Dopamine D1-like receptors regulate agonistic components of pair bond maintenance behaviors in male titi monkeys (Callicebus cupreus)

Abstract

Several neurobiological mechanisms are implicated in the formation of selective pair bonds in socially monogamous mammals, however much less is known about the mechanisms that underlie the long-term behavioral maintenance of these bonds. In prairie voles (Microtus ochrogaster), agonistic behavior that contributes to pair bond maintenance are regulated by dopamine activity at D1-like receptors (D1R) within the mesocorticolimbic system. Evidence suggests D1Rs similarly regulate the behavioral components of pair bond maintenance in socially monogamous titi monkeys (Callicebus cupreus); however, evaluation with behavioral pharmacology is necessary to evaluate this hypothesis. In the current study we evaluated the role of D1Rs in behavioral components of pair bond maintenance in captive male titi monkeys (N = 8). We administered two doses of a D1R selective antagonist, SCH23390, (0.1 mg/kg, 0.01 mg/kg) or saline vehicle to male titi monkeys and presented pairs with a simulated intruder monkey via the use of a mirror stimulus. The non-reflective back of the mirror stimulus was used for control sessions. We video recorded responses to the five-minute stimulus presentations and later scored for arousal and agonistic behaviors relevant to mate guarding as well as affiliative behavior between the pair mates. We also conducted a locomotor assessment to evaluate the potential side effect for SCH23390 of impaired locomotion. Finally, we collected blood samples at the end of each session to assay for plasma cortisol responses. We found evidence of locomotor impairment only with the high dose of SCH23390, and therefore analyses were conducted comparing only test sessions where low dose SCH23390 and saline were administered. With saline administration, males displayed more agonistic behavior via back arching and tail lashing as well as restraining their female partners when viewing the mirror compared to the back of the mirror. D1R antagonist treatment attenuated these agonistic behaviors indicative of mate guarding when males viewed the mirror. Results also indicated that this reduction in agonistic behavior occurred without evidence of overall behavioral blunting or generally reduced social interest. Likewise changes in agonistic behavior were not driven by differences in HPA activity across testing sessions. Mate-directed affiliative behavior, including lip smacks and approaches to female partners, were not altered by D1R antagonist treatment. Dyadic social contact was higher with D1R antagonist treatment, but this was due to a reduction in contact termination by the treated males, which was typically followed by an approach or arousal display to the simulated intruder. These results provide further evidence that D1R activity regulates mate guarding behaviors in titi monkeys and suggests that the dopamine system plays a similar role in the agonistic behavioral components of pair bond maintenance behavior in non-human primates and rodents.