The DOI matches its Crossref record; 148 of the 148 references it cites were found in a registry or an index.
Neuroethology of primate social behavior
Open accessAbstract
A neuroethological approach to human and nonhuman primate behavior and cognition predicts biological specializations for social life. Evidence reviewed here indicates that ancestral mechanisms are often duplicated, repurposed, and differentially regulated to support social behavior. Focusing on recent research from nonhuman primates, we describe how the primate brain might implement social functions by coopting and extending preexisting mechanisms that previously supported nonsocial functions. This approach reveals that highly specialized mechanisms have evolved to decipher the immediate social context, and parallel circuits have evolved to translate social perceptual signals and nonsocial perceptual signals into partially integrated social and nonsocial motivational signals, which together inform general-purpose mechanisms that command behavior. Differences in social behavior between species, as well as between individuals within a species, result in part from neuromodulatory regulation of these neural circuits, which itself appears to be under partial genetic control. Ultimately, intraspecific variation in social behavior has differential fitness consequences, providing fundamental building blocks of natural selection. Our review suggests that the neuroethological approach to primate behavior may provide unique insights into human psychopathology.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“It has also been suggested that individual differences in social behavior result in part from differences in the neuromodulatory regulation of neural circuits 6 .”
From Oxytocin modulates social value representations in the amygdala (2019) · cites this paper as [6]
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 [6]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
Influence of life stress on depression: moderation by a polymorphism in the 5-HTT gene
Caspi, A., Sugden, K., Moffitt, T. E., Taylor, A., Craig, I. W., Harrington, H., McClay, J., Mill, J., Martin, J., Braithwaite, A., et al. (2003) · Science · doi:10.1126/science.1083968 · Cited by 8,120
Sociobiology: The New Synthesis.
Lenski, G. E., & Wilson, E. O. (1976) · Social Forces · doi:10.2307/2576242 · Cited by 6,271
Five Rules for the Evolution of Cooperation
Nowak, M. A. (2006) · Science · doi:10.1126/science.1133755 · Cited by 5,894
Physiology and neurobiology of stress and adaptation: central role of the brain
McEwen, B. S. (2007) · Physiological Reviews · doi:10.1152/physrev.00041.2006 · Cited by 5,429 · cited 1×
“Hormones strongly influence brain development (102, 103) and shape the expression of fundamental behaviors like feeding, fleeing, fighting, and mating (104).”
BackgroundOptimal foraging, the marginal value theorem
Charnov, E. L. (1976) · Theoretical Population Biology · doi:10.1016/0040-5809(76)90040-x · Cited by 5,374
Social Relationships and Health.
Cohen, S. (2004) · American Psychologist · doi:10.1037/0003-066x.59.8.676 · Cited by 4,852
Empathy for Pain Involves the Affective but not Sensory Components of Pain
Singer, T., Seymour, B., O'Doherty, J., Kaube, H., Dolan, R. J., & Frith, C. D. (2004) · Science · doi:10.1126/science.1093535 · Cited by 3,929
Oxytocin increases trust in humans
Kosfeld, M., Heinrichs, M., Zak, P. J., Fischbacher, U., & Fehr, E. (2005) · Nature · doi:10.1038/nature03701 · Cited by 3,690
Wingfield, J. C., Hegner, R. E., Dufty, & Ball, G. F. (1990) · The American Naturalist · doi:10.1086/285134 · Cited by 2,330
The expensive-tissue hypothesis: The brain and the digestive system in human and primate evolution
Aiello, L. C., & Wheeler, P. (1995) · Current Anthropology · doi:10.1086/204350 · Cited by 2,291
Flagged first, then by citations
Research works printed but not linked: 4
- JM Allman Evolving Brains (Scientifc American Library, New York, 1999).
- BB Smuts, DL Cheney, RM Seyfarth, RW Wrangham, TT Struhsaker Primate Societies (Univ of Chicago Press, Chicago, 1987).
- DW Stephens, JR Krebs Foraging Theory (Princeton Univ Press, Princeton, 1986).
- R Plomin Behavioral Genetics (Worth, 4th Ed, New York, 2001).
