Shared neural coding for social hierarchy and reward value in primate amygdala
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The social brain hypothesis posits that dedicated neural systems process social information. In support of this, neurophysiological data have shown that some brain regions are specialized for representing faces. It remains unknown, however, whether distinct anatomical substrates also represent more complex social variables, such as the hierarchical rank of individuals within a social group. Here we show that the primate amygdala encodes the hierarchical rank of individuals in the same neuronal ensembles that encode the rewards associated with nonsocial stimuli. By contrast, orbitofrontal and anterior cingulate cortices lack strong representations of hierarchical rank while still representing reward values. These results challenge the conventional view that dedicated neural systems process social information. Instead, information about hierarchical rank—which contributes to the assessment of the social value of individuals within a group—is linked in the amygdala to representations of rewards associated with nonsocial stimuli. New data reveal that the amygdala—a brain area specialized for emotion—also signals the hierarchical rank of peers in a social group. These neural signals likely mediate appropriate social and emotional behavior in many social settings.
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Neurons sensitive to the rank of the individual being viewed in the social hierarchy are found in the macaque amygdala, OFC, and anterior cingulate cortex.
“Neurons that are sensitive to the rank of the individual being viewed in the social hierarchy are found not only in the macaque amygdala, but also in the closely connected OFC, and anterior cingulate cortex (Munuera et al., 2018).”
From The orbitofrontal cortex: reward, emotion and depression (2020) · cites this paper as Munuera et al., 2018
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“Indeed, one recent result suggests that neural ensembles in the amygdala that encode the value of CSs also encode information about the hierarchical rank of conspecifics within a social group (48).”
BackgroundShared yet dissociable neural codes across eye gaze, valence and expectation
Pryluk, R., Shohat, Y., Morozov, A., Friedman, D., Taub, A. H., & Paz, R. (2020) · Nature · doi:10.1038/s41586-020-2740-8 · Cited by 35 · see citing works
Isaac, J., Karkare, S. C., Balasubramanian, H., Schappaugh, N., Javier, J. L., Rashid, M., & Murugan, M. (2024) · Nature Communications · doi:10.1038/s41467-024-52294-6 · Cited by 32 · see citing works
Two brains in action: Joint-action coding in the primate frontal cortex
Ferrari-Toniolo, S., Visco‐Comandini, F., & Battaglia‐Mayer, A. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.1512-18.2019 · Cited by 31 · see citing works
“Therefore, the relevance of these neurons in social cognition might reside in allowing coordinated motor interactions among individuals, because being social implies, among other cognitive attitudes, to be able to flexibly adjust the own action to that of another conspecific (Munuera et al., 2018).”
BackgroundNeuronal Circuits for Social Decision-Making and Their Clinical Implications
Báez-Mendoza, R., Vázquez, Y., Mastrobattista, E. P., & Williams, Z. M. (2021) · Frontiers in Neuroscience · doi:10.3389/fnins.2021.720294 · Cited by 32 · see citing works
The impact of sociality and affective valence on brain activation: A meta-analysis
Atzil, S., Satpute, A. B., Zhang, J., Parrish, M. H., Shablack, H., MacCormack, J. K., Leshin, J. C., Goel, S. S., Brooks, J. A., Kang, J., et al. (2023) · NeuroImage · doi:10.1016/j.neuroimage.2023.119879 · Cited by 30 · see citing works
“We first tested whether sociality and valence could themselves be classified in broad-scale brain patterns since past findings are inconsistent on this point (Chavez and Heatherton, 2015; Lindquist et al., 2016; Munuera et al., 2018).”
BackgroundPrefrontal circuits guiding social preference: Implications in autism spectrum disorder
Fortier, A. V., Meisner, O. C., Nair, A. R., & Chang, S. W. C. (2022) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2022.104803 · Cited by 30 · see citing works
“In a study investigating representation of social hierarchy and reward value in macaques, researchers found that the same subpopulation of amygdala neurons encoded both social hierarchy and reward association information in social and nonsocial reward tasks (Munuera et al., 2018).”
