Nonverbal face-to-face interactions in macaques and humans: A translational pilot study.

Human and nonhuman primate mother-infant dyads engage in face-to-face interactions critical for optimal infant development. In semi-free-ranging rhesus macaques (Macaca mulatta), maternal primiparity and infant sex influence the expression of nonverbal face-to-face mother-infant interactions. However, whether similar patterns of variation exist in laboratory-housed macaques or human mothers is not well understood. Comparing both species would yield information regarding the translational validity of macaques to humans in this important social/developmental domain. In this pilot study, we first compared semi-free-ranging (n = 39) and laboratory-housed (n = 20) macaques, finding that laboratory-housed dyads, first-time mothers, and mothers of sons engaged in higher rates of face-to-face interactions regardless of housing. After translating the nonhuman primate coding scheme for use in a small but diverse group of human mother-infant dyads (N = 27; 44.4% African American, 18.5% American Indian, 7.4% Asian/Asian American, and 29.6% White), we found that, like macaques, human mothers of sons engaged in more face-to-face interactions; however, experienced (vs. first-time) mothers engaged in more interactions. Macaques and humans also engaged in species-specific interactions with their infants. We conclude that components of caregiver-infant nonverbal face-to-face interactions are translatable across human and nonhuman primate species and represent an exciting avenue for future caregiving work.

Amniotic fluid cortisol predicts neonatal and infant development in non-stressed rhesus monkeys: Implications for prenatal stress.

Prenatal stress adversely affects offspring development, with fetal cortisol (CORT) exposure being a primary hypothesized mechanism for stress-induced developmental deficits. Fetal CORT exposure can be assessed via measurements in amniotic fluid. However, in humans, amniocentesis is typically only performed for clinical reasons such as karyotyping; thus, amniotic fluid CORT cannot be obtained from a random sample. To test the hypothesis that fetal CORT exposure predicts neonatal and infant development in healthy primates, we measured amniotic fluid CORT in N = 18 healthy rhesus macaque (Macaca mulatta) dams (50:50 female:male infants) between 80 and 124 days gestation (mean ± SEM = 98.3 ± 2.9 days out of 165 days gestational length; i.e., second trimester). Maternal hair cortisol concentrations (HCCs) were assessed throughout pregnancy and lactation. Offspring were assessed for physical growth, neurological development, cognitive development, and HCCs across postnatal days 30-180. Controlling for gestational age at amniocentesis, higher amniotic fluid CORT significantly predicted slower infant growth rate (g/day) in the first 30 days (ß = -0.19; R2 = 0.71, p = .008), poorer sensorimotor scores on the day 30 neonatal assessment (ß = -0.28; R2 = 0.76, p = .015), and longer time to complete training (ß = 0.48; R2 = 0.54, p = .026), but better performance (ß = 0.91; R2 = 0.60, p = .011) on a discrimination cognitive task at 120-180 days. Amniotic fluid CORT was not associated with maternal or infant HCCs. Although these results are correlative, they raise the intriguing possibility that fetal CORT exposure in non-stress-exposed primates, as measured by amniotic fluid CORT, programs multiple aspects of neonatal and infant development. On the other hand, amniotic fluid CORT may not relate to chronic CORT levels in either mothers or infants when assessed by hair sampling.

Early life adversities and lifelong health outcomes: A review of the literature on large, social, long-lived nonhuman mammals.

Social nonhuman animals are powerful models for studying underlying factors related to lifelong health outcomes following early life adversities (ELAs). ELAs can be linked to lifelong health outcomes depending on the species, system, sensitive developmental periods, and biological pathways. This review focuses on the literature surrounding ELAs and lifelong health outcomes in large, social, relatively long-lived nonhuman mammals including nonhuman primates, canids, hyenas, elephants, ungulates, and cetaceans. These mammals, like humans but unlike the most-studied rodent models, have longer life histories, complex social structures, larger brains, and comparable stress and reproductive physiology. Collectively, these features make them compelling models for comparative aging research. We review studies of caregiver, social, and ecological ELAs, often in tandem, in these mammals. We consider experimental and observational studies and what each has contributed to our knowledge of health across the lifespan. We demonstrate the continued and expanded need for comparative research to inform about the social determinants of health and aging in both humans and nonhuman animals.