Cited by
Sorted by citations
Items 101–157 of 157
Laser stimulation of the skin for quantitative study of decision-making and motivation
Pai, J., Ogasawara, T., Bromberg-Martin, E. S., Ogasawara, K., Gereau, R. W., & Monosov, I. E. (2022) · Cell Reports Methods · doi:10.1016/j.crmeth.2022.100296 · Cited by 9
“However, in some contexts, the naturalistic qualities of other non-nociceptive stimuli may be desirable or required (Adams et al., 2012; Ahmadlou et al., 2021; Anderson and Perona, 2014; Bigot et al., 2022; Chang et al., 2013; Friedman et al., 2017; McCall et al., 2017; Menegas et al., 2017; Mobbs et al., 2018; Nambur…”
BackgroundNeural mechanisms of predicting individual preferences based on group membership
Vijayakumar, S., Hartstra, E., Mars, R. B., & Harold Bekkering, A. (2020) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsaa136 · Cited by 7
“Many of the regions identified here are present in some form in other primates (Rushworth et al., 2012; Chang et al., 2013).”
BackgroundPrimate Sex and Its Role in Pleasure, Dominance and Communication
Clarke, E., Bradshaw, K., Drissell, K., Kadam, P., Rutter, N., & Vaglio, S. (2022) · Animals · doi:10.3390/ani12233301 · Cited by 6
“Knowledge of reproductive physiology of species and specific life histories of study populations [42], along with data on change in neuromodulator hormones like oxytocin, vasopressin, and oestrogen, which are related to experiential pleasure [43], are necessary for a meaningful inclusion of pleasure in research.”
BackgroundIn the light of evolution VII: The human mental machinery
Cela‐Conde, C. J., Lombardo, R. G., Avise, J. C., & Ayala, F. J. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1307207110 · Cited by 6
Matsumoto, J., Kaneko, T., Kimura, K., Negrete, S. B., Guo, J. Y., Suda‐Hashimoto, N., Kaneko, A., Morimoto, M., Nishimaru, H., Setogawa, T., et al. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.09.13.556332 · Cited by 6
A Unique Case of Adoption in Golden Snub-Nosed Monkeys
Zhao, H., Li, J., Wang, Y., Li, N., Pan, R. L., & Li, B. (2024) · Animals · doi:10.3390/ani14213075 · Cited by 5
“This complex social framework suggests the need for exceptional spatial memory, intelligence, and recognition abilities to manage social and individual challenges similar to those humans face [19].”
BackgroundSlumber under pressure: REM sleep and stress response
Schaefke, B., Li, J., Zhao, B., Wang, L., & Tseng, Y.-T. (2025) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2025.102771 · Cited by 6
Sauciuc, G.-A., Persson, T., & Madsen, E. A. (2022) · Comparative Cognition & Behavior Reviews · doi:10.3819/ccbr.2022.170003 · Cited by 7
Tricoche, L., d’Halluin, M. R., Meunier, M., & Pélisson, D. (2024) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsae079 · Cited by 5
“This attention network has been included in the brain models of social behavior only recently (Chang et al. 2013, Patel et al. 2019).”
Chang, S. W. C., & Platt, M. (2014) · Current Biology · doi:10.1016/j.cub.2014.08.044 · Cited by 6
Self-citationMentalizing in Nonhuman Primates
Arre, A. M., & Santos, L. R. (2021) · Springer eBooks · doi:10.1007/978-3-030-51890-5_7 · Cited by 5
The Effects of Social Experience on the Stress System and Immune Function in Nonhuman Primates
Kohn, J. N., Panagiotakopoulos, L., & Neigh, G. N. (2016) · Developments in primatology · doi:10.1007/978-3-319-30872-2_4 · Cited by 5
Gurvich, C., & Thomas, N. (2021) · Brain Sciences · doi:10.3390/brainsci11030318 · Cited by 5
Bethell, E., Kemp, C., Thatcher, H. R., Schroeder, J., Arbuckle, K., Farningham, D. A. H., Witham, C., Holmes, A., MacLarnon, A. M., & Semple, S. (2019) · doi:10.32942/osf.io/5nzd4 · Cited by 5
Exploring rodent prosociality: A conceptual framework
Charron, V., Talbot, J., & Plamondon, H. (2025) · Translational Neuroscience · doi:10.1515/tnsci-2025-0375 · Cited by 3
“Prosocial behaviors have been studied in many animals, ranging from humans [19] to non-human primates [20,21], rodents [22], avians [23], invertebrates [24], and fi shes [25].”