BackgroundNoritake, A., Ninomiya, T., & Isoda, M. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.02.018 · Cited by 29 · see citing works
Neurobiological Bases of Social Networks
Han, M., Jiang, G., Luo, H., & Shao, Y. (2021) · Frontiers in Psychology · doi:10.3389/fpsyg.2021.626337 · Cited by 35 · see citing works
Shi, W., Meisner, O. C., Blackmore, S., Jadi, M. P., Nandy, A. S., & Chang, S. W. C. (2023) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2023.107793 · Cited by 27 · see citing works
“Under social behavioral contexts, the amygdala has been found to encode a variety of social variables including social cues (Bergan et al., 2014) and social values (Grabenhorst et al., 2019; Munuera et al., 2018) involved in learning and decision-making.”
BackgroundMethodInterconnected neural circuits mediating social reward
Isaac, J., & Murugan, M. (2024) · Trends in Neurosciences · doi:10.1016/j.tins.2024.10.004 · Cited by 25 · see citing works
The Neural Circuit Architecture of Social Hierarchy in Rodents and Primates
Ferreira‐Fernandes, E., & Peça, J. (2022) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2022.874310 · Cited by 20 · see citing works
Functions of primate amygdala neurons in economic decisions and social decision simulation
Grabenhorst, F., & Schultz, W. (2021) · Behavioural Brain Research · doi:10.1016/j.bbr.2021.113318 · Cited by 18 · see citing works
“As described above, amygdala neurons are more strongly involved in processing social hierarchy information than neurons in orbitofrontal cortex and anterior cingulate cortex [58].”
BackgroundInfluentialMesoscopic-scale functional networks in the primate amygdala
Morrow, J. K., Cohen, M. X., & Gothard, K. M. (2020) · eLife · doi:10.7554/elife.57341 · Cited by 19 · see citing works
“…things further, an increasing number of single unit studies reported that neurons in the amygdala respond to multiple stimulus dimensions and task parameters ( Kyriazi et al., 2018 ; Morrow et al., 2019 ; Munuera et al., 2018 ; Putnam and Gothard, 2019 ; Saez et al., 2015 ; Gothard, 2020 ).”
BackgroundPettine, W. W., Louie, K., Murray, J. D., & Wang, X. (2021) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1008791 · Cited by 22 · see citing works
Pujara, M. S., Ciesinski, N. K., Reyelts, J. F., Rhodes, S. E. V., & Murray, E. A. (2022) · Journal of Neuroscience · doi:10.1523/jneurosci.0794-21.2022 · Cited by 19 · see citing works
Kelly, E. A., Thomas, V. K., Indraghanty, A., & Fudge, J. L. (2021) · Journal of Neuroscience · doi:10.1523/jneurosci.1056-21.2021 · Cited by 18 · see citing works
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 · see citing works
“Studies carried out in non-human primates have shown responsiveness of individual OFC neurons to faces [43,44] and distinguished images in biologically relevant social categories twice as readily as representing juice volume [13].”
BackgroundMidline thalamic inputs to the amygdala: Ultrastructure and synaptic targets
Amir, A., Paré, J., Smith, Y., & Paré, D. (2018) · The Journal of Comparative Neurology · doi:10.1002/cne.24557 · Cited by 16 · see citing works
Organization 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 17 · see citing works
A Multiparadigm Approach to Characterize Dominance Behaviors in CD1 and C57BL6 Male Mice
Cum, M., Pérez, J. A. S., Iwata, R. L., Lopez, N., Higgs, A., Li, A., Ye, C., Wangia, E., Wright, E. S., Restrepo, C. G., et al. (2024) · eNeuro · doi:10.1523/eneuro.0342-24.2024 · Cited by 19 · see citing works
“Similarly in nonhuman primates, social rank impacts how the amygdala and frontal cortex respond to social cues (Hu et al., 2016; Munuera et al., 2018).”
Newmyer, B. A., Whindleton, C. M., Klein, P., Beenhakker, M. P., Jones, M., & Scott, M. M. (2019) · JCI Insight · doi:10.1172/jci.insight.126283 · Cited by 15 · see citing works
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 18 · see citing works
Tang, H., Bartolo, R., & Averbeck, B. B. (2024) · Neuron · doi:10.1016/j.neuron.2024.08.018 · Cited by 14 · see citing works
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 · see citing works
“It has been shown that the amygdala volume is positively correlated with increasing social ranks [54] and that individual amygdala neurons encode social ranks and reward values in overlapping manners [55].”
