Intranasal oxytocin does not change partner preference in female titi monkeys (Plecturocebus cupreus), but intranasal vasopressin decreases it.

Strong social bonds are critical to human health; however, the mechanisms by which social bonds are formed and maintained are still being elucidated. The neurohormones oxytocin (OT) and vasopressin (AVP) are considered likely candidates. Primate females, both human and nonhuman, remain understudied populations. Here, we conducted a pharmacological study coupled with a behavioral partner preference test (PPT) to better understand the mechanistic basis of attachment in adult female titi monkeys (Plecturocebus cupreus). This pair-bonding species shares a conserved form of oxytocin with humans and is an excellent model organism to study the neural basis of social bonding. We performed intranasal administration of three doses of oxytocin (IN-OT), two doses of vasopressin (IN-AVP), one dose of an oxytocin antagonist (IN-OTA) and one dose of a saline treatment. We found that compared to the saline control, the IN-AVP treatment (lower dose, 40 IU/kg) decreased the time spent in proximity to the partner and increased lip-smacking toward the stranger. We found no effects of IN-OT or IN-OTA manipulation on partner preference. In contrast, low-dose IN-AVP weakened the partner preference in female titi monkeys.

Survival rates and mortality risks of Plecturocebus cupreus at the California National Primate Research Center.

This article describes survivorship and explores factors affecting mortality risks in a captive colony of coppery titi monkeys (Plecturocebus cupreus) housed at the California National Primate Research Center (CNPRC), at UC Davis, in Davis, CA. We analyzed data collected on individuals since the colony's creation in the 1960s, with a sample of 600 animals with partially complete information (date of birth, age at death, body mass, parental lineage). We used three methods: (1) Kaplan-Meier regressions followed by a log-rank test to compare survival in male and female titi monkeys, (2) a breakpoint analysis to identify shifts in the survival curves, and (3) Cox regressions to test the effect of body mass change, parental pair tenure, and parental age on mortality risk. We found that males tend to have a longer median lifespan than females (14.9 and 11.4 years; p = 0.094) and that survival decreases earlier in males than in females during adulthood (9.8 and 16.2 years). A body mass loss of 10% from adulthood to the time of death led to a 26% higher risk of dying (p < 0.001) as compared to an individual with stable body mass. We found no evidence of sociobiological factors on mortality risks (parental age, parental pair tenure), but an exploratory analysis suggested that a higher rate of offspring conceptions increases mortality risks. This description of factors influencing survival and mortality in titi monkeys is a first step toward understanding aging in this species to consider titi monkeys as a primate model for socioemotional aging.

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

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.

Neuroimaging of human and non-human animal emotion and affect in the context of social relationships.

Long-term relationships are essential for the psychological wellbeing of humans and many animals. Positive emotions and affective experiences (e.g., romantic or platonic love) seem to be closely related to the creation and maintenance of social bonds. When relationships are threatened or terminated, other emotions generally considered to be negative can arise (e.g., jealousy or loneliness). Because humans and animals share (to varying degrees) common evolutionary histories, researchers have attempted to explain the evolution of affect and emotion through the comparative approach. Now brain imaging techniques allow the comparison of the neurobiological substrates of affective states and emotion in human and animal brains using a common methodology. Here, we review brain imaging studies that feature emotions characterized by the context of social bonding. We compare imaging findings associated with affective and emotional states elicited by similar social situations between humans and animal models. We also highlight the role of key neurohormones (i.e., oxytocin, vasopressin, and dopamine) that jointly support the occurrence of socially contextualized emotions and affect across species. In doing so, we seek to explore and clarify if and how humans and animals might similarly experience social emotion and affect in the context of social relationships.

Exploring the behavioral reactions to a mirror in the nocturnal grey mouse lemur: sex differences in avoidance.