Religion in the Emergence of Civilization: Çatalhöyük as a Case Study
Whitley, D. S. (2014) · Time and Mind · doi:10.1080/1751696x.2014.935150 · Cited by 4
Schwartz, P. J. (2024) · Frontiers in Psychology · doi:10.3389/fpsyg.2024.1427816 · Cited by 4
“…adaptive complex behavioral traits is the focus of ongoing theoretical and experimental research (Tosches, 2017; Barrett and Finlay, 2018; Seoane, 2020) and has been specifically investigated in relation to the evolution of dPAG defensive functions in non-human primates (Chang et al., 2013).”
BackgroundGroup-specific social dynamics affect urinary oxytocin levels in Taï male chimpanzees
Anna, P., Liran, S., Tobias, D., Catherine, C., & Roman, W. (2019) · Cambridge University Press eBooks · doi:10.1017/9781108674218.022 · Cited by 3
Social Curiosity in MonkeysPreprint
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
“…primates, which live in large and often hierarchically organized societies, where processing social information for the purpose of learning and socializing can be just as critical to survival as processing information about the nature of food resources (Mitani et al., 2012; Chang et al., 2013).”
Self-citationKing, S. B., & Singh, M. (2023) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1010966 · Cited by 2
Chhetala, S., Adhikari, R. B., Subedi, J. R., & Ghimire, T. R. (2025) · Health Science Reports · doi:10.1002/hsr2.71568 · Cited by 2
Zhou, W., Wang, Y., Ge, D., Yang, Q., Song, G., Cheng, J., Tian, T., Zhang, Y., Xu, J., Liu, Y., et al. (2026) · Biological Conservation · doi:10.1016/j.biocon.2026.111905 · Cited by 2
“Natural Laboratory Complex” for novel primate neuroscience
Iriki, A., & Tramacere, A. (2022) · Frontiers in Integrative Neuroscience · doi:10.3389/fnint.2022.927605 · Cited by 2
Group specific social dynamics affect urinary ocytocin levels in Tai male chimpanzees
Preis, A., Samuni, L., Deschner, T., Crockford, C., & Wittig, R. M. (2019) · MPG.PuRe (Max Planck Society) · Cited by 2
Social context alters metacognitionPreprint
Mahmoodi, A., Ringwald, K. G., Wittmann, M. K., & Mehring, C. (2019) · doi:10.31234/osf.io/ez8qw · Cited by 2
Royo, J., Orset, T., Catani, M., Pouget, P., & de Schotten, M. T. (2025) · Journal of Neuroscience · doi:10.1523/jneurosci.1646-24.2025 · Cited by 4
“The parallels between squirrel monkeys and humans suggest an evolutionary continuity in the neural substrates of social dominance (Adolphs and Birmingham, 2012; Kumaran et al., 2012; Chang et al., 2013; Watanabe and Yamamoto, 2015; Yokoyama et al., 2021; Oesch, 2024).”
Psychedelic studies in nonhuman primates: Past and future
Masthay, J. C., Kwan, A. C., & Chang, S. W. C. (2025) · Molecular Psychiatry · doi:10.1038/s41380-025-03240-5 · Cited by 2
“NHP studies could serve as an important component of this investigation and allow researchers to explore potential neural mechanisms underlying psychedelic-induced social effects, as NHPs display complex social repertoires and share many neural substrates of social behavior with humans [140, 141].”
Self-citationA multi-dimensional transfer learning framework for studying reward-guided behaviors across species
Liu, Y. M., Turnbull, A. G., Adeli, E., Zhao, G., Wang, K. H., & Lin, F. V. (2025) · Nature Mental Health · doi:10.1038/s44220-025-00547-8 · Cited by 1
“Nonetheless, AI-powered analysis of animal physiology, such as monitoring changes in heart rate or pupil dilation, which have been used in human research 98,99 , may enhance our understanding of reward-guided responses in the context of animal foraging or social bonding 95,100–102 .”
