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Developmental shifts in social cognition: socio-emotional biases across the lifespan in rhesus monkeys

  • Alexandra G. RosatiEmail author
  • Alyssa M. Arre
  • Michael L. Platt
  • Laurie R. Santos
Original Article
Part of the following topical collections:
  1. An evolutionary perspective on the development of primate sociality

Abstract

Humans exhibit a suite of developmental changes in social cognition across the lifespan. To what extent are these developmental patterns unique? We first review several social domains in which humans undergo critical ontogenetic changes in socio-cognitive processing, including social attention and theory of mind. We then examine whether one human developmental transition—a shift in socio-emotional preferences—also occurs in non-human primates. Specifically, we experimentally measured socio-emotional processing in a large population of rhesus macaques (Macaca mulatta) ranging from infancy to old age. We tested whether macaques, like humans, also exhibited developmental shifts from a negativity bias at younger ages, indicating preferential attention to negative socio-emotional stimuli, to a positivity bias at older ages. We first assessed monkeys’ (n = 337) responses to negative socio-emotional stimuli by comparing their duration of looking towards photos of negative conspecific signals (threat displays) versus matched neutral expressions. In contrast to the pattern observed in humans, we found that older monkeys were more attentive to negative emotional stimuli than were younger monkeys. In a second study, we used the same method to examine monkeys’ (n = 132) attention to positive (affiliative displays) versus matched neutral expressions. Monkeys did not exhibit an overall preference for positive stimuli, nor major age-related changes in their attention. These results indicate that while monkeys show robust ontogenetic shifts in social preferences, they differ from humans by exhibiting an increasing negativity bias with age. Studies of comparative cognitive development can therefore provide insight into the evolutionary origins of human socio-cognitive development.

Significance statement

Humans are characterized by complex and flexible social behavior. Understanding the proximate psychological mechanisms and developmental processes that underpin these social behaviors can shed light on the evolutionary history of our species. We used a comparative developmental approach to identify whether a key component of human social cognition, responses to emotionally-charged social stimuli, are shared with other primates. Humans exhibit important shifts in this aspect of our social cognition: younger individuals attend more to negative stimuli, whereas older adults tend to focus on positive information. These shifts are thought to appropriately tailor our age-dependent social goals. We found that, unlike humans, rhesus monkeys show an increasing negativity bias with age. By examining primate cognition across the lifespan, this work can help disentangle how complex forms of social behavior emerge across species.

Keywords

Social cognition Comparative development Primates Socio-emotional biases Emotional signals 

Notes

Acknowledgments

We thank the editors of the special issue; two anonymous reviewers for comments on the manuscript; Lindsey Jones, Samantha Monier, and Alondra Arguello for assistance with data collection and coding; and Kerby Shedden at the University of Michigan’s Consulting for Statistics, Computing and Analytics Research (CSCAR) for statistical advice. The authors are grateful to the Cayo Santiago Santiago Field Station and staff including Angelina Ruiz Lambides, Nahiri Rivera Barreto, Giselle Caraballo Cruz, and Bianca Giura for their research support.

Funding

This work was supported by NIMH (R01MH096875), a National Center for Research Resources CM-5-P40RR003640-13 award to the Caribbean Primate Research Center and the University of Puerto Rico, and an Office of Research Infrastructure Programs (ORIP) of the National Institutes of Health (NIH) through Grant Number 5P40OD012217 to the Caribbean Primate Research Center and the University of Puerto Rico. LRS was supported by the James S. McDonnell Foundation (no. 220020242).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflicts of interest.

Ethics approval

All non-invasive behavioral tests were approved by the Institutional Animal Care and Use Committee (IACUC) for Yale University (no. 2014-11624), as well as the Cayo Santiago IACUC (#8310106) administered through the University of Puerto Rico Medical Sciences Campus. All tests adhered to site guidelines for animal research.

Supplementary material

Video S1

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265_2018_2573_MOESM1_ESM.pdf (132 kb)
ESM 1 (PDF 131 kb)

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Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Departments of Psychology and AnthropologyUniversity of MichiganAnn ArborUSA
  2. 2.Department of PsychologyYale UniversityNew HavenUSA
  3. 3.Departments of Neuroscience, Psychology, and MarketingUniversity of PennsylvaniaPhiladelphiaUSA

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