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Neural mechanisms of social decision-making in the primate amygdala
Open accessAbstract
Significance: Making social decisions requires evaluation of benefits and costs to self and others. Long associated with emotion and vigilance, neurons in primate amygdala also signal reward and punishment as well as information about the faces and eyes of others. Here we show that neurons in the basolateral amygdala signal the value of rewards for self and others when monkeys make social decisions. These value-mirroring neurons reflected monkeys’ tendency to make prosocial decisions on a momentary as well as long-term basis. We also found that delivering the social peptide oxytocin into basolateral amygdala enhances both prosocial tendencies and attention to the recipients of prosocial decisions. Our findings endorse the amygdala as a critical neural nexus regulating social decisions.
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“In nonhuman primates, exogenous inhaled oxytocin promotes social donation behavior 26 and focal infusion of oxytocin into the amygdala significantly increases prosocial decisions 7 .”
From Oxytocin modulates social value representations in the amygdala (2019) · cites this paper as [7]
In the citing paper
“Individual differences in social preferences in nonhuman primates have been shown to be due in part to oxytocinergic regulation of amygdala-related neural circuits 6,7 .”
From Oxytocin modulates social value representations in the amygdala (2019) · cites this paper as [7]
In the citing paper
“This result is consistent with studies in both nonhuman primates 7 and in human neuroimaging studies 16 suggesting that the amygdala represents how undesirable an outcome is.”
From Oxytocin modulates social value representations in the amygdala (2019) · cites this paper as [7]
In the citing paper
“Moreover, we found evidence that social value distance is also encoded by neural responses in the ventral striatum and TPJ in prosocials, consistent with previous findings linking prosocial decisions with several hubs in the social brain network 7,36 , including the amygdala, ventral striatum and TPJ.”
From Oxytocin modulates social value representations in the amygdala (2019) · cites this paper as [7]
In the citing paper
“This is consistent with studies showing that the amygdala plays a critical role in allocating attention to other people 7 and in integrating social information 42 and social emotions 13 into decision-making.”
From Oxytocin modulates social value representations in the amygdala (2019) · cites this paper as [7]
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“Several recent studies have focused on the role of subcortical structures in social reward monitoring, such as the hypothalamus (Noritake et al. 2020) and the amygdala (Chang et al. 2015; Grabenhorst et al. 2019; Dal Monte et al. 2020).”
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
Self-citationDu, Y., He, L., Wang, Y., & Liao, D. (2022) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2022.854692 · Cited by 15
Djerdjaj, A., Ng, A. J., Rieger, N. S., & Christianson, J. P. (2022) · Behavioural Brain Research · doi:10.1016/j.bbr.2022.114050 · Cited by 15
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
Self-citationA view-based decision mechanism for rewards in the primate amygdala
Fabian Grabenhorst, B., Ponce‐Alvarez, A., Battaglia‐Mayer, A., Deco, G., & Schultz, W. (2023) · Neuron · doi:10.1016/j.neuron.2023.08.024 · Cited by 11
Putnam, 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].”
BackgroundInfluentialSelf-citationLiu, X., Cui, D., Li, D., Jiao, R., Wang, X., Jia, S., Hou, D., Li, T., Liu, H., Wang, P., et al. (2017) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2017.00327 · Cited by 12
“The amygdala and PC are major targets of the olfactory system and have close interactions with the SON in social recognition (Chang et al., 2015).”
BackgroundNeural 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
A Context-Dependent Switch From Sensing to Feeling in the Primate Amygdala
Martin, A. B., Cardenas, M. A., Andersen, R. K., Bowman, A. I., Hillier, E. A., Bensmaı̈a, S. J., Fuglevand, A. J., & Gothard, K. M. (2022) · Cell Reports · doi:10.1016/j.celrep.2023.112056 · Cited by 14
Kalenscher, T., Schönfeld, L.-M., Löbner, S., Wöhr, M., van Berkel, M., Zech, M.-P., & van Wingerden, M. (2021) · Language, cognition and mind · doi:10.1007/978-3-030-50200-3_19 · Cited by 11
Virtual social grooming in macaques and its psychophysiological effects
Disarbois, É., & Duhamel, J. (2024) · Scientific Reports · doi:10.1038/s41598-024-62638-3 · Cited by 10
“…interaction, one could suggest that vicarious processes could be at play, and engage similar mechanisms and brain circuits that have been found to support empathic responses to both painful and rewarding stimuli 26,27 , and the still poorly understood mechanisms involved in giving grooming 28 .”
