The importance of social behavior in nonhuman primate studies of aging: A mini-review.

Social behavior plays an important role in supporting both psychological and physical health across the lifespan. People's social lives change as they age, and the nature of these changes differ based on whether people are on healthy aging trajectories or are experiencing neurodegenerative diseases that cause dementia, such as Alzheimer's disease and Parkinson's disease. Nonhuman primate models of aging have provided a base of knowledge comparing aging trajectories in health and disease, but these studies rarely emphasize social behavior changes as a consequence of the aging process. What data exist hold particular value, as negative effects of disease and aging on social behavior are likely to have disproportionate impacts on quality of life. In this mini review, we examine the literature on nonhuman primate models of aging with a focus on social behavior, in the context of both health and disease. We propose that adopting a greater focus on social behavior outcomes in nonhuman primates will improve our understanding of the intersection of health, aging and sociality in humans.

Monkey visual attention does not fall into the uncanny valley.

Very humanlike artificial agents can induce feelings of uneasiness in human perceivers. Stimuli that generate this response are said to occupy "the uncanny valley". Given inconsistent findings in the literature, whether or not nonhuman animals experience the uncanny valley is unclear. Here, we recorded the visual attention of eleven male rhesus monkeys as they viewed faces varying in realness across five levels, with visual attention measured by both number and duration of visual fixations on faces as a whole and on areas of interest within the faces (e.g., eyes, mouth). Face stimuli varied in terms of the realism of the image and behavior depicted by the face (lipsmack, threat, bared teeth, and neutral). We largely found no support that rhesus monkeys perceive an uncanny valley when viewing our stimuli; however, monkeys did generally pay more attention to eyes and less attention to mouths in real images compared to less realistic images. Across all stimuli, monkeys' visual attention was drawn to the mouths of images when teeth were visible. These findings suggest that rhesus monkeys in our study did not display an uncanny valley effect when viewing realistic stimuli but did percieve affective information depicted by faces regardless of how real those faces appear.

Relationship tenure differentially influences pair-bond behavior in male and female socially monogamous titi monkeys (Callicebus cupreus).

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.

Vasopressin, but not oxytocin, modulates responses to infant stimuli in marmosets providing care to dependent infants.

In family-living species, the quality and patterning of caregiving is the product of an individual's role within the family (mother, father, sibling) and parental experience, both of which interact with underlying neurobiological substrates. Among these substrates are the nonapeptides vasopressin and oxytocin, which modulate maternal, paternal, and alloparental care. We used a nonhuman primate model of the "nuclear family," the marmoset (Callithrix jacchus), to investigate relationships between caregiving experience, role within the family, and activation of either the oxytocin or vasopressin systems in shaping responsiveness to offspring. During two phases of offspring development (early infancy, juvenile), mothers, fathers, and older siblings were treated with vasopressin, oxytocin, or saline via intranasal application, and tested for responses to infant distress stimuli in a within-subjects design. Interest in infant stimuli was highest among marmosets that were caring for infants compared to those caring for juveniles, and parentally experienced marmosets were quicker to respond to infant stimuli than first-time caregivers. Moreover, marmosets treated with vasopressin showed enhanced responsiveness to infant stimuli compared to control stimuli only when caring for infants. Thus, in all classes of marmoset caregivers, vasopressin enhances responsiveness to infant-associated stimuli in caregivers during periods in which infant care is most crucial.

Dopamine receptor manipulation does not alter patterns of partner preference in long-term marmoset pairs.

The relationship between socially monogamous mates is dynamic and regulated by neurobiological influences. Research in rodent models has indicated a key role for the neurotransmitter dopamine (DA) and its receptors (DAR) in mediating the formation and maintenance of monogamous bonds. DAR activation was pharmacologically manipulated in marmosets housed in long-term pairs. Marmosets exposed to DAR manipulation were tested in a partner preference test under two social conditions: one in which their mate could visually observe their interactions with an opposite-sex individual, and one in which their pair mate could not visually observe these interactions. Marmosets displayed a spatial preference for the mate compared to an unfamiliar conspecific, however, they displayed a sexual preference for an unfamiliar conspecific over their mate. D1R manipulation had no impact on marmoset partner preference. However, activation of D2Rs reduced the time marmosets spent in contact with either stimulus animal, indicating a decrease in social interest, but did not reduce time spent in proximity to the stimulus animals nor number of sexual solicitations. Additionally, social context (visibility of the mate) did not influence marmoset behavior. These findings suggest that D2Rs may be involved in regulating generalized, but not partner-specific, social interest in marmoset monkeys.

Social Monogamy in Nonhuman Primates: Phylogeny, Phenotype, and Physiology.

