Dataset Information

Neural correlates and effect of jealousy on cognitive flexibility in the female titi monkey (Plecturocebus cupreus).

ABSTRACT: Jealousy is a social emotion that manifests as behavioral reactions from an individual toward a threat to a valuable relationship. Monogamous species exhibit jealousy-type behaviors as an adaptive response to preserve the relationship. Jealousy is also a complex, negatively-valenced emotion which may include fear of loss, anxiety, suspiciousness, and anger. Negative emotion may impair cognitive processes such as cognitive flexibility, an ability important for coping with new situations. However, little is known about how complex social emotions influence cognitive flexibility. To understand the interaction between jealousy and cognitive flexibility, we examined the neural, physiological, and behavioral factors involved in jealousy and cognitive flexibility in female titi monkeys. We presented subjects with a jealousy provoking scenario, followed by a reversal learning task and a PET scan with a glucose-analog radiotracer. We found that female titi monkeys reacted to a jealousy provoking scenario with increased locomotor behavior and higher glucose uptake in the cerebellum; however, hormone measures and were not affected. As only two females demonstrated cognitive flexibility, the effects of jealousy were difficult to interpret. Locomotion behavior was also negatively correlated with glucose uptake in brain areas linked with motivation, sociality, and cognitive flexibility. Surprisingly, glucose uptake in the orbitofrontal cortex (OFC) was significantly decreased during jealousy scenarios, while uptake in the anterior cingulate cortex (ACC) was decreased during reversal tasks. Our findings suggest that the presence of an intruder produces less visible behavioral reactions in female titis than in males, while still reducing activity in the OFC.

SUBMITTER: Zablocki-Thomas PB

PROVIDER: S-EPMC10957291 | biostudies-literature | 2023 Jun

REPOSITORIES: biostudies-literature

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Neural correlates and effect of jealousy on cognitive flexibility in the female titi monkey (Plecturocebus cupreus).

Zablocki-Thomas Pauline B PB Savidge Logan E LE Witczak Lynea R LR Ferrer Emilio E Hobson Brad A BA Chaudhari Abhijit J AJ Freeman Sara M SM Bales Karen L KL

Hormones and behavior 20230403

Jealousy is a social emotion that manifests as behavioral reactions from an individual toward a threat to a valuable relationship. Monogamous species exhibit jealousy-type behaviors as an adaptive response to preserve the relationship. Jealousy is also a complex, negatively-valenced emotion which may include fear of loss, anxiety, suspiciousness, and anger. Negative emotion may impair cognitive processes such as cognitive flexibility, an ability important for coping with new situations. However, ...[more]

PMID: 37018894

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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: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.

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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:Worldwide urban expansion and deforestation have caused a rapid decline of non-human primates in recent decades. Yet, little is known to what extent these animals can tolerate anthropogenic noise arising from roadway traffic and human presence in their habitat. We studied six family groups of titis residing at increasing distances from a busy highway, in a park promoting ecotourism near Santa Cruz de la Sierra, Bolivia. We mapped group movements, sampled the titis' behavior, collected fecal samples from each study group and conducted experiments in which we used a mannequin simulating a human intrusion in their home range. We hypothesized that groups of titi monkeys exposed to higher levels of anthropogenic noise and human presence would react weakly to the mannequin and show higher concentrations of fecal cortisol compared with groups in least perturbed areas. Sound pressure measurements and systematic monitoring of soundscape inside the titis' home ranges confirmed the presence of a noise gradient, best characterized by the root-mean-square (RMS) and median amplitude (M) acoustic indices; importantly, both anthropogenic noise and human presence co-varied. Study groups resided in small, overlapping home ranges and they spent most of their time resting and preferentially used the lower forest stratum for traveling and the higher levels for foraging. Focal sampling analysis revealed that the time spent moving by adult pairs was inversely correlated with noise, the behavioral change occurring within a gradient of minimum sound pressures ranging from 44 dB(A) to 52 dB(A). Validated enzyme-immunoassays of fecal samples however detected surprisingly low cortisol concentrations, unrelated to the changes observed in the RMS and M indices. Finally, titis' response to the mannequin varied according to our expectation, with alarm calling being greater in distant groups relative to highway. Our study thus indicates reduced alarm calling through habituation to human presence and suggests a titis' resilience to anthropogenic noise with little evidence of physiological stress.

Dataset Information

Neural correlates and effect of jealousy on cognitive flexibility in the female titi monkey (Plecturocebus cupreus).

Publications

Neural correlates and effect of jealousy on cognitive flexibility in the female titi monkey (Plecturocebus cupreus).

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