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 · see citing works
Putnam, P. T., & Chang, S. W. C. (2021) · Behavioural Brain Research · doi:10.1016/j.bbr.2021.113356 · Cited by 11 · see citing works
“images, the authors were able to demonstrate that same neuronal ensembles that encoded reward values were also encoding dominance hierarchies [14].”
BackgroundInfluentialSocial status as a latent variable in the amygdala of observers of social interactions
Lee, S., Rutishauser, U., & Gothard, K. M. (2024) · Neuron · doi:10.1016/j.neuron.2024.09.010 · Cited by 12 · see citing works
“45 When the observers and the observed have a history of interactions, conditioning can explain the status-related responses.”
Ahmed, N., Headley, D. B., & Paré, D. (2021) · Journal of Neurophysiology · doi:10.1152/jn.00253.2021 · Cited by 10 · see citing works
The Perspective from Cognitive Neuroscience
Kemmerer, D. L. (2019) · Oxford University Press eBooks · doi:10.1093/oso/9780190682620.003.0002 · Cited by 10 · see citing works
Folloni, D., Verhagen, L., Mars, R. B., Fouragnan, E. F., Constans, C., Aubry, J., Rushworth, M. F. S., & Sallet, J. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/342303 · Cited by 10 · see citing works
The big mixup: Neural representation during natural modes of primate visual behavior
Leopold, D. A. (2024) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2024.102913 · Cited by 8 · see citing works
“The amygdala is an important recipient and integrator of sensory and social information, with neurons responding to combinations of visual, auditory and somatosensory input [50] as well as a mixture of social and cognitive variables [37,51,52].”
BackgroundMilewski, T. M., Lee, W., Young, R. L., Hofmann, H. A., & Curley, J. P. (2025) · PLoS Genetics · doi:10.1371/journal.pgen.1011548 · Cited by 7 · see citing works
Is this worth the trouble? Strategic conflict management in Tonkean macaques
Ballesta, S., & Meunier, H. (2023) · iScience · doi:10.1016/j.isci.2023.108176 · Cited by 7 · see citing works
Beyond faces: the contribution of the amygdala to visual processing in the macaque brain
Taubert, J., Wardle, S. G., Patterson, A., & Baker, C. I. (2024) · Cerebral Cortex · doi:10.1093/cercor/bhae245 · Cited by 6 · see citing works
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 · see citing works
Social 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 6 · see citing works
Evaluations from Superiors Matter More: Evidence from Behavior and Event-related Potentials
Duan, R., Li, Z., Hu, J., Li, P., & Warren, C. M. (2022) · Journal of Cognitive Neuroscience · doi:10.1162/jocn_a_01894 · Cited by 5 · see citing works
Qu, C., Huang, Y., Philippe, R., Cai, S., Derrington, E. A., Moisan, F., Shi, M., & Dreher, J. (2024) · Communications Biology · doi:10.1038/s42003-024-05976-2 · Cited by 5 · see citing works
“Keeping Up with the Joneses”: Subjective Social Status Predicts Proactive Coping
Archibald, J. L., & Neupert, S. D. (2022) · Journal of Adult Development · doi:10.1007/s10804-022-09392-w · Cited by 5 · see citing works
“Consistent with primate research where rank within hierarchies greatly influences quality of life (Sapolsky, 2005) and access to resources (Bercovitch, 1991; Munuera et al., 2018), perceptions of one’s social status within their local community predicts efforts to meet future challenges and successfully adapt.”
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 · see citing works
Utilizing social foraging as a framework to study decisions in groups
Garg, K., Deng, W., & Mobbs, D. (2026) · iScience · doi:10.1016/j.isci.2026.114940 · Cited by 4 · see citing works
“168 However, other evidence suggests specialized mechanisms underlying social processes.”
Dwortz, M. F., & Curley, J. P. (2025) · Neuroscience · doi:10.1016/j.neuroscience.2025.05.025 · Cited by 4 · see citing works
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 · see citing works
Neuronal Mechanisms Underlying Face Recognition in Non‐human Primates
Amita, H., Koyano, K. W., & Kunimatsu, J. (2024) · Japanese Psychological Research · doi:10.1111/jpr.12530 · Cited by 4 · see citing works
Dynamic coding and sequential integration of multiple reward attributes by primate amygdala neurons
Fabian Grabenhorst, B., & Báez-Mendoza, R. (2025) · Nature Communications · doi:10.1038/s41467-025-58270-y · Cited by 6 · see citing works
“Previous studies showed that primate amygdala neurons signal changing values in individual and social learning contexts 1,2,9,12,16 – 18 , and code subjective values based on multiple attributes during immediate and longer-term economic choices 10,11,13,19 .”
