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Long term effects of chronic intranasal oxytocin on adult pair bonding behavior and brain glucose uptake in titi monkeys (Plecturocebus cupreus).

ABSTRACT: Intranasal oxytocin (IN OXT) administration has been proposed as a pharmacological treatment for a range of biomedical conditions including neurodevelopmental disorders. However, studies evaluating the potential long-lasting effects of chronic IN OXT during development are still scarce. Here we conducted a follow-up study of a cohort of adult titi monkeys that received intranasal oxytocin 0.8 IU/kg (n = 15) or saline (n = 14) daily for six months during their juvenile period (12 to 18 months of age), with the goal of evaluating the potential long-lasting behavioral and neural effects one year post-treatment. Subjects were paired with an opposite-sex mate at 30 months of age (one year post-treatment). We examined pair affiliative behavior in the home cage during the first four months and tested for behavioral components of pair bonding at one week and four months post-pairing. We assessed long-term changes in brain glucose uptake using ¹⁸FDG positron emission tomography (PET) scans. Our results showed that OXT-treated animals were more affiliative across a number of measures, including tail twining, compared to SAL treated subjects (tail twining is considered the "highest" type of affiliation in titi monkeys). Neuroimaging showed no treatment differences in glucose uptake between SAL and OXT-treated animals; however, females showed higher glucose uptake in whole brain at 23 months, and in both the whole brain and the social salience network at 33 months of age compared to males. Our results suggest that chronic IN OXT administration during development can have long-term effects on adult social behavior.

SUBMITTER: Razo RA

PROVIDER: S-EPMC9250651 | biostudies-literature | 2022 Apr

REPOSITORIES: biostudies-literature

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Long term effects of chronic intranasal oxytocin on adult pair bonding behavior and brain glucose uptake in titi monkeys (Plecturocebus cupreus).

Razo Rocío Arias-Del RA Velasco Vazquez Maria de Lourdes ML Turcanu Petru P Legrand Mathieu M Floch Maeva M Weinstein Tamara A R TAR Goetze Leana R LR Freeman Sara M SM Baxter Alexander A Witczak Lynea R LR Sahagún Elizabeth E Berger Trish T Jacob Suma S Lawrence Rebecca H RH Rothwell Emily S ES Savidge Logan E LE Solomon Marjorie M Mendoza Sally P SP Bales Karen L KL

Hormones and behavior 20220202

Intranasal oxytocin (IN OXT) administration has been proposed as a pharmacological treatment for a range of biomedical conditions including neurodevelopmental disorders. However, studies evaluating the potential long-lasting effects of chronic IN OXT during development are still scarce. Here we conducted a follow-up study of a cohort of adult titi monkeys that received intranasal oxytocin 0.8 IU/kg (n = 15) or saline (n = 14) daily for six months during their juvenile period (12 to 18 months of ...[more]

PMID: 35123106

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Project description:In socially monogamous titi monkeys, involuntary separation from a pair mate can produce behavioral distress and increased cortisol production. The neuropeptide oxytocin (OXT) is thought to play an important role in the separation response of pair-bonded species. Previous studies from our lab have shown that chronic intranasal oxytocin (IN OXT) during development can have long-term effects on adult social behavior. In the current study, we examined the chronic and acute effects of IN OXT or Saline (SAL) on the subjects' response to a brief separation from their pair mates. Subjects with a history of chronic IN OXT or SAL treatment during development received a single dose of OXT or SAL as adults 30 min before being separated from their pair mate. Chronic treatment consisted of a daily dose of IN OXT (0.8 IU/kg) or SAL (control) from 12 to 18 months of age. Subjects (N = 29) were introduced to a pair mate at 30 months of age. After the pairs had cohabitated for 5 months, pairs underwent two "Brief Separation" (OXT and SAL) and two "Non-Separation" (OXT and SAL) test sessions. Vocalizations and locomotion were measured as behavioral indices of agitation or distress during the Brief Separation and Non-Separation periods (30 min each). We collected blood samples after the Brief Separation and Non-Separation periods to measure cortisol levels. Our results showed subjects treated with chronic OXT had a reduction in long call and peep vocalizations compared to subjects treated with chronic SAL. Subjects treated with chronic SAL and acute OXT produced more peeps and long calls compared to animals treated with acute SAL; however, patterns in this response depended on sex. Cortisol and locomotion were significantly higher during the Brief Separation period compared to the Non-Separation period; however, we did not find any treatment or sex effects. We conclude that chronic IN OXT given during development blunts the separation response, while acute OXT in chronic SAL subjects had sexually dimorphic effects, which could reflect increased partner seeking behaviors in males and increased anxiety in females.

