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Review
. 2017 Sep 25;90(3):373-387.
eCollection 2017 Sep.

Titi Monkeys as a Novel Non-Human Primate Model for the Neurobiology of Pair Bonding

Karen L Bales  1   2 , Rocío Arias Del Razo  1   2 , Quinn A Conklin  1   3 , Sarah Hartman  4 , Heather S Mayer  1 , Forrest D Rogers  1 , Trenton C Simmons  1 , Leigh K Smith  1 , Alexia Williams  1 , Donald R Williams  1 , Lynea R Witczak  1   2 , Emily C Wright  1
Affiliations
Review

Titi Monkeys as a Novel Non-Human Primate Model for the Neurobiology of Pair Bonding

Karen L Bales et al. Yale J Biol Med. .

Abstract

It is now widely recognized that social bonds are critical to human health and well-being. One of the most important social bonds is the attachment relationship between two adults, known as the pair bond. The pair bond involves many characteristics that are inextricably linked to quality of health, including providing a secure psychological base and acting as a social buffer against stress. The majority of our knowledge about the neurobiology of pair bonding comes from studies of a socially monogamous rodent, the prairie vole (Microtus ochrogaster), and from human imaging studies, which inherently lack control. Here, we first review what is known of the neurobiology of pair bonding from humans and prairie voles. We then present a summary of the studies we have conducted in titi monkeys (Callicebus cupreus)-a species of socially monogamous New World primates. Finally, we construct a neural model based on the location of neuropeptide receptors in the titi monkey brain, as well as the location of neural changes in our imaging studies, with some basic assumptions based on the prairie vole model. In this model, we emphasize the role of visual mating stimuli as well as contributions of the dopaminergic reward system and a strong role for the lateral septum. This model represents an important step in understanding the neurobiology of social bonds in non-human primates, which will in turn facilitate a better understanding of these mechanisms in humans.

Keywords: dopamine; opioids; oxytocin; pair bond; prairie vole; relationships; social monogamy; vasopressin.

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Figures

Figure 1
Figure 1
Summary of advantages and disadvantages of studying the neurobiology of pair bonding in prairie voles, titi monkeys, and humans.
Figure 2
Figure 2
Titi monkey family; pair bonded male and female with infant. © Kathy West, California National Primate Research Center.
Figure 3
Figure 3
Proposed model for the neurobiology of pair bond formation in male titi monkeys. Arrow heads indicate excitatory effects on the subsequent neural region while flat heads indicate inhibitory effects. Dashed lines represent either prior or later neural processing not detailed in the model. The + and – signs correspond to positively and negatively valenced neuronal populations respectively. Not all connections between areas are shown, in order to reduce the complexity of the figure. Region shading corresponds to the justification for inclusion in the model; white regions were hypothesized to be important for pair bond behavior based on a variety of factors (e.g. receptor presence, anatomical connections), light gray regions were included based on importance in other models (e.g. vole), and dark gray regions were included based on the results from PET studies we have previously conducted on titi monkeys. Abbreviations: CA3=hippocampus; CeA=central amygdala; LGN=lateral geniculate nucleus; LS=lateral septum; NAc=nucleus accumbens; PUL=pulvinar; PVN=paraventricular nucleus of the hypothalamus; SC=superior colliculus; VTA=ventral tegmental area; V1=primary visual cortex.
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