Pettine, W. W., Louie, K., Murray, J. D., & Wang, X. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.01.28.923649 · Cited by 5 · see citing works
“…has recently arisen that takes into account the multiple brain areas implicated in decisions (Wunderlich, Rangel, and O’Doherty 2009; Peck, Lau, and Salzman 2013; Paton et al. 2006; Munuera, Rigotti, and Salzman 2018; Louie and Glimcher 2010; Chen and Stuphorn 2015; Steinmetz et al. 2019).”
BackgroundPrefrontal and Subcortical c-Fos Mapping of Reward Responses across Competitive and Social Contexts
Almeida, C. D. P. C., Cum, M., Illescas-Huerta, E., Chambers, A. R., Ye, C., Shah, A., Jain, A., Li, A., & Padilla-Coreano, N. (2025) · eNeuro · doi:10.1523/eneuro.0158-25.2025 · Cited by 2 · see citing works
“Interestingly, a study in nonhuman primates demonstrated that BLA neurons that encode social rank overlap with those that encode reward (Munuera et al., 2018).”
Decision-Making with Predictions of Others’ Likely and Unlikely Choices in the Human Brain
Ma, N., Harasawa, N., Ueno, K., Cheng, K., & Nakahara, H. (2024) · Journal of Neuroscience · doi:10.1523/jneurosci.2236-23.2024 · Cited by 3 · see citing works
Folloni, D., Roumazeilles, L., Bryant, K., Manger, P. R., Bertelsen, M. F., Khrapitchev, A. A., Rudebeck, P. H., & Mars, R. B. (2026) · Journal of Neuroscience · doi:10.1523/jneurosci.0377-25.2026 · Cited by 3 · see citing works
Munuera, J. (2018) · Journal of Experimental Neuroscience · doi:10.1177/1179069518782459 · Cited by 3 · see citing works
Prefrontal–Amygdala Pathways for Object and Social Value Representation
Pujara, M. S., & Murray, E. A. (2024) · Journal of Cognitive Neuroscience · doi:10.1162/jocn_a_02144 · Cited by 2 · see citing works
Can we tackle climate change by behavioral hacking of the dopaminergic system?
Munuera, J., & Burguière, E. (2022) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2022.996955 · Cited by 2 · see citing works
“Since the DA system has also been identified in social behavior encoding (Klein and Platt, 2013; Gunaydin et al., 2014; Munuera et al., 2018), using social strategies to curve climate change sounds like a valid approach.”
BackgroundNeuronal response of the primate striatum tail to face of socially familiar persons
Kunimatsu, J., Amita, H., & Hikosaka, O. (2024) · iScience · doi:10.1016/j.isci.2024.110043 · Cited by 2 · see citing works
“44 In this study,weusedimagesof thefaces of individuals who had beencaringfor themonkeysdaily forover a year.”
Maladaptive learning and the amygdala—prefrontal circuit
Likhtik, E., & Paz, R. (2019) · Elsevier eBooks · doi:10.1016/b978-0-12-813983-7.00021-5 · Cited by 2 · see citing works
Shared neural codes for eye-gaze and valencePreprint
Pryluk, R., Shohat, Y., Morozov, A., Friedman, D., Taub, A. H., & Paz, R. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/736462 · Cited by 2 · see citing works
Scheggia, D., Greca, F. L., Maltese, F., Carrano, N., Luca, M. D., & Papaleo, F. (2021) · Research Square · doi:10.21203/rs.3.rs-404701/v1 · Cited by 2 · see citing works
The role of the amygdala in processing social and affective touchPreprint
Gothard, K. M., & Fuglevand, A. J. (2021) · doi:10.31234/osf.io/un9gs · Cited by 2 · see citing works
“For example, in monkeys, the same neurons respond to the magnitude of rewards received and to the social status of familiar conspecifics [27] or to combinations of task-related vigilance, face identity, and reward amount [28].”
BackgroundHow Do Language-Specific Concepts Relate to Cognition?