Are hair cortisol levels dependent on hair growth rate? A pilot study in rhesus macaques.

Research incorporating the analysis of glucocorticoids, specifically cortisol, in hair samples has exploded over the past 10-15 years, yet factors contributing to the accumulation of cortisol in hair are not yet fully characterized. In particular, it is not clear whether cortisol accumulation in hair is dependent on hair growth rate, a possibility raised by prior rodent studies reporting glucocorticoid-mediated inhibition of hair growth. Using rhesus macaque monkeys (Macaca mulatta), an extensively studied nonhuman primate species, the present pilot study evaluated the hypothesis that hair cortisol accumulation is inversely related to hair growth rate (i.e., slower hair growth leading to elevated cortisol levels). Hair samples were collected from 19 adult female macaques and 17 infants (9 males) 3 months apart using a shave-reshave procedure from the same site below the posterior vertex of the scalp. The second hair samples were measured to the nearest millimeter (mm) for growth rate over the previous 3 months and assayed for hair cortisol concentrations (HCCs) using enzyme immunoassay. Because of the possibility of age-related differences in hair growth rate, correlational analyses were performed separately for adults and infants to determine whether HCC values were associated with growth rate in each age group. These analyses revealed that neither group displayed a significant correlation of HCCs with hair growth. The results additionally showed that overall, adults had a faster hair growth rate than infants and, as expected from previous studies, had lower HCCs than infants. Our results suggest that higher HCCs within the non-stress range do not result from cortisol-mediated inhibition of hair growth. Moreover, similarities between humans and macaque monkeys in both HPA axis regulation and hair growth rates argue that these findings are relevant for human hair cortisol studies. Extrapolation to other species in which the features of hair growth and the relevant regulatory mechanisms are less well understood should be done with caution.

Human milk: From complex tailored nutrition to bioactive impact on child cognition and behavior.

Human milk is a highly complex liquid food tailor-made to match an infant's needs. Beyond documented positive effects of breastfeeding on infant and maternal health, there is increasing evidence that milk constituents also impact child neurodevelopment. Non-nutrient milk bioactives would contribute to the (long-term) development of child cognition and behavior, a process termed 'Lactocrine Programming'. In this review we discuss the current state of the field on human milk composition and its links with child cognitive and behavioral development. To promote state-of-the-art methodologies and designs that facilitate data pooling and meta-analytic endeavors, we present detailed recommendations and best practices for future studies. Finally, we determine important scientific gaps that need to be filled to advance the field, and discuss innovative directions for future research. Unveiling the mechanisms underlying the links between human milk and child cognition and behavior will deepen our understanding of the broad functions of this complex liquid food, as well as provide necessary information for designing future interventions.

100 years of comparative psychology advancing practice, policy, and the public-And what the future requires.

This year marks the 100th anniversary since the inception of the original Journal of Comparative Psychology. This review highlights the evolution of Journal of Comparative Psychology and the field of comparative psychology over the past century through the lens of the field's contributions in the realms of science practice, science policy, and public opinion. The review culminates with a look ahead to the next 100 years, with both challenges that are likely to remain as well as potential paths to continue growth and success. (PsycInfo Database Record (c) 2021 APA, all rights reserved).

Behavioral and hormonal changes following social instability in young rhesus macaques (Macaca mulatta).

