cited by 19
“Numerous studies have indicated that the mPFC exhibits heightened activity during social bonding in rodent species (Lee et al., 2016), social preference behavior in non-human primates (Chang et al., 2013), and observations of social interactions among conspecific animals (Sliwa and Freiwald, 2017).”
BackgroundAgent-specific learning signals for self–other distinction during mentalising
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BackgroundDamage to the Ventromedial Prefrontal Cortex Impairs Learning from Observed Outcomes
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“Our experimental paradigm, therefore, differs from previous studies in the field of social decision-making that have examined how individuals learn from and imitate the behavior of intelligent social agents (Sanfey 2007; Hampton et al. 2008; Behrens et al. 2009; Burke et al. 2010; Seo and Lee 2012; Boorman et al. 2013…”
BackgroundResultElectrophysiological signatures of inequity-dependent reward encoding in the human OFC
Marciano, D., Staveland, B. R., Lin, J. J., Sáez, I., Hsu, M., & Knight, R. T. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.112865 · Cited by 20
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Ontogenetic Ritualization of Primate Gesture as a Case Study in Dyadic Brain Modeling
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“OFC and anterior cingulate (ACC) neurons, in a separate but similarly 'interactive' study, were shown to differentially process how rewards were allocated between others and oneself, with ACC gyrus appearing important for processing the 'shared experience' of rewards (Chang et al. 2012).”
InfluentialCompetitive and cooperative games for probing the neural basis of social decision-making in animals
Wang, H., & Kwan, A. C. (2023) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105158 · Cited by 18
“There is emerging evidence that monkeys and rodents would exhibit pro-or anti-social choices for other animals that are otherwise absent (Chang et al., 2013; Haroush and Williams, 2015; Hernandez-Lallement et al., 2014; Marquez et al., 2015).”
Another in need enhances prosociality and modulates frontal theta oscillations in young adults
Lavín, C., Soto‐Icaza, P., López, V., & Billeke, P. B. (2023) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2023.1160209 · Cited by 19
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Tavoni, G., Cocco, S., & Monasson, R. (2016) · Journal of Computational Neuroscience · doi:10.1007/s10827-016-0617-5 · Cited by 18
“This observation suggests that PFC could play a role in the representation of reward, together with adjacent frontal areas, where reward-related activity has been reported (Chang et al. 2013).”
BackgroundOrganization of parietoprefrontal and temporoprefrontal networks in the macaque
Giarrocco, F., & Averbeck, B. B. (2021) · Journal of Neurophysiology · doi:10.1152/jn.00092.2021 · Cited by 18
Cost-benefit analysis: the first real rule of fight club?
Hillman, K. L. (2013) · Frontiers in Neuroscience · doi:10.3389/fnins.2013.00248 · Cited by 17
“Other-referenced valuations predominate in the ACC gyrus (Chang et al., 2013), a region previously shown to be important in conspecific-based learning (Behrens et al., 2008).”
BackgroundMethodInfluentialReward and decision processes in the brains of humans and nonhuman primates
Sirigu, A., & Duhamel, J. (2016) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2016.18.1/asirigu · 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
“…of spatial information that occurs in reference frames such as eye-centered or bodycentered coordinates (Andersen et al. 1997, Cohen and Andersen 2002), neurons representing others can also be seen as working in reference frames, not only self-centered but also other-centered (Chang 2013, 2017).”
BackgroundMethodInfluentialLuo, F., Deng, J.-Y., Sun, X., Zhen, J., & Luo, X.-D. (2023) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2220353120 · Cited by 14
Social 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
“…i.e. processing a reward in a “self-oriented” or “other-oriented” reference frame is theorized to be supported by a coordinate transformation framework (Chang, 2013), analogous to how distinctly referenced information is transformed from one frame of reference to another to perform sensorimotor…”
BackgroundSelf-citationStrategic Motives Drive Proposers to Offer Fairly in Ultimatum Games: An fMRI Study
Chen, Y.-H., Chen, Y., Kuo, W., Kan, K., Yang, C., & Yen, N. (2017) · Scientific Reports · doi:10.1038/s41598-017-00608-8 · Cited by 17
Aly-Mahmoud, M., Carlier, P., Salam, S. A., Selmani, M. H., Moftah, M. Z., Esclapez, M., & Boussaoud, D. (2017) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2017.00082 · Cited by 18
“Furthermore, neuronal recordings in monkeys have shown that neurons in the prefrontal cortex and basal ganglia code the social value of reward (Chang et al., 2013), and monitor others’ actions and their outcomes (Yoshida et al.”
