The primary goal of this research is to further our understanding of the neurobiological basis of social bonding, using a unique non-human primate model. Dysfunctions in social bonding underlie a number of developmental and psychiatric disorders, as well as having long-term consequences for physical and psychological health. In this broader context, we propose to study a species which displays high levels of selective social bonding, the monogamous titi monkey (Callicebus cupreus). This species displays a pair-bond, or selective attachment between males and females, as well as attachment by offspring to their father. Non-human primate models are a valuable addition to rodent models, in being neuroanatomically much closer to humans. In many cases they are also preferable to studying humans directly, because of the greater control possible over individual experience and experimental conditions. Arginine vasopressin (AVP) and oxytocin (OT) are neuropeptide hormones known to be involved in social bonding in rodents. Although there is also evidence for their role in primate social bonding, the directionality of the process is unclear. We propose to distinguish between three models of the relationship between AVP, OT and social bonding: a) Maturational - the formation of social bonds in a monogamous species are the results of irreversible, age-related maturational processes in which changes in the AVP and OT systems (increases in synthesis, changes in receptor binding) set up a predisposition to form a pair-bond;b) Situational - changes in the AVP and OT systems are completely environmental and the direct result of the formation of a pair-bond or parental attachment. In this model, these changes are reversible upon the loss of the attachment figure, and c) Combination - while irreversible maturational changes in AVP and/or OT set the stage for formation of an adult attachment, the formation of a pair-bond then induces further changes and the loss of an attachment figure can """"""""reset"""""""" the process. Our previous research in this species shows evidence for both maturational changes (gonadal hormones, Valeggia et al., 1999) and situational changes (adrenocortical response to formation and disruption of attachment bonds, Mendoza et al., 2000). Our overarching hypothesis for the current research is that both processes are combined with respect to neuropeptide regulation of pair-bonding - the proposed """"""""combination"""""""" model.

Public Health Relevance

Here we propose to study the relationship between the hormones oxytocin and vasopressin, and the development of social bonding in a non-human primate model, the coppery titi monkey. This is relevant to the study of disorders of social bonding such as autism.

National Institute of Health (NIH)
Eunice Kennedy Shriver National Institute of Child Health & Human Development (NICHD)
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Biobehavioral Regulation, Learning and Ethology Study Section (BRLE)
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Freund, Lisa S
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University of California Davis
Veterinary Sciences
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United States
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Kanthaswamy, Sree; Bales, Karen L (2018) Evaluating the genetic status of a closed colony of titi monkeys (Callicebus cupreus) using multigenerational pedigrees. J Med Primatol 47:139-141
Maninger, Nicole; Mendoza, Sally P; Williams, Donald R et al. (2017) Imaging, Behavior and Endocrine Analysis of ""Jealousy"" in a Monogamous Primate. Front Ecol Evol 5:
Hostetler, Caroline M; Hinde, Katherine; Maninger, Nicole et al. (2017) Effects of pair bonding on dopamine D1 receptors in monogamous male titi monkeys (Callicebus cupreus). Am J Primatol 79:1-9
Larke, Rebecca H; Toubiana, Alice; Lindsay, Katrina A et al. (2017) Infant titi monkey behavior in the open field test and the effect of early adversity. Am J Primatol 79:
Maninger, Nicole; Hinde, Katie; Mendoza, Sally P et al. (2017) Pair bond formation leads to a sustained increase in global cerebral glucose metabolism in monogamous male titi monkeys (Callicebus cupreus). Neuroscience 348:302-312
Carp, Sarah B; Rothwell, Emily S; Bourdon, Alexis et al. (2016) Development of a partner preference test that differentiates between established pair bonds and other relationships in socially monogamous titi monkeys (Callicebus cupreus). Am J Primatol 78:326-39
Bales, Karen L; Saltzman, Wendy (2016) Fathering in rodents: Neurobiological substrates and consequences for offspring. Horm Behav 77:249-59
Larke, Rebecca H; Maninger, Nicole; Ragen, Benjamin J et al. (2016) Serotonin 1A agonism decreases affiliative behavior in pair-bonded titi monkeys. Horm Behav 86:71-77
Díaz-Muñoz, Samuel L; Bales, Karen L (2016) ""Monogamy"" in Primates: Variability, Trends, and Synthesis: Introduction to special issue on Primate Monogamy. Am J Primatol 78:283-7
Hinde, Katie; Muth, Chelsea; Maninger, Nicole et al. (2016) Challenges to the Pair Bond: Neural and Hormonal Effects of Separation and Reunion in a Monogamous Primate. Front Behav Neurosci 10:221

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