Social instability (SI) occurs when there is competition over social status. Reduced certainty of social status can lead to heightened aggression, which can increase physiological stress responses as individuals prepare to fight for their social status. However, adults can use proactive coping mechanisms to reduce the physiological stress induced by SI, such as increasing affiliation. Very little is known, however, about the behavioral and hormonal effects of SI early in development. Filling these gaps in knowledge would add to the fields of primatology and developmental and comparative psychology. We conducted an opportunistic study of a peer group of 18 rhesus macaque (Macaca mulatta) yearlings before and during SI. We used social network analysis to measure individuals' dominance certainty (DC; in their aggressive and submissive network) and their position in affiliative networks (grooming and play) and analyzed hair cortisol concentrations (HCCs). As predicted, during SI, we observed a decrease in DC, indicating that individuals had less stable dominance positions. As well, during SI, we observed increased rates of social grooming and decreased rates of social play, reflecting potential coping mechanisms. More socially connected individuals in social grooming and social play networks received higher levels of coalitionary support. Contrary to predictions, DC did not predict HCCs; rather, individuals that were more connected in the social play network exhibited smaller increases in HCCs during SI, revealing a potential buffering effect of social play. Our results underscore the need for further research on the effects of SI during ontogeny. (PsycInfo Database Record (c) 2021 APA, all rights reserved).

The prefrontal cortex in a pandemic: Restoring functions with system-, family-, and individual-focused interventions.

The COVID-19 pandemic is an unanticipated and uncontrollable chronic stressor that is detrimental to the mental and behavioral health of children and families, particularly those from disadvantaged and marginalized backgrounds. Chronic stress impairs a myriad of prefrontal cortical functions, important for coping with the COVID-19 pandemic, and has consequences on dyadic parent-child functioning. Informed by neuroscience and clinical evidence, sensitive parenting is a vital avenue of intervention that buffers against the toxic effects of COVID-19 on parent-child mental health. In the context of the COVID-19 pandemic, we first discuss the neurobiological, psychological, and behavioral mechanisms behind exacerbated mental health risks in families. We then highlight the role of sensitive parenting as a buffer against stress-related mental health problems, and conclude with recommendations for systemic-, family-, and individual-interventions to most effectively address stress-related mental health problems and their impact on children and families during the COVID-19 pandemic. (PsycInfo Database Record (c) 2021 APA, all rights reserved).

Impacts of early social experience on cognitive development in infant rhesus macaques.

Although much is known about the influences of early life experiences on the neurobiology and behavior of macaque models of child development, there is scant literature on cognitive development with respect to early rearing. Here, we examined the effects of rearing condition on affective reactivity and cognitive development in infant rhesus macaques. Infants were pseudo-randomly assigned to one of the two rearing conditions: nursery reared (NR, N = 32; 16 peer-reared, 16 surrogate-peer-reared) or mother-peer-reared (MPR, N = 7). During the first month of life, infants were administered the Primate Neonatal Neurobehavioral Assessment (PNNA). Beginning at 4 months old, infants were tested on cognitive tasks that assessed reward association, cognitive flexibility, and impulsivity. We found no gross cognitive differences between MPR and NR infants. However, MPR infants were more reactive than NR infants on the PNNA. Additionally, reactivity on the PNNA correlated with impulsivity, such that infants who were more reactive at 1 month of age completed fewer trials correctly on this task at 8-10 months. These findings are the first to directly compare cognitive development in MPR and NR infants, and add to the existing literature elucidating the influences of early social experience on temperament and development.

Dominance rank predicts social network position across developmental stages in rhesus monkeys.

