Social connections predict brain structure in a multidimensional free-ranging primate society

Author:

Testard Camille1ORCID,Brent Lauren J. N.2ORCID,Andersson Jesper3,Chiou Kenneth L.45ORCID,Negron-Del Valle Josue E.45ORCID,DeCasien Alex R.678ORCID,Acevedo-Ithier Arianna1,Stock Michala K.9ORCID,Antón Susan C.67ORCID,Gonzalez Olga10ORCID,Walker Christopher S.11ORCID,Foxley Sean312ORCID,Compo Nicole R.1314,Bauman Samuel13ORCID,Ruiz-Lambides Angelina V.13ORCID,Martinez Melween I.13ORCID,Skene J. H. Pate1516ORCID,Horvath Julie E.17181920,Unit Cayo Biobank Research,Higham James P.67,Miller Karla L.3,Snyder-Mackler Noah4521ORCID,Montague Michael J.1ORCID,Platt Michael L.12223ORCID,Sallet Jérôme2425ORCID

Affiliation:

1. Department of Neuroscience, University of Pennsylvania, Philadelphia, PA, USA.

2. Centre for Research in Animal Behaviour, University of Exeter, Exeter, UK.

3. Wellcome Integrative Neuroimaging Centre, fMRIB, Oxford, UK.

4. Center for Evolution and Medicine, Arizona State University, Tempe, AZ, USA.

5. School of Life Sciences, Arizona State University, Tempe, AZ, USA.

6. Department of Anthropology, New York University, New York, NY, USA.

7. New York Consortium in Evolutionary Primatology, NYCEP, New York, NY, USA.

8. Section on Developmental Neurogenomics, National Institute of Mental Health, Washington, DC, USA.

9. Department of Sociology and Anthropology, Metropolitan State University of Denver, Denver, CO, USA.

10. Texas Biomedical Research Institute, San Antonio, TX, USA.

11. Department of Molecular Biomedical Sciences, College of Veterinary Medicine, North Carolina State University, Raleigh, NC, USA.

12. Department of Radiology, University of Chicago, Chicago, IL, USA.

13. Caribbean Primate Research Center, University of Puerto Rico, Sabana Seca, Puerto Rico.

14. Comparative Medicine, University of South Florida, Tampa, FL, USA.

15. Department of Neurobiology, Duke University, Durham, NC, USA.

16. Institute of Cognitive Science, University of Colorado, Boulder, CO, USA.

17. Department of Biological and Biomedical Sciences, North Carolina Central University, Durham, NC 27707, USA.

18. Department of Biological Sciences, North Carolina State University, Raleigh, NC, USA.

19. North Carolina Museum of Natural Sciences, Raleigh, NC 27601, USA.

20. Department of Evolutionary Anthropology, Duke University, Durham, NC 27708, USA.

21. ASU-Banner Neurodegenerative Disease Research Center, Arizona State University, Tempe, AZ, USA.

22. Department of Psychology, University of Pennsylvania, Philadelphia, PA, USA.

23. Marketing Department, University of Pennsylvania, Philadelphia, PA, USA,

24. Department of Experimental Psychology, Wellcome Integrative Neuroimaging Centre, Oxford, UK.

25. Stem Cell and Brain Research Institute, Inserm, Université Lyon 1, Bron U1208, France.

Abstract

Reproduction and survival in most primate species reflects management of both competitive and cooperative relationships. Here, we investigated the links between neuroanatomy and sociality in free-ranging rhesus macaques. In adults, the number of social partners predicted the volume of the mid–superior temporal sulcus and ventral-dysgranular insula, implicated in social decision-making and empathy, respectively. We found no link between brain structure and other key social variables such as social status or indirect connectedness in adults, nor between maternal social networks or status and dependent infant brain structure. Our findings demonstrate that the size of specific brain structures varies with the number of direct affiliative social connections and suggest that this relationship may arise during development. These results reinforce proposed links between social network size, biological success, and the expansion of specific brain circuits.

Publisher

American Association for the Advancement of Science (AAAS)

Subject

Multidisciplinary

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