Parkinson, C. M., & Wheatley, T. P. (2016) · Behavioral and Brain Sciences · doi:10.1017/s0140525x15001600 · Cited by 1
Dando, M. (2020) · Advanced sciences and technologies for security applications · doi:10.1007/978-3-030-53790-6_9 · Cited by 1
Passingham, R. E. (2021) · Oxford University Press eBooks · doi:10.1093/oso/9780198844570.003.0003 · Cited by 1
Kozieł, S. M., Ignasiak, Z., Ignasiak, Z., Rokita, A., Cichy, I., Dutkowski, A., Ściślak, M., Kochan, K., Spinek, A. E., Spinek, A., et al. (2023) · Anthropological Review · doi:10.18778/1898-6773.85.4.06 · Cited by 2
“For example, OT was found to increase envy and gloating (Shamay-Tsoory 2009), decrease trust and the inclination to cooperate in individuals with borderline personality disorder (Bartz et al. 2011), and facilitate out-group derogation (De Dreu et al. 2011).”
BackgroundInfluentialBauman, M. D., Crawley, J. N., & Berman, R. F. (2019) · Wiley eBooks · doi:10.1002/9780470015902.a0022368.pub2 · Cited by 1
Fan, S., Monte, O. D., Nair, A. R., Fagan, N., & Chang, S. W. C. (2024) · SSRN Electronic Journal · doi:10.2139/ssrn.4683180 · Cited by 1
Self-citationRoyo, J., Orset, T., Catani, M., Pouget, P., & de Schotten, M. T. (2024) · Research Square · doi:10.21203/rs.3.rs-4772053/v1 · Cited by 1
Foraging for Information in the Prefrontal Cortex
Adams, G. K. (2014) · DukeSpace (Duke University)
Self-citationKozieł, S. M., Kociuba, M., Ignasiak, Z., Rokita, A., Cichy, I., Dutkowski, A., Ściślak, M., Kochan, K., Sebastjan, A., Spinek, A. E., et al. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.11.30.403592
“With growing number of investigations on the effects of oxytocin on behaviour, cognition, and neuropsychiatry, it is becoming clear that its functions are far more complex than initially was presumed [9,10].”
BackgroundGrooming interactions and cooperation in wild Barbary macaques (Macaca sylvanus)
Molesti, S. (2014) · Lincoln Repository (University of Lincoln) · doi:10.24385/lincoln.24327271
大村, 剛., 跡部, 一., 片山, 進., 渡辺, 肇., 平川, 舜., 百瀬, 和., 前田, 陽., 小野, 真., 清水, 雅., 井出, 忠., et al. (1985) · 日本臨床細胞学会雑誌
Sauciuc, G.-A., Persson, T., & Madsen, E. A. (2021) · OSF Preprints (OSF Preprints) · doi:10.31219/osf.io/3v4dr · Cited by 1
Scheun, J., & Gulson, J. (2019) · Springer eBooks · doi:10.1007/978-3-319-47829-6_1406-1
A Neuroetholical Study of Human Behavior in the Context of Meditation in Religions
Jurjewicz, H. (2017) · Communications - Scientific letters of the University of Zilina · doi:10.26552/com.c.2017.1.69-74
“b) Open-Monitoring Meditation Mindfulness necessitates a meditator to concentrate every sound or sight and track inner self-talk and internal bodily sensations [19].”
