Abstract

Close social bonds are integral for good health and longevity in humans and non-human primates (NHPs), yet we have very little understanding of the neurobiological differences between healthy and unhealthy relationships. Our current understanding of social bonding is grounded in Bowlby’s theory of attachment. Work done with human infants and adult couples has suggested that attachment behavior developed in infancy remains stable through development into adulthood. Unfortunately, knowledge of the neurobiological correlates of attachment behavior has been limited due to a lack of animal models with both infant and adult attachments similar to humans. To address this, we measured behavioral responses to separation from their primary attachment figure in infant and adult titi monkeys (Plecturocebus cupreus). In Experiment 1, we tested for a linear relationship between the subject’s response to separation as an infant and their response to separation as an adult. We found greater decreases in infant locomotor behavior in the presence, as opposed to absence, of their primary attachment figure to be indicative of decreased anxiety-like behavior in the presence, as opposed to absence, of their adult pair mates during a novelty response task. In Experiment 2, we increased our sample size, accounted for adverse early experience, and tested a different outcome measure, adult affiliative behavior. We hypothesized that the level of intensity of an infant’s response to separation would explain affiliative behavior with their mate as an adult, but adverse early experience could change this relationship. When we compared infant response to separation to adult affiliative behavior during the first 6 months of their first adult pair bond, we observed a linear relationship for infants with typical early experience, but not for infants with adverse early experience. Infants with a greater change in locomotive behavior between the father and alone conditions were more affiliative with their first adult pair mate. These data support the use of titi monkeys as an appropriate animal model for further investigation of the neurobiology underlying attachment behavior.

Highlights

  • Both humans and non-human primates (NHPs) rely on close social bonds to survive and thrive in their environments (Berkman and Syme, 1979; House et al, 1988; Holt-Lunstad et al, 2010; Stanton and Campbell, 2014)

  • The current study examined the relationship between infant attachment behavior and adult attachment behavior in the titi monkey

  • Our results suggest that the type of attachment behavior which an infant titi monkey displays with their father is indicative of the type of attachment behavior they will share with their adult pair mate

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Summary

Introduction

Both humans and non-human primates (NHPs) rely on close social bonds to survive and thrive in their environments (Berkman and Syme, 1979; House et al, 1988; Holt-Lunstad et al, 2010; Stanton and Campbell, 2014). The current article is written from a developmental perspective, but it should be noted that Attachment Theory has been historically discussed within different psychological contexts (for a detailed review see George and West, 1999) For both infant-parent and adult romantic relationships, the attachment is defined by three distinct behaviors: proximity maintenance, distress upon involuntary separation, and the ability of the attachment figure to ameliorate stress during anxiety-provoking instances (Bowlby, 1969; Hazan and Shaver, 1987; French et al, 2018). While these three behaviors are the keystones of attachments and relationships, they vary between and within individuals, reflecting the quality of the bond. Developing an NHP model capable of illustrating individual variation in attachment behavior, similar to that in humans, from infancy to adulthood could open opportunities to understand the intricate effects of attachments on behavior, cognition, and biology

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