BackgroundScaling Our World View: How Monoamines Can Put Context Into Brain Circuitry
Stratmann, P., Albu‐Schäffer, A., & Jörntell, H. (2018) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2018.00506 · Cited by 14
Pupil Correlates of Decision Variables in Mice Playing a Competitive Mixed-Strategy Game
Wang, H., Ortega, H. K., Atilgan, H., Murphy, C. E., & Kwan, A. C. (2022) · eNeuro · doi:10.1523/eneuro.0457-21.2022 · Cited by 17
“…spiking activity patterns that suggest neural representations of various decision variables in prefrontal cortical regions, lateral intraparietal cortex, and amygdala (Barraclough et al., 2004; Chang et al., 2013; Dal Monte et al., 2020; Haroush and Williams, 2015; Seo et al., 2007, 2009).”
BackgroundCircuit-Based Approaches to Understanding the Anterior Cingulate Cortex (ACC)
Myers, D. C., Simon, J. R., Oh, J., Kabotyanski, K. E., Fujimoto, S., Oathes, D., Rudebeck, P., Amemori, K., Sheth, S., & Fudge, J. (2025) · Journal of Neuroscience · doi:10.1523/jneurosci.1311-25.2025 · Cited by 12
Neuroimaging of human and non-human animal emotion and affect in the context of social relationships
Zablocki-Thomas, P. B., Rogers, F. D., & Bales, K. L. (2022) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2022.994504 · Cited by 13
Socially relative reward valuation in the primate brain
Isoda, M. (2020) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2020.11.008 · Cited by 13
“The ACCg plays a causal role in the valuation of social signals [57] and contains neurons signaling which monkey — self or other — receives a reward [29].”
Neural basis of cooperative behavior in biological and artificial intelligence systems
Jiang, M., Gu, L., Ma, M., Li, Q., Kao, J. C., & Hong, W. (2025) · Science · doi:10.1126/science.adw8151 · Cited by 12
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
“27 Similarly, neuroimaging in humans revealed that ACC, especially the gyrus subregion (ACCg), represents another individual’s rewarding events, 25 and its activation level changes as a function of trait-level empathy.”
InfluentialSelf-citationMohammadi, Z., Ashwood, Z. C., & Pillow, J. W. (2025) · Nature Communications · doi:10.1038/s41467-025-66738-0 · Cited by 19
“Incorporating data from various brain areas 65,66 could enhance our understanding ofanimaldecision-making strategies.”
Bault, N., di Pellegrino, G., Puppi, M., Opolczynski, G., Monti, A., Braghittoni, D., Thibaut, F., Rustichini, A., & Coricelli, G. (2019) · Journal of Cognitive Neuroscience · doi:10.1162/jocn_a_01372 · Cited by 11
“Neurons of ACC, however, encoded either peers’ rewards or both the monkey’s own and its peers’ rewards (Chang et al., 2013), which is consistent with a role of these neurons in social comparison.”
ResultPutnam, P. T., & Chang, S. W. C. (2021) · Behavioural Brain Research · doi:10.1016/j.bbr.2021.113356 · Cited by 11
“Using this paradigm, the authors had previously demonstrated that monkeys prefer to donate liquid to the other monkey over no one, a behavior supported by vicarious social reward [28,30,80, 81,102].”
BackgroundSelf-citationMoral Dilemma Judgment Revisited: A Loreta Analysis
da Rocha, A. F., Rocha, F., & Massad, E. (2013) · Journal of Behavioral and Brain Science · doi:10.4236/jbbs.2013.38066 · Cited by 12
“Benefit and risk simulations are supposed to take profit of individual knowledge and their autobiographic history [17-20].”