Monogamy as a social system has been both a scientific puzzle and a sociocultural issue for decades. In this review, we examine social monogamy from a comparative perspective with a focus on primates, our closest genetic relatives. We break down monogamy into component elements, including pair-bonding and partner preference, mate guarding or jealousy, social attachment, and biparental care. Our survey of primates shows that not all features are present in species classified as socially monogamous, in the same way that human monogamous relationships may not include all elements-a perspective we refer to as "monogamy à la carte." Our review includes a survey of the neurobiological correlates of social monogamy in primates, exploring unique or common pathways for the elemental components of monogamy. This compilation reveals that the components of monogamy are modulated by a suite of androgenic steroids, glucocorticoid hormones, the nonapeptide hormones oxytocin and vasopressin, and other neurotransmitter systems (e.g., dopamine and opioids). We propose that efforts to understand the biological underpinnings of complex human and animal sociosexual relationships will be well served by exploring individual phenotypic traits, as opposed to pursuing these questions with the assumption that monogamy is a unitary trait or a species-specific characteristic.

Early-life Social Adversity and Developmental Processes in Nonhuman Primates.

Most primate species produce offspring that are altricial and highly dependent upon caregivers. As a consequence, a host of developmental trajectories can be dramatically altered by variation in early experiences. We review the impact of early social experiences (in both experimental models and natural contexts) on developmental profiles in three species of nonhuman primates: marmosets, squirrel monkeys, and macaques. Graded exposure to early-life social adversity (ELSA) produces short- to long-term effects on multiple developmental outcomes, including affect, social behavior, cognitive and attentional processes, and in the neural substrates that underlie these sociobehavioral traits.

Oxytocin modulates behavioral and physiological responses to a stressor in marmoset monkeys.

Social isolation is a major source of stress and can lead to activation of the hypothalamic-pituitary-adrenal (HPA) axis. The presence of a close social partner can reduce the magnitude of the HPA-axis response during a stressor, a phenomenon known as social buffering. The oxytocin (OXT) system has been identified as one candidate for mediating social buffering due to its role in the facilitation of social bonding and the expression of prosocial behavior. The goal of the present study was to determine whether the OXT system contributes to social buffering of HPA-axis activity in response to stressor exposure in marmoset monkeys (Callithrix jacchus). Male and female marmosets experienced a standardized psychogenic stressor with and without their long-term mate under OXT-treatments (Pro(8)-OXT, Leu(8)-OXT, OXT antagonist, and saline); we assessed HPA-axis activity by measuring urinary cortisol across the stressor. We found that blocking, but not augmenting, the OXT system altered patterns of cortisol and proximity behavior in response to a stressor. We demonstrated that (1) the presence of a mate during a stressor significantly attenuated HPA-axis activity in female, but not male, marmosets; (2) male, but not female, marmosets treated with an OXT antagonist had significantly higher HPA-axis activity across the stressor than when they were treated with saline, suggesting that the OXT system may reduce the stressor-induced rise in cortisol levels; (3) male and female marmosets treated with an OXT antagonist spent significantly less time in close proximity to their mate during the first 30 min of the stressor than when they were treated with saline, suggesting that the OXT system may be important for the expression of partner-seeking behavior during a stressor. Thus, the OXT system and social context differentially influenced how the HPA-axis responded to a stressor in male and female marmosets, and may modulate HPA-axis activity by promoting the expression of proximity behavior with a close social partner.

Development of a partner preference test that differentiates between established pair bonds and other relationships in socially monogamous titi monkeys (Callicebus cupreus).

Partner preference, or the selective social preference for a pair mate, is a key behavioral indicator of social monogamy. Standardized partner preference testing has been used extensively in rodents but a single test has not been standardized for primates. The goal of this study was to develop a partner preference test with socially monogamous titi monkeys (Callicebus cupreus) adapted from the widely used rodent test. In Experiment 1, we evaluated the test with pairs of titi monkeys (N = 12) in a three-chambered apparatus for 3 hr. The subject was placed in the middle chamber, with grated windows separating it from its partner on one side and an opposite sex stranger on the other side. Subjects spent a greater proportion of time in proximity to their partners' windows than the strangers', indicating a consistent preference for the partner over the stranger. Touching either window did not differ between partners and strangers, suggesting it was not a reliable measure of partner preference. Subjects chose their partner more than the stranger during catch and release sessions at the end of the test. In Experiment 2, we compared responses of females with current partners (N = 12) in the preference test with other relationship types representing former attachment bonds (N = 13) and no attachment bond (N = 8). Only females from established pair bonds spent significantly more time near their partner's window compared to the stranger's indicating that this measure of preference was unique to current partners. Other measures of preference did not differentiate behavior toward a current partner and other relationship types. This test reproduces behavioral patterns found in previous studies in titi monkeys highlighting the accuracy of this new partner preference test. This test can be used as a standardized measure of partner preference in titi monkeys to quantitatively study pair bonding and evaluate factors influencing partner preference.