Kemmerer, D. L. (2019) · Oxford University Press eBooks · doi:10.1093/oso/9780190682620.003.0006 · Cited by 1 · see citing works
Czoty, P. W., Kawas, M. I., Madi, K. V., Barcus, R. A., Kim, J., Hudson, J. P., Galbo, L. K., Yuan, H., Daunais, J. B., & Whitlow, C. T. (2025) · Cerebral Cortex · doi:10.1093/cercor/bhaf043 · Cited by 1 · see citing works
“To date, brain imaging studies in monkeys have largely agreed with human data in implicating the prefrontal cortex, amygdala and ventral striatum in the representation of social dominance (eg Sallet et al.2011; Noonan et al.2014; Munuera et al. 2018).”
Lee, S. G., Dormán, H., Nádasdy, Z., & Gothard, K. M. (2026) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2516365123 · Cited by 1 · see citing works
Liu, J., Qu, C., Philippe, R., Li, S. S., Derrington, E. A., Corgnet, B., & Dreher, J.-C. (2026) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2606871123 · Cited by 2 · see citing works
The Perspective from Semantic Typology
Kemmerer, D. L. (2019) · Oxford University Press eBooks · doi:10.1093/oso/9780190682620.003.0001 · Cited by 1 · see citing works
Computational Modeling of Basic Cognitive Functionalities
(2023) · Cambridge University Press eBooks · doi:10.1017/9781108755610.014 · Cited by 1 · see citing works
Doya, K. (2025) · Elsevier eBooks · doi:10.1016/b978-0-443-15754-7.00088-2 · Cited by 1 · see citing works
Are We Ever Conscious of Concepts?
Kemmerer, D. L. (2019) · Oxford University Press eBooks · doi:10.1093/oso/9780190682620.003.0007
Multisensory Processing in the Primate Amygdala
Morrow, J. K. (2019) · UA Campus Repository (The University of Arizona)
Visual add-ons during vertebrate evolution
Pfaff, D. W. (2020) · Elsevier eBooks · doi:10.1016/b978-0-323-85861-8.00014-1
Layered Synchronization and Identification of Uncertain Delayed Hierarchical Networks
Chai, Y., & Zhang, H. (2021) · Mathematical Problems in Engineering · doi:10.1155/2021/8890949
“Constantly left in varied conditions, many complex networks comprise multilevel structures and multicomponent systems [12], and stereoscopic hierarchical network is one of them.”
BackgroundPrivacy, Neuroscience and Algorithms
Grant, D. (2021) · Cambridge University Press eBooks · doi:10.1017/9781108883931.003
Kelly, E., Thomas, V. K., Indraghanty, A., & Fudge, J. L. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.05.07.443119
“The same neural ensembles in monkey amygdala can code reward associated with both nonsocial and social stimuli (Munuera et al., 2018), indicating a common or overlapping circuitry available for coding ‘salience’ and ‘social’ cue evaluation.”
Background
- Authors
- Munuera, J., Rigotti, M., & Salzman, C. D.
- Affiliations
- Columbia University (US)
- IBM (United States) (US)
- New York State Psychiatric Institute (US)
- Corresponding author
- Munuera, Jérôme
- Salzman, C. Daniel
- Venue
- Nature Neuroscience
- Published
- 2018-02-19
- Volume
- 21
- Issue
- 3
- Pages
- 415-423
- ISSN
- 1097-6256 (ISSN-L)
- 1546-1726
- PMC
- PMC6092962
- OpenAlex
- W2789621216
- Cited by
- 126
- References
- 62
- Citations by year
- 2026: 9 · 2025: 17 · 2024: 17 · 2023: 7 · 2022: 12 · 2021: 22 · 2020: 12 · 2019: 25 · 2018: 5
- FWCI
- 21.66
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Nature Neuroscience (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Simons Foundation
- Philippe Foundation
- Fondation Fyssen
- National Institutes of Health
- National Institute of Mental Health (R01MH082017)
- National Eye Institute (P30EY019007)
- Topics
- Social Sciences › Psychology › Social Psychology › Primate Behavior and Ecology
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Face Recognition and Perception
- Keywords
- social hierarchy, hierarchical rank, amygdala, reward value, social brain hypothesis, orbitofrontal cortex, anterior cingulate cortex, primate social behavior, face processing
- MeSH terms
- Amygdala, Animals, Conditioning, Operant, Hierarchy, Social, Macaca mulatta, Male, Neurons, Photic Stimulation, Reward
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