Neural representation of others during action observation in posterior medial prefrontal cortex
Falcone, R., Cirillo, R., Ceccarelli, F., & Genovesio, A. (2021) · Cerebral Cortex · doi:10.1093/cercor/bhab499 · Cited by 11
Xu, T., Zhang, L., Zhou, F., Fu, K., Gan, X., Chen, Z., Zhang, R., Lan, C., Wang, L., Kendrick, K. M., et al. (2025) · Communications Biology · doi:10.1038/s42003-025-07561-7 · Cited by 15
“Finally, the OFC plays an important role in self-reference, including prioritized encoding of self-referenced rewards in PEs 30 .”
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
Balancing evidence and norms in cultural evolution
MacCoun, R. J. (2015) · Organizational Behavior and Human Decision Processes · doi:10.1016/j.obhdp.2014.09.009 · Cited by 10
Kim, K.-I., Jung, W. H., Woo, C., & Kim, H. (2022) · NeuroImage · doi:10.1016/j.neuroimage.2022.119355 · Cited by 10
Integrative Modeling of Prefrontal Cortex
Alexander, W. H., Vassena, E., Deraeve, J., & Langford, Z. D. (2017) · Journal of Cognitive Neuroscience · doi:10.1162/jocn_a_01138 · Cited by 12
“…& Brown, 2014) based on the PRO model, as well as tests of model predictions performed by other researchers (Jahn, Nee, Alexander, & Brown, 2014; Chang, Gariépy, & Platt, 2013; Talmi, Atkinson, & El-Deredy, 2013; Ferdinand, Mecklinger, Kray, & Gehring, 2012; Bryden, Johnson, Tobia, Kashtelyan,…”
Shaw, D. J., Czekóová, K., Gajdoš, M., Staněk, R., Špalek, J., & Brázdil, M. (2018) · Human Brain Mapping · doi:10.1002/hbm.24446 · Cited by 10
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
“…activities of the prefrontal cortex are reported to reflect the social context regarding whether an individual’s task performance is associated with only the individual’s own reward or with both the individual’s and a task-uninvolved partner’s rewards (Azzi et al., 2012; Chang et al., 2012).”
BackgroundSkirzewski, M., Molotchnikoff, S., Hernandez, L. F., & Maya‐Vetencourt, J. F. (2022) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2021.806376 · Cited by 9
Vázquez, D., Schneider, K. N., & Roesch, M. R. (2022) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2022.926388 · Cited by 11
“Recent work demonstrates that this is also true in the social domain (Machado and Bachevalier, 2006; Azzi et al., 2012; Chang et al., 2013).”
BackgroundInfluentialWu, Z., Jin, T., Chen, C., Liu, X., & Yan, J. (2023) · Traffic Injury Prevention · doi:10.1080/15389588.2023.2181078 · Cited by 9
Metadata
- Authors
- Chang, S. W. C., Gariépy, J.-F., & Platt, M. L.
- Affiliations
- Duke University (US)
- Corresponding author
- Chang, Steve W C
- Venue
- Nature Neuroscience
- Published
- 2012-12-23
- Volume
- 16
- Issue
- 2
- Pages
- 243-250
- ISSN
- 1097-6256 (ISSN-L)
- 1546-1726
- PMC
- PMC3557617
- OpenAlex
- W2025969629
- Cited by
- 336
- References
- 53
- Citations by year
- 2026: 19 · 2025: 36 · 2024: 16 · 2023: 24 · 2022: 25 · 2021: 54 · 2020: 18 · 2019: 15 · 2018: 23 · 2017: 21 · 2016: 20 · 2015: 21 · 2014: 20 · 2013: 24
- FWCI
- 10.66
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Canadian Institutes of Health Research (84765)
- National Institute of Mental Health (K99MH099093, MH095894, R00-MH099093, R01MH086712, R01MH095894)
- National Institute of Neurological Disorders and Stroke (T32NS051156)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Primate Behavior and Ecology
- Keywords
- social decision-making, orbitofrontal cortex, anterior cingulate cortex, neural coding, collective experience, autism spectrum disorder, sociopathy
- MeSH terms
- Action Potentials, Analysis of Variance, Animals, Brain Mapping, Decision Making, Gyrus Cinguli, Macaca mulatta, Male, Neurons, Photic Stimulation, Reward, Social Behavior, Prefrontal Cortex
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