BackgroundMontgomery, E. B. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-822829-6.00026-6
Scheun, J., & Gulson, J. (2022) · Springer eBooks · doi:10.1007/978-3-319-55065-7_1406
Wise, S. P. (2023) · doi:10.1093/oso/9780192868398.003.0017
Tricoche, L., d’Halluin, M. R., Meunier, M., & Pélisson, D. (2024) · doi:10.31219/osf.io/umrax
Periodic Fasting: Evolutionary Perspectives Explaining the Clinical Benefits
Pijl, H. (2024) · Springer eBooks · doi:10.1007/978-3-031-49622-6_8
The case for a primary social drive: Revisiting definitions for primary drives
Christoffersen, M. (2025) · Acta Psychologica · doi:10.1016/j.actpsy.2025.104696
Social behavior in primates and its neural correlates
Qi, G., & Chang, S. W. C. (2025) · Elsevier eBooks · doi:10.1016/b978-0-443-27380-3.00002-6
Self-citationNakamura, M., Sato, T., Kurotani, T., Sakai, K., Hadjiev, A. M., Sasai, S., Mimura, K., Kawai, N., Shimmura, T., & Ichinohe, N. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.11.17.688777
Contributions of nonhuman primate research to unraveling the social brain and its impairments
Gacoin, M., Jiang, H., Obliger-Debouche, M., Cléry, J. C., & Sliwa, J. (2025) · Revue de primatologie · doi:10.4000/15cqb · Cited by 1
Clarifying the neural circuit mechanisms of spontaneous social behavior in macaques
Ninomiya, T., Kaneko, T., Ono, Y., Kobayashi, K., & Isoda, M. (2026) · Frontiers in Neural Circuits · doi:10.3389/fncir.2026.1783133
“…information by observing others’ eye gaze and facial expressions, and exhibit a rich repertoire of social behaviors in both natural and laboratory environments (Emery et al., 1997; Chang et al., 2013; Nakamichi, 2016; Hayashi et al., 2020), making them well suited for social neuroscience research.”
Circuits neuronaux sous-tendant la régulation émotionnelle par le système ocytocinergique
Goyon, S. (2018) · theses.fr (ABES) · doi:10.70675/c8c9bec0z7b79z4826z862az93b128e1ada6
Assessing the Reinforcing Efficacy of Conspecific Social Videos in Rhesus MonkeysPreprint
Ramirez-Ovalle, G., Zaraza, D., & Grant, K. A. (2026) · Research Square · doi:10.21203/rs.3.rs-9839183/v1
Pomerantz, O., Day, A. M., Ojakangas, T. A., Cook, H. L., Ardeshir, A., & McCowan, B. (2026) · American Journal of Primatology · doi:10.1002/ajp.70224
Metadata
- Authors
- Chang, S. W. C., Brent, L. J. N., Adams, G. K., Klein, J. T., Pearson, J. M., Watson, K. K., & Platt, M. L.
- Affiliations
- Duke University (US)
- University of North Carolina at Chapel Hill (US)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2013-06-10
- Volume
- 110
- Issue
- supplement_2
- Pages
- 10387-10394
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC3690617
- OpenAlex
- W1999221289
- Cited by
- 157
- References
- 147
- Citations by year
- 2026: 5 · 2025: 10 · 2024: 11 · 2023: 8 · 2022: 15 · 2021: 11 · 2020: 11 · 2019: 20 · 2018: 15 · 2017: 9 · 2016: 13 · 2015: 10 · 2014: 12 · 2013: 6
- FWCI
- 20.25
- 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)
- Carolina Digital Repository (University of North Carolina at Chapel Hill) (submittedVersion)
- UNC Libraries
- Funders
- U.S. Department of Defense (W81XWH1110584, W81XWH-11-1-, W81XWH)
- National Institutes of Health (5r00mh099093-04, 5f31mh081443-03, 5r01ey019303-04)
- National Institute of Mental Health (K99MH099093, R00-MH099093, MH089484, MH086712, R01MH086712, R01MH089484, F31-MH081443, R01MH096875, R01MH095894)
- National Eye Institute (R01-EY019303)
- National Institute of General Medical Sciences (T32GM008441)
- Congressionally Directed Medical Research Programs
- Topics
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Primate Behavior and Ecology
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Neuroendocrine regulation and behavior
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Evolutionary Psychology and Human Behavior
- Keywords
- neuroethology, primate social behavior, social cognition, brain evolution, neuromodulation, social motivation, social perception, genetic control of behavior, natural selection, non-human primates
- MeSH terms
- Animals, Animal Communication, Biological Evolution, Humans, Models, Biological, Nerve Net, Primates, Selection, Genetic, Social Behavior
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