BackgroundVardanjani, M. M., Ghasemian, S., Sheibani, V., & Mansouri, F. A. (2021) · Behavioural Brain Research · doi:10.1016/j.bbr.2021.113409 · Cited by 10
Interactive effects of OXTR and GAD1 on envy-associated behaviors and neural responses
Tanaka, T., Nishimura, F., Kakiuchi, C., Kasai, K., Kimura, M., & Haruno, M. (2019) · PLOS ONE · doi:10.1371/journal.pone.0210493 · Cited by 9
Steeper social discounting after human basolateral amygdala damage
Tobias Kalenscher, A., Lüpken, L. M., Stoop, R., Terburg, D., & van Honk, J. (2025) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2500692122 · Cited by 9
Role of Prefrontal Cortex Circuitry in Maintaining Social Homeostasis
Lee, S., & Williams, Z. M. (2024) · Biological Psychiatry · doi:10.1016/j.biopsych.2024.07.007 · Cited by 10
Latent goal models for dynamic strategic interaction
Iqbal, S., Yin, L., Drucker, C. B., Qian, K., Gariépy, J., Platt, M. L., & Pearson, J. M. (2019) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1006895 · Cited by 10
Self-citation5-HT1A receptor agonism in the basolateral amygdala increases mutual-reward choices in rats
Schönfeld, L.-M., Schäble, S., Zech, M.-P., & Tobias Kalenscher, A. (2020) · Scientific Reports · doi:10.1038/s41598-020-73829-z · Cited by 8
Douglas, H. M., Halverstadt, B. A., Reinhart-Anez, P., Webber, E. S., & Cromwell, H. C. (2018) · Behavioural Processes · doi:10.1016/j.beproc.2018.06.016 · Cited by 8
Methylation of OXT and OXTR genes, central oxytocin, and social behavior in female macaques
Leon, D. D., Nishitani, S., Walum, H., McCormack, K. M., Wilson, M. E., Smith, A. K., Young, L. J., & Sánchez, M. M. (2020) · Hormones and Behavior · doi:10.1016/j.yhbeh.2020.104856 · Cited by 7
Impact of internal and external factors on prosocial choices in rhesus macaques
Sallet, J., Emberton, A., Wood, J., & Rushworth, M. F. S. (2021) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2019.0678 · Cited by 6
“Moreover it is increased by local infusion of oxytocin into the amygdala [62].”
BackgroundSocial Risk Coding by Amygdala Activity and Connectivity with the Dorsal Anterior Cingulate Cortex
Kim, J.-C., Zangemeister, L., Tobler, P. N., Schultz, W., & Fabian Grabenhorst, B. (2024) · Journal of Neuroscience · doi:10.1523/jneurosci.1149-24.2024 · Cited by 7
Hwang, S., Meffert, H., VanTieghem, M., Sinclair, S., Bookheimer, S. Y., Vaughan, B. S., & Blair, J. (2018) · Clinical Psychopharmacology and Neuroscience · doi:10.9758/cpn.2018.16.4.449 · Cited by 8
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
Self-citationAghajani, M., Klapwijk, E. T., Colins, O. F., Ziegler, C., Domschke, K., Vermeiren, R. R. J. M., & van der Wee, N. J. A. (2018) · Biological Psychiatry: Cognitive Neuroscience and Neuroimaging · doi:10.1016/j.bpsc.2017.12.010 · Cited by 21
The amygdala and the pursuit of future rewards
Johnson, S. T., & Fabian Grabenhorst, B. (2025) · Frontiers in Neuroscience · doi:10.3389/fnins.2024.1517231 · Cited by 4
Mentalizing in Nonhuman Primates
Arre, A. M., & Santos, L. R. (2021) · Springer eBooks · doi:10.1007/978-3-030-51890-5_7 · Cited by 5
Faykoo-Martinez, M., Mooney, S. J., & Holmes, M. M. (2018) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2018.00272 · Cited by 6
“For example, manipulation of OT signaling alters multiple social behaviors including prosociality/aggression, social recognition, short-term social memory, alloparenting, and pup care (Ferguson et al., 2000, 2001; Francis et al., 2000; Champagne et al., 2001; Consiglio et al., 2005; Olazábal and Young, 2006a,b; Choler…”
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
Self-citationMeisner, 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
Self-citation
Metadata
- Authors
- Chang, S. W. C., Fagan, N. A., Toda, K., Utevsky, A. V., Pearson, J. M., & Platt, M. L.
- Affiliations
- Yale University (US)
- Duke University (US)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2015-12-14
- Volume
- 112
- Issue
- 52
- Pages
- 16012-16017
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC4702988
- OpenAlex
- W2217623521
- Cited by
- 157
- References
- 69
- Citations by year
- 2026: 5 · 2025: 19 · 2024: 14 · 2023: 6 · 2022: 15 · 2021: 19 · 2020: 16 · 2019: 18 · 2018: 21 · 2017: 12 · 2016: 11
- FWCI
- 24.06
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- HHS | NIH | National Institute of Mental Health (R00-MH099093, R01-MH095894)
- DOD | Army Research Office (W81XWH-11-1-0584)
- Japan Society for the Promotion of Science (No number)
- HHS | NIH | National Institute of Environmental Health Sciences (K01-ES-025442)
- Topics
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- social decision-making, amygdala, basolateral amygdala, oxytocin, dictator game, prosocial behavior, reward valuation, punishment, social preferences, neuromodulation, primate social behavior
- MeSH terms
- Animals, Choice Behavior, Cues, Decision Making, Humans, Macaca mulatta, Markov Chains, Models, Neurological, Monte Carlo Method, Neural Pathways, Neurons, Oxytocics, Oxytocin, Reward, Social Behavior, Basolateral Nuclear Complex
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