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Neuronal reference frames for social decisions in primate frontal cortex
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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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Effort shapes social cognition and behaviour: A neuro-cognitive framework
Contreras-Huerta, L. S., Pisauro, M. A., & Apps, M. A. J. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.08.003 · Cited by 91
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The role of temporal cortex in the control of attention
Ramezanpour, H., & Fallah, M. (2022) · Current Research in Neurobiology · doi:10.1016/j.crneur.2022.100038 · Cited by 76
“, 2012), anterior cingulate cortex (Chang et al., 2013; Yoshida et al., 2012; Haroush and Williams, 2015) have so far been considered to play a more important role when it comes to social action monitoring, action observation, and action execution.”
BackgroundNieder, A. (2018) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2016.0514 · Cited by 76
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
“Reward neurons distinguish between own and other’s reward (3, 4) and show differential activity during social competition (5) and movement (6).”
BackgroundDistinct neural representations for prosocial and self-benefiting effort
Lockwood, P. L., Wittmann, M. K., Nili, H., Matsumoto-Ryan, M., Abdurahman, A., Cutler, J., Husain, M., & Apps, M. A. J. (2022) · Current Biology · doi:10.1016/j.cub.2022.08.010 · Cited by 73
The social dilemma: prefrontal control of mammalian sociability
Yizhar, O., & Levy, D. R. (2021) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2021.01.007 · Cited by 76
Neural signatures of natural behaviour in socializing macaques
Testard, C., Tremblay, S., Parodi, F., DiTullio, R. W., Acevedo-Ithier, A., Gardiner, K. L., Kording, K. P., & Platt, M. L. (2024) · Nature · doi:10.1038/s41586-024-07178-6 · Cited by 85
Self-citationChang, S. W. C., & Platt, M. L. (2014) · Brain Research · doi:10.1016/j.brainres.2013.11.006 · Cited by 71
“Moreover, not surprisingly, when given a choice between rewarding themselves only and the recipients only, the actor monkeys prefer to deliver juice almost exclusively to themselves (Chang et al., 2012, 2013a).”
BackgroundSelf-citationVicarious Reinforcement Learning Signals When Instructing Others
Apps, M. A. J., Lesage, E., & Ramnani, N. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.3669-14.2015 · Cited by 71
Endogenous opioids regulate social threat learning in humans
Haaker, J., Yi, J., Petrović, P., & Olsson, A. (2017) · Nature Communications · doi:10.1038/ncomms15495 · Cited by 71
Levels 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
Self-citationSocial Information Signaling by Neurons in Primate Striatum
Klein, J. T., & Platt, M. L. (2013) · Current Biology · doi:10.1016/j.cub.2013.03.022 · Cited by 72
“This plasticity notwithstanding, we believe that the medial-to-lateral organization of social and nutritive information coding is a general property of primate striatum for the following reasons: 1) human neuroimaging has found a similar topography [3–5, 7]; 2) the orbitofrontal cortex (OFC) and the anterior cingulate…”
Self-citationShank mutant mice as an animal model of autism
Yoo, J., Bakes, J., Bradley, C. A., Collingridge, G. L., & Kaang, B. (2013) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2013.0143 · Cited by 76
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“[64–73].”
Basile, 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
Self-citationIntegration of individual and social information for decision-making in groups of different sizes
Park, S. A., Goïame, S., O'Connor, D. A., & Dreher, J.-C. (2017) · PLOS Biology · doi:10.1371/journal.pbio.2001958 · Cited by 67
Jiang, Y., & Platt, M. L. (2018) · Scientific Reports · doi:10.1038/s41598-018-25607-1 · Cited by 69
Self-citationPrefrontal cortex interactions with the amygdala in primates
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“In contrast, the ACC contained three separate populations of neurons that signaled social outcomes: one that signaled rewards to self, another for rewards to a conspecific, and a third one with shared signaling of reward to self and the conspecific [222].”
BackgroundWhat makes the dorsomedial frontal cortex active during reading the mental states of others?
Isoda, M., & Noritake, A. (2013) · Frontiers in Neuroscience · doi:10.3389/fnins.2013.00232 · Cited by 64
“Very recently, a coordinate transformation approach has been proposed to account for such operations (Chang, 2013; Chang et al., 2013).”