Social network analysis is increasingly common in studying complex interactions among individuals. Across a range of primates, high-ranking adults are generally more socially connected, which results in better fitness outcomes. However, it still remains unclear whether this relationship between social network position and dominance rank emerges in infancy and whether, in species with a social transmission of dominance rank, social network positions are driven by the presence of the mother. To fill this gap, we first explored whether dominance ranks were related to social network position, measured via eigenvector centrality, in infants, juveniles, and adults in a troop of semi-free-ranging rhesus macaques (Macaca mulatta). We then examined relationships between dominance rank and eigenvector centrality in a peer-only group of yearlings who were reared with their mothers in either a rich, socially complex environment of multigenerational (MG) kin support or a unigenerational group of mothers and their infants from birth through 8 months. In Experiment 1, we found that mother's network position predicted offspring network position and that dominants across all age categories were more central in affiliative networks (social contact, social grooming, and social play). Experiment 2 showed that high-ranking yearlings in a peer-only group were more central only in the social contact network. Moreover, yearlings reared in a socially complex environment of MG kin support were more central. Our findings suggest that the relationship between dominance rank and social network position begins early in life, and that complex early social environments can promote later social competency. Our data add to the growing body of evidence that the presence/absence of the mother and kin influence how dominance rank affects social network position. These findings have important implications for the role of caregivers in the social status of developing primates, which ultimately ties to health and fitness outcomes.

A descriptive analysis of gut microbiota composition in differentially reared infant rhesus monkeys (Macaca mulatta) across the first 6 months of life.

The gastrointestinal microbiome is recognized as a critical component in host immune function, physiology, and behavior. Early life experiences that alter diet and social contact also influence these outcomes. Despite the growing number of studies in this area, no studies to date have examined the contribution of early life experiences on the gut microbiome in infants across development. Such studies are important for understanding the biological and environmental factors that contribute to optimal gut microbial colonization and subsequent health. We studied infant rhesus monkeys (Macaca mulatta) across the first 6 months of life that were pseudo-randomly assigned to one of two different rearing conditions at birth: mother-peer-reared (MPR), in which infants were reared in social groups with many other adults and peers and nursed on their mothers, or nursery-reared (NR), in which infants were reared by human caregivers, fed formula, and given daily social contact with peers. We analyzed the microbiome from rectal swabs (total N = 97; MPR = 43, NR = 54) taken on the day of birth and at postnatal Days 14, 30, 90, and 180 using 16S rRNA gene sequencing. Bacterial composition differences were evident as early as 14 days, with MPR infants exhibiting a lower abundance of Bifidobacterium and a higher abundance of Bacteroides than NR infants. The most marked differences were observed at 90 days, when Bifidobacterium, Lactobacillus, Streptococcus, Bacteroides, Clostridium, and Prevotella differed across rearing groups. By Day 180, no differences in the relative abundances of the bacteria of interest were observed. These novel findings in developing primate neonates indicate that the early social environment as well as diet influence gut microbiota composition very early in life. These results also lay the groundwork for mechanistic studies examining the effects of early experiences on gut microbiota across development with the ultimate goal of understanding the clinical significance of developmental changes.

Interindividual differences in neonatal sociality and emotionality predict juvenile social status in rhesus monkeys.

In humans, socioeconomic status (SES) has profound outcomes on socio-emotional development and health. However, while much is known about the consequences of SES, little research has examined the predictors of SES due to the longitudinal nature of such studies. We sought to explore whether interindividual differences in neonatal sociality, temperament, and early social experiences predicted juvenile social status in rhesus monkeys (Macaca mulatta), as a proxy for SES in humans. We performed neonatal imitation tests in infants' first week of life and emotional reactivity assessments at 2 and 4 weeks of age. We examined whether these traits, as well as the rearing environment in the first 8 months of life (with the mother or with same-aged peers only) and maternal social status predicted juvenile (2-3 years old) social status following the formation of peer social groups at 8 months. We found that infants who exhibited higher rates of neonatal imitation and newborn emotional reactivity achieved higher social status as juveniles, as did infants who were reared with their mothers, compared to infants reared with peers. Maternal social status was only associated with juvenile status for infant dyads reared in the same maternal group, indicating that relative social relationships were transferred through social experience. These results suggest that neonatal imitation and emotional reactivity may reflect ingrained predispositions toward sociality that predict later outcomes, and that nonnormative social experiences can alter socio-developmental trajectories. Our results indicate that neonatal characteristics and early social experiences predict later social outcomes in adolescence, including gradients of social stratification.

