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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.
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“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]
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“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]
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An Emerging Field of Primate Social Neurophysiology: Current Developments
Chang, S. W. C. (2017) · eNeuro · doi:10.1523/eneuro.0295-17.2017 · Cited by 21
Self-citationCheng, J. T., & Kornienko, O. (2020) · Springer eBooks · doi:10.1007/978-3-030-35784-9_22 · Cited by 20
Social network dynamics precede a mass eviction in group-living rhesus macaques
Larson, S. M., Ruiz-Lambides, A. V., Platt, M. L., & Brent, L. J. N. (2017) · Animal Behaviour · doi:10.1016/j.anbehav.2017.08.019 · Cited by 20
Self-citationNeuropsychological and socio–cognitive deficits in patients with obstructive sleep apnea
Macchitella, L., Romano, D. L., Marinelli, C. V., Toraldo, D. M., Arigliani, M., Benedetto, M. D., & Angelelli, P. (2021) · Journal of Clinical and Experimental Neuropsychology · doi:10.1080/13803395.2021.1944609 · Cited by 19
“…that similar neural and cognitive processes underlie both social and nonsocial cognition (e.g., Brown & Brüne, 2012; Callejas et al., 2014; Chang et al., 2013; Corbetta et al., 2008; Decety & Lamm, 2007; Greene et al., 2009; Krall et al., 2016; McKinnon & Moscovitch, 2007; Mitchell, 2008;…”
BackgroundAmygdala growth from youth to adulthood in the macaque monkey
Schumann, C. M., Scott, J. A., Lee, A., Bauman, M. D., & Amaral, D. G. (2019) · The Journal of Comparative Neurology · doi:10.1002/cne.24728 · Cited by 18
“Much like humans, rhesus macaques live in complex social groups and have evolved a sophisticated social communication system that includes a variety of facial expressions, body postures, and vocalizations (Chang et al., 2013).”
BackgroundEpigenomics and gene regulation in mammalian social systems
Guerrero-Altamirano, T., Fickel, J., Benhaiem, S., & Weyrich, A. (2020) · Current Zoology · doi:10.1093/cz/zoaa005 · Cited by 17
Fan, S., Monte, O. D., Nair, A. R., Fagan, N. A., & Chang, S. W. C. (2024) · Neuron · doi:10.1016/j.neuron.2024.05.004 · Cited by 19
Self-citationWild female vervet monkeys change grooming patterns and partners when freed from feeding constraints
García, M. G., Farine, D. R., Brachotte, C., Borgeaud, C., & Bshary, R. (2021) · Animal Behaviour · doi:10.1016/j.anbehav.2021.08.027 · Cited by 17
The Genetic Basis of Primate Behavior: Genetics and Genomics in Field-Based Primatology
Brent, L. J. N., & Melin, A. D. (2013) · International Journal of Primatology · doi:10.1007/s10764-013-9732-6 · Cited by 16
“…of years of careful and intensive study, will allow primatologists to deftly leverage genetic and genomic data to detect the effects of natural selection and to build realistic models of the dynamic contigency that exists among genes, behaviors, the environment, and fitness (Chang et al. 2013).”
BackgroundSelf-citationOxytocin, vasopressin, and primate behavior: Diversity and insight
Freeman, S. M., & Bales, K. L. (2018) · American Journal of Primatology · doi:10.1002/ajp.22919 · Cited by 15
Role of the social actor during social interaction and learning in human-monkey paradigms
Nougaret, S., Ferrucci, L., & Genovesio, A. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.05.004 · Cited by 14
Epiphenomenal neural activity in the primate cortexPreprint
Tremblay, S., Testard, C., Inchauspé, J., & Petrides, M. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.09.12.506984 · Cited by 14
Ryan, A. M., Murai, T., Lau, A. R., Hogrefe, C. E., McAllister, A. K., Carter, C. S., & Bauman, M. D. (2020) · Developmental Psychobiology · doi:10.1002/dev.22003 · Cited by 14
“They navigate their social world by rapidly interpreting social information from a variety of signals such as facial expressions, gestures, and vocalizations (Chang et al., 2013).”