Project description:As social animals, many primates use acoustic communication to maintain relationships. Vocal individuality has been documented in a diverse range of primate species and call types, many of which have presumably different functions. Auditory recognition of one's neighbors may confer a selective advantage if identifying conspecifics decreases the need to participate in costly territorial behaviors. Alternatively, vocal individuality may be nonadaptive and the result of a unique combination of genetics and environment. Pair-bonded primates, in particular, often participate in coordinated vocal duets that can be heard over long distances by neighboring conspecifics. In contrast to adult calls, infant vocalizations are short-range and used for intragroup communication. Here, we provide two separate but complementary analyses of vocal individuality in distinct call types of coppery titi monkeys (Plecturocebus cupreus) to test whether individuality occurs in call types from animals of different age classes with presumably different functions. We analyzed 600 trill vocalizations from 30 infants and 169 pulse-chirp duet vocalizations from 30 adult titi monkeys. We predicted that duet contributions would exhibit a higher degree of individuality than infant trills, given their assumed function for long-distance, intergroup communication. We estimated 7 features from infant trills and 16 features from spectrograms of adult pulse-chirps, then used discriminant function analysis with leave-one-out cross-validation to classify individuals. We correctly classified infants with 48% accuracy and adults with 83% accuracy. To further investigate variance in call features, we used a multivariate variance components model to estimate variance partitioning in features across two levels: within- and between-individuals. Between-individual variance was the most important source of variance for all features in adults, and three of four features in infants. We show that pulse-chirps of adult titi monkey duets are individually distinct, and infant trills are less individually distinct, which may be due to the different functions of the vocalizations.

Project description:Pair-bonded primates have uniquely enduring relationships and partners engage in a suite of behaviors to maintain these close bonds. In titi monkeys, pair bond formation has been extensively studied, but changes across relationship tenure remain unstudied. We evaluated differences in behavioral indicators of pair bonding in newly formed (~6 months paired, n = 9) compared to well-established pairs (average 3 years paired, n = 8) of titi monkeys (Callicebus cupreus) as well as sex differences within the pairs. We hypothesized that overall males would contribute more to maintenance than females, but that the pattern of maintenance behaviors would differ between newly formed and well-established pairs. Each titi monkey (N = 34) participated in a partner preference test (PPT), where the subject was placed in a middle test cage with grated windows separating the subject from the partner on one side and an opposite-sex stranger on the other side. During this 150-min behavioral test, we quantified four key behaviors: time in proximity to the partner or stranger as well as aggressive displays toward the partner or stranger. Overall, we found different behavioral profiles representing newly formed and well-established pair-bond relationships in titi monkeys and male-biased relationship maintenance. Males spent ∼40% of their time in the PPT maintaining proximity to the female partner, regardless of relationship tenure. Males from well-established bonds spent less time (14%) near the female stranger compared to males from newly formed bonds (21%) at the trend level. In contrast, females from well-established bonds spent less (23%) time near the male partner in the PPT compared to females from newly formed bonds (47%). Aggressive displays were more frequent in newly formed bonds compared to well-established bonds, especially for females. Scan sampling for homecage affiliation showed that newly formed pairs were more likely to be found tail twining than well-established pairs.

Project description: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.

Project description:Coordination of oxytocin (OT) activity and partner interactions is important for the facilitation and maintenance of monogamous pair bonds. We used coppery titi monkeys (Callicebus cupreus) to identify the effects of male aggressive temperament on OT activity, affiliative partner-directed behaviors, aggressive partner-directed behaviors, anxiety-related behaviors, and hormone-behavior interactions. We used a mirror technique, simulating an intruder in the home territory of pairs to elicit behavioral responses, and quantified behaviors using an established ethogram. Plasma concentrations of OT (pg/ml) were quantified using enzyme immunoassay. We used general linear mixed models to predict 1) percent change in OT as a function of aggression score, and 2) percent change in behaviors as a function of aggression, OT, and OT by aggression interactions. High-aggressive males exhibited a significant drop in OT concentration relative to control when exposed to the front of the mirror (β = -0.22, SE = 0.10, t = -2.20, p = 0.04). High-aggressive males spent significantly less time in contact with their mates (β = -1.35, SE = 0.60, t = -2.26, p = 0.04) and lip-smacked less (β = -1.02, SE = 0.44, t = -2.32, p = 0.03) relative to control. We also saw a trend toward an interaction effect between OT and proximity such that High-aggressive males displaying a drop in OT exhibited a smaller percent increase in social proximity (β = 6.80, SE = 3.48, t = 1.96, p = 0.07). Males exhibiting a decrease in OT also trended toward back-arching and tail-lashing less in response to the mirror (β = 4.53, SE = 2.5, t = 1.82, p = 0.09). To our knowledge, this is the first empirical study to examine interactions between OT and temperament in adult monogamous primates. Future studies should incorporate measures of pair-mate interactions and early-life experience to further understand variation in responses to social stressors and their effects on pair bonding.

Dataset Information

Long term effects of chronic intranasal oxytocin on adult pair bonding behavior and brain glucose uptake in titi monkeys (Plecturocebus cupreus).

Publications

Long term effects of chronic intranasal oxytocin on adult pair bonding behavior and brain glucose uptake in titi monkeys (Plecturocebus cupreus).

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