Expression of bond-related behaviors affects titi monkey responsiveness to oxytocin and vasopressin treatments

Abstract

Social bonds influence physiology and behavior, which can shape how individuals respond to physical and affective challenges. Coppery titi monkey (Plecturocebus cupreus) offspring form selective bonds with their fathers, making them ideal for investigating how father-daughter bonds influence juveniles' responses to oxytocin (OT) and arginine-vasopressin (AVP) manipulations. We quantified the expression of father-daughter bond-related behaviors in females (n = 10) and gave acute intranasal treatments of saline, low/medium/high OT, low/high AVP, or an OT receptor antagonist (OTA) to subjects prior to a parent preference test. While females spent more time in proximity to their parents than strangers, we found a large degree of individual variation. Females with greater expression of bonding behaviors responded to OT treatments in a dose-dependent manner. Subjects also spent less time in proximity to strangers when treated with High OT (p = 0.003) and Low OT (p = 0.007), but more time when treated with High AVP (p = 0.007), Low AVP (p = 0.009), and OTA (p = 0.001). Findings from the present study suggest that variation in the expression of bond-related behaviors may alter responsiveness to OT and AVP, increasing engagement with unfamiliar social others. This enhanced sociality with strangers may promote the formation of pair bonds with partners.

Keywords: early‐life experience; intranasal oxytocin; intranasal vasopressin; nonhuman primate; preference test; proximity maintenance; social bond.

FIGURE 1

Schematic for parent preference test. Subject placed in center arena, the subjects’ parents would be in one of the stimulus animal cages, and a pair of unfamiliar adult titi monkeys would be in the other stimulus animal cage. Time spent in the preference zones of the stimulus pairs was live-scored in five 30-minute blocks.

FIGURE 2

Summary of time females spent in the preference zone of the parents, the preference zone of the stranger pair of titi monkeys, and the non-social “other” areas of the testing arena, separated by Treatment. In general, females spent more time in their parents’ proximity zone than they did near the strangers and in the non-social areas of the test. Parent = Parent preference zone duration; Stranger = Stranger preference zone duration; Other = Other (or “non-social”) zone duration. Saline = saline; LowOT = 0.8 IU/kg OT; MedOT = 8.0 IU/kg OT; HighOT = 80.0 IU/kg OT; LowAVP = 40 IU/kg AVP; HighAVP = 80 IU/kg AVP; OTA = 10 mg/kg OTA Abbreviations: AVP, arginine-vasopressin; OT, oxytocin; OTA, oxytocin receptor antagonist.

FIGURE 3

Summary of interaction between Treatment and Juvenile Parent Preference for significant interactions only. In comparison to when daughters are treated with saline (control), females spend less time in their parents’ proximity zone when treated with the high dosage of oxytocin, the low and high doses of arginine-vasopressin, and the oxytocin antagonist if they spent a greater percentage of time (relative to the sample mean) near their parents during juvenile parent preference testing (control condition). For a combined graph of all interaction effects see Supporting Information Figure S2. Saline = saline; HighAVP = 80 IU/kg AVP; HighOT = 80.0 IU/kg OT; LowAVP = 40 IU/kg AVP; OTA = 10 mg/kg OTA. Abbreviations: AVP, arginine-vasopressin; OT, oxytocin; OTA, oxytocin receptor antagonist.

FIGURE 4

Summary of interaction between Treatment and IOF Grate for significant interactions only. In comparison to the control condition (females treated with saline), females that spent more time touching the grate during infant open field (IOF) testing a) spent less time in proximity to the strangers when treated with the low and high doses of oxytocin, and b) spent more time in proximity to the strangers when treated with the low and high doses of arginine-vasopressin and the oxytocin receptor antagonist. For a combined graph of all interaction effects see Supporting Information Figure S3. Saline = saline; HighOT = 80.0 IU/kg OT; LowOT = 0.8 IU/kg OT; HighAVP = 80 IU/kg AVP; LowAVP = 40 IU/kg AVP; OTA = 10 mg/kg OTA. Abbreviations: AVP, arginine-vasopressin; OT, oxytocin; OTA, oxytocin receptor antagonist.