BackgroundPrenatal maternal stress effects on the development of primate social behavior
Schülke, O., Ostner, J., & Berghänel, A. (2019) · Behavioral Ecology and Sociobiology · doi:10.1007/s00265-019-2729-1 · Cited by 17
“Variation in social behavior strategies may result from differences in the underlying cognitive function and hormonal regulation of social behavior (Uno et al. 1994; Chang et al. 2013; Brent et al. 2014; Pearce et al. 2017; Crockford et al. 2018).”
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-citationDepletion of giant ANK2 in monkeys causes drastic brain volume loss
Qin, D., Zhou, J., He, X., Shen, X., Li, C., Chen, H.-Z., Yan, L., Hu, Z., Li, X., Lv, L., et al. (2021) · Cell Discovery · doi:10.1038/s41421-021-00336-4 · Cited by 12
Individual differences in social attachment: A multi‐disciplinary perspective
Gustison, M. L., & Phelps, S. M. (2022) · Genes Brain & Behavior · doi:10.1111/gbb.12792 · Cited by 15
Behavioral screening tools for identifying autism in macaques: existing and promising tests
Qin, D., Wu, S., Chen, Y., & Hu, X. (2018) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2018.12.018 · Cited by 12
Do young rhesus macaques know what others see?: A comparative developmental perspective
Arre, A. M., Clark, C. S., & Santos, L. R. (2019) · American Journal of Primatology · doi:10.1002/ajp.23054 · Cited by 10
“Rhesus macaques are one of the most well‐studied primate species in the domain of social cognition (Call & Tomasello, 2008; Chang et al., 2013; Drayton & Santos, 2016; Platt, Seyfarth, & Cheney, 2016; Rosati et al., 2010).”
BackgroundCanini, M., Pecco, N., Caglioni, M., Katušić, A., Išasegi, I. Ž., Oprandi, C., Scifo, P., Pozzoni, M., Lorioli, L., Garbetta, G., et al. (2023) · Journal of Neuroscience Research · doi:10.1002/jnr.25207 · Cited by 11
The motivational role of affect in an ecological model
Gabriel, R. H. (2021) · Theory & Psychology · doi:10.1177/0959354321992869 · Cited by 10
“The relational nature of the dorsomedial PFC (along with part of the posterior cingulate and a region of the anterior cingulate) is likewise illustrated in its role in joint attention, theory of mind, and various forms of social cognition (Chang et al., 2013).”
BackgroundInfluentialNeural basis of multi-sensory communication in primates
Sliwa, J., Mallet, M., Christiaens, M., & Takahashi, D. Y. (2022) · Ethology Ecology & Evolution · doi:10.1080/03949370.2021.2024266 · Cited by 15
“…in the processing of reward contingencies and social valuation (Paus 2001; Rudebeck et al. 2006; Rushworth et al. 2007; Behrens et al. 2009; Chang et al. 2013), it may transform perceived social risks and rewards into appropriately responsive facial displays, such as lip-smacking, fear…”
BackgroundMethodInfluentialMatsumoto, J., Kaneko, T., Kimura, K., Negrete, S. B., Guo, J. Y., Suda‐Hashimoto, N., Kaneko, A., Morimoto, M., Nishimaru, H., Setogawa, T., et al. (2025) · Science Advances · doi:10.1126/sciadv.adn1355 · Cited by 14
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-citationRhesus macaques form preferences for brand logos through sex and social status based advertising
Acikalin, M. Y., Watson, K. K., Fitzsimons, G. J., & Platt, M. L. (2018) · PLoS ONE · doi:10.1371/journal.pone.0193055 · Cited by 8
Self-citationSerotonin, behavior, and natural selection in New World monkeys
Reales, G., Paixão‐Côrtes, V. R., Cybis, G. B., GONÇALVES, G. L., Pissinatti, A., Salzano, F. M., & Bortolini, M. C. (2018) · Journal of Evolutionary Biology · doi:10.1111/jeb.13295 · Cited by 8
A dyadic brain model of ape gestural learning, production and representation
Gasser, B., & Arbib, M. A. (2019) · Animal Cognition · doi:10.1007/s10071-018-1228-5 · Cited by 8
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
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