Most mirror-image stimulation studies (MIS) have been conducted on social and diurnal animals in order to explore self-recognition, social responses, and personality traits. Small, nocturnal mammals are difficult to study in the wild and are under-represented in experimental behavioral studies. In this pilot study, we explored the behavioral reaction of a small nocturnal solitary forager-the grey mouse lemur (Microcebus murinus)-an emergent animal model in captivity. We assessed whether MIS can be used to detect a repeatable behavioral reaction, whether individuals will present a similar reaction toward a conspecific and the mirror, and whether males and females respond similarly. We tested 12 individuals (six males and six females) twice in three different contexts: with a mirror, with a live conspecific, and with a white board as a neutral control. We detected significant repeatability for the activity component of the behavioral reaction. There was a significant effect of the context and the interaction between presentation context and sex for avoidance during the first session for males but not for females. Males avoided the mirror more than they avoided a live conspecific. This pilot study opens a discussion on the behavioral differences between males and females regarding social interactions and reproduction in the nocturnal solitary species, and suggests that males are more sensitive to context of stimulation than females.

Heritability and genetic correlations of personality, life history and morphology in the grey mouse lemur (Microcebus murinus).

The recent interest in animal personality has sparked a number of studies on the heritability of personality traits. Yet, how the sources variance these traits can be decomposed remains unclear. Moreover, whether genetic correlations with life-history traits, personality traits and other phenotypic traits exist as predicted by the pace-of-life syndrome hypothesis remains poorly understood. Our aim was to compare the heritability of personality, life-history and morphological traits and their potential genetic correlations in a small primate (Microcebus murinus). We performed an animal model analysis on six traits measured in a large sample of captive mouse lemurs (N = 486). We chose two personality traits, two life-history traits and two morphological traits to (i) estimate the genetic and/or environmental contribution to their variance, and (ii) test for genetic correlations between these traits. We found modest narrow-sense heritability for personality traits, morphological traits and life-history traits. Other factors including maternal effects also influence the sources of variation in life-history and morphological traits. We found genetic correlations between emergence latency on the one hand and radius length and growth rate on the other hand. Emergence latency was also genetically correlated with birth weight and was influenced by maternal identity. These results provide insights into the influence of genes and maternal effects on the partitioning of sources of variation in personality, life-history and morphological traits in a captive primate model and suggest that the pace-of-life syndrome may be partly explained by genetic trait covariances.

An integrative modeling approach to the age-performance relationship in mammals at the cellular scale.

Physical and cognitive performances change across lifespan. Studying cohorts of individuals in specific age ranges and athletic abilities remains essential in assessing the underlying physiological mechanisms that result in such a drop in performance. This decline is now viewed as a unique phenotypic biomarker and a hallmark of the aging process. The rates of decline are well documented for sets of traits such as running or swimming but only a limited number of studies have examined the developmental and senescent phases together. Moreover, the few attempts to do so are merely descriptive and do not include any meaningful biological features. Here we propose an averaged and deterministic model, based on cell population dynamics, replicative senescence and functionality loss. It describes the age-related change of performance in 17 time-series phenotypic traits, including human physical and cognitive skills, mouse lemur strength, greyhound and thoroughbred speed, and mouse activity. We demonstrate that the estimated age of peak performance occurs in the early part of life (20.5% ± 6.6% of the estimated lifespan) thus emphasizing the asymmetrical nature of the relationship. This model is an initial attempt to relate performance dynamics to cellular dynamics and will lead to more sophisticated models in the future.

Personality and performance are affected by age and early life parameters in a small primate.

A whole suite of parameters is likely to influence the behavior and performance of individuals as adults, including correlations between phenotypic traits or an individual's developmental context. Here, we ask the question whether behavior and physical performance traits are correlated and how early life parameters such as birth weight, litter size, and growth can influence these traits as measured during adulthood. We studied 486 captive gray mouse lemurs (Microcebus murinus) and measured two behavioral traits and two performance traits potentially involved in two functions: exploration behavior with pull strength and agitation score with bite force. We checked for the existence of behavioral consistency in behaviors and explored correlations between behavior, performance, morphology. We analyzed the effect of birth weight, growth, and litter size, while controlling for age, sex, and body weight. Behavior and performance were not correlated with one another, but were both influenced by age. Growth rate had a positive effect on adult morphology, and birth weight significantly affected emergence latency and bite force. Grip strength was not directly affected by early life traits, but bite performance and exploration behavior were impacted by birth weight. This study shows how early life parameters impact personality and performance.