Cortisol in Neonatal Mother's Milk Predicts Later Infant Social and Cognitive Functioning in Rhesus Monkeys.

Milk provides not only the building blocks for somatic development but also the hormonal signals that contribute to the biopsychological organization of the infant. Among mammals, glucocorticoids (GCs) in mother's milk have been associated with infant temperament. This study extended prior work to investigate rhesus monkey (Macaca mulatta) mother-infant dyads (N = 34) from birth through 8 months postpartum. Regression analysis revealed that cortisol concentrations in milk during the neonatal period predicted impulsivity on a cognitive task, but not global social behaviors, months later. During this time period, sex-differentiated social behavior emerged. For female infants, milk cortisol concentrations predicted total frequency of play. Collectively, these findings support and extend the "lactational programming" hypothesis on the impact of maternal-origin hormones ingested via milk.

Sex and rank affect how infant rhesus macaques look at faces.

We investigated how differences in infant sex and mothers' dominance status affect infant rhesus macaques' (Macaca mulatta) interest in visually exploring emotional facial expressions. Thirty-eight infants were presented with animated avatars of macaque facial expressions during the first month of life. Sons of high-ranking mothers looked more at faces, especially the eye region, than sons of low-ranking mothers, but no difference in looking duration was found for daughters. Males looked significantly more at eyes than females, but this effect was reversed in infants who were reared without mothers in a primate nursery facility. In addition, in mother-infant interactions, mothers of sons were more likely to gaze at their infant's face compared to mothers of daughters. Combined with previous research indicating that rhesus macaque mothers interact differently with infants based on their own rank and infant's sex, these results support the view that social experiences shape early face preferences in rhesus macaques.

Rank acquisition in rhesus macaque yearlings following permanent maternal separation: The importance of the social and physical environment.

Rank acquisition is a developmental milestone for young primates, but the processes by which primate yearlings attain social rank in the absence of the mother remain unclear. We studied 18 maternally reared yearling rhesus macaques (Macaca mulatta) that differed in their social and physical rearing environments. We found that early social experience and maternal rank, but not individual traits (weight, sex, age), predicted dominance acquisition in the new peer-only social group. Yearlings also used coalitions to reinforce the hierarchy, and social affiliation (play and grooming) was likely a product, rather than a determinant, of rank acquisition. Following relocation to a familiar environment, significant rank changes occurred indicating that familiarity with a physical environment was salient in rank acquisition. Our results add to the growing body of literature emphasizing the role of the social and physical environment on behavioral development, namely social asymmetries among peers.

Relationships between affiliative social behavior and hair cortisol concentrations in semi-free ranging rhesus monkeys.

Sociality is a fundamental aspect of human behavior and health. One benefit of affiliative social relationships is reduced short-term levels of glucocorticoids (GCs), which are indicative of physiological stress. Less is known, however, about chronic GC production in relation to affiliative social behavior. To address this issue, we studied a semi-free ranging troop of rhesus macaques (Macaca mulatta) and collected hair samples to measure hair cortisol concentrations (HCCs), as a measure of chronic GC production, during routine biannual exams. We collected social behavior (both aggressive and affiliative) and hair samples for 32 adult female rhesus macaques over one year (Experiment 1). Our results indicated that adult females who initiated higher levels of social affiliation had significantly lower levels of HCCs. Neither the initiation nor the receipt of aggression were significantly related to HCCs in this study. In a second experiment we studied 28 mother-infant dyads for the first 90days postpartum to examine mother-infant facial interactions (i.e. mutual gazing). We analyzed HCCs during weaning approximately one year later, which is a major transitional period. We found that infants that engaged in higher levels of mutual gazing in the first 90days postpartum had significantly lower levels of HCCs during weaning. Finally, we studied 17 infant rhesus macaques (13 males) to examine whether social behavior (such as play) in the first five months of life correlated with infant HCCs over those months (Experiment 3). We found that infant males that engaged in more social play had significantly lower levels of HCCs. By relying on an animal model, our study shows that affiliative social traits are associated with lower long-term GC production. Future research should address the complex interactions between social behavior, chronic GC production, and mental and physical health.