BackgroundConserved features of anterior cingulate networks support observational learning across species
Burgos-Robles, A., Gothard, K. M., Monfils, M., Morozov, A., & Vicentic, A. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.09.009 · Cited by 64
“Support for these functions of the cingulate come from its activation during tasks that require the subjects to predict the (social) behaviors of others (Apps et al., 2013; Apps and Ramnani, 2014; Chang et al., 2013; de Araujo et al., 2012; Haroush and Williams, 2015).”
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
“…8 and emotional experiences of others 46 to support psychological processes including empathy 46 and social learning, in both monkeys and humans 8,47 Nevertheless, our observation that some neurons in ACCg encode strategic social information monkeys used to play chicken aligns with prior…”
Self-citationFace cells in orbitofrontal cortex represent social categories
Barat, E., Wirth, S., & Duhamel, J.-R. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1806165115 · Cited by 58
“In addition, neurons in the OFC are more sensitive to rewards when they are not shared, suggesting that they code the social context of a given reward (28).”
BackgroundBalsters, J. H., Mantini, D., Apps, M. A. J., Eickhoff, S. B., & Wenderoth, N. (2016) · NeuroImage: Clinical · doi:10.1016/j.nicl.2016.03.016 · Cited by 50
“Keywords: Autism Spectrum Disorder Cingulate cortex Resting state fMRI Meta-Analytic Connectivity Modeling”
BackgroundPrefrontal Contribution to Decision-Making under Free-Choice Conditions
Funahashi, S. (2017) · Frontiers in Neuroscience · doi:10.3389/fnins.2017.00431 · Cited by 68
“Recently, prefrontal single-neuron activities have been examined in social and real competitive conditions of two monkeys (Yoshida et al., 2012; Chang et al., 2013; Haroush and Williams, 2015).”
BackgroundAnterior Cingulate Cortex Signals Attention in a Social Paradigm that Manipulates Reward and Shock
Schneider, K. N., Sciarillo, X. A., Nudelman, J. L., Cheer, J. F., & Roesch, M. R. (2020) · Current Biology · doi:10.1016/j.cub.2020.07.039 · Cited by 58
“In monkey ACC, neurons fire when reward is allocated to a conspecific, to oneself, or in both contexts [24].”
Monte, O. D., Fan, S., Fagan, N. A., Chu, C.-C. J., Zhou, M. B., Putnam, P. T., Nair, A. R., & Chang, S. W. C. (2022) · Neuron · doi:10.1016/j.neuron.2022.04.013 · Cited by 55
Self-citationPezzulo, G., Iodice, P., Ferraina, S., & Kessler, K. (2013) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2013.00800 · Cited by 54
“Neural modulation for self and other reward outcome expectation/monitoring has been shown in different areas of the frontal lobe of primates (Chang et al., 2013) and the estimate of self/other motivational variables have been proposed to act as a gain modulation during common FOR generation (Chang,…”
BackgroundJovanovic, 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
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Evolution, Emotion, and Episodic Engagement
Pine, D. S., Wise, S. P., & Murray, E. A. (2021) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2020.20081187 · Cited by 52
Comparative connectomics of the primate social brain
Yokoyama, C., Autio, J. A., Ikeda, T., Sallet, J., Mars, R. B., Essen, D. C. V., Glasser, M. F., Sadato, N., & Hayashi, T. (2021) · NeuroImage · doi:10.1016/j.neuroimage.2021.118693 · Cited by 44
“Electrophysiological recordings and fMRI studies in macaques have revealed distinct contributions of the different subdivisions of the mPFC region to social cognition, from social valuation, to processing social interactions, to social communication and learning from others (Chang et al., 2013; Haroush and Williams, 2…”
BackgroundOne cranium, two brains not yet introduced: Distinct but complementary views of the social brain
Prounis, G. S., & Ophir, A. G. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.11.011 · Cited by 46
“For example, compared to other regions of the ACC, a relatively large proportion of neurons in the ACCg of macaques respond solely to the reward outcome of others in a modified dictator game (Chang et al., 2013).”
BackgroundSeven computations of the social brain
Molapour, T., Hagan, C. C., Silston, B., Wu, H., Ramstead, M. J. D., Friston, K. J., & Mobbs, D. (2021) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsab024 · Cited by 44
“Moreover, neuroimaging studies in humans suggest an important division between social and nonsocial subregions within the ACC, namely the sulcus (ACCs) and gyrus (ACCg) (Chang et al., 2013; Apps et al., 2016; Joiner et al., 2017; Kendal et al., 2018).”
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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