Elo-rating for Tracking Rank Fluctuations after Demographic Changes Involving Semi-free-ranging Rhesus Macaques (Macaca mulatta).

Rhesus macaques (Macaca mulatta) are gregarious primates that form despotic societies characterized by frequent and intense aggression. Within long-term social groups, demographic changes may influence hierarchical stability, potentially resulting in conflict and violently abrupt hierarchical changes. This conflict can result in serious implications for animal welfare, and thus, predictive tools would be invaluable to captive managers in determining social instabilities. Using the method Elo-rating to track rank changes and dominance stability, we predicted that demographic changes to a population of semi-free ranging rhesus macaques would result in changes in hierarchical stability. Over a 3 y period, dominance data were recorded on all troop members to track the hierarchy. Throughout the 3 y, significant changes occurred to the population (mainly due to health and colony management reasons; no changes specifically occurred for this study) including permanent removal of a large group of natal males, temporary and permanent removal of top-ranking females, and depositions of top-ranking families. Our retrospective study suggests that removing natal males was beneficial in promoting overall troop stability (that is, stability of dominance relationships), although remaining males opportunistically attempted to increase in rank, perhaps due to limited competition. Our results also suggest that removing top-ranking females, even temporarily, destabilized dominance relationships; consequently adjacently ranked females opportunistically increased in Elo-rating, both before and after the depositions of the α families. Thus, these challenges to the established hierarchy can be predicted by increases in Elo-rating within the ß families after demographic changes to the α families. Our results suggest that the presence of natal males and the removal of top-ranking females should be minimized to maintain stable dominance relationships. In addition, longitudinal data reflecting dominance ranks, collected by using Elo-rating, may help managers of captive colonies in predicting dominance instabilities before they occur.

Differential relationships between chronic hormone profiles in pregnancy and maternal investment in rhesus monkey mothers with hair loss in the neonatal period.

Hair loss is commonly used as an indicator of well being in primate facilities, yet it has been shown to also occur in otherwise healthy pregnant and postpartum females. There is significant variability in the incidence of hair loss during these important developmental periods, reasons for which remain unclear. We studied female rhesus monkeys (Macaca mulatta, n = 47) with and without hair loss in pregnancy/postpartum. We hypothesized that, similar to previously published reports, pregnancy would result in an increased likelihood of hair loss, and that hair loss would be correlated with higher hair cortisol concentrations (HCCs). We further hypothesized that hair loss among pregnant females is related to differential maternal investment. We studied a subset of monkeys (n = 26) from mid-to-late pregnancy through peak lactation, some of which exhibited hair loss in the perinatal period (n = 15), and some of which did not (n = 11). We examined fetal measurements, infant birth weight, infant growth rate, and milk yield volume (MYV) in the first 30 days as indices of investment. We found that pregnant monkeys showed a greater incidence of hair loss across the study year (χ2(2) = 6.55, P = 0.038), and that mothers with hair loss had significantly higher HCCs in pregnancy than those without (F(2,28) = 3.8, P = 0.017, ηp2 = 0.21). HCCs in pregnancy were correlated with severity of hair loss in the neonatal period (r(37) = 0.42, P = 0.008). Moreover, HCCs in pregnancy were positively correlated with infant birth weight (r(12) = 0.56, P = 0.038), infant growth rate (r(12) = 0.64, P = 0.014), and MYV (r(11) = 0.85, P < 0.001) for alopecic but not non-alopecic mothers. These mothers did not differ in fetal measurements, infant birth weight/growth rate, or MYV. Our results suggest that hair loss in some monkeys, especially during the birthing season, may be a signal of greater physiological stress during pregnancy and differential investment by mothers to their offspring. Am. J. Primatol. 79:e22489, 2017. © 2015 Wiley Periodicals, Inc.