Evidence for kinship information contained in the rhesus macaque (Macaca mulatta) face

The ability to recognize kin is an important social skill for primates. Humans are adept at using facial similarity to recognize likely kin, and there is evidence that nonhuman primates are also able to use facial similarity to make judgments about kinship. However, if and how nonhuman primate faces actually contain kinship information remains unclear. To test whether there is objectively measurable facial similarity in related nonhuman primates, we compared facial measurements from related (paternal half-sisters) and unrelated adult female rhesus macaques (Macaca mulatta). Facial measurements were first summarized into 5 factors using a principal component analysis. Differences in these factors between the faces of related macaques were compared with differences between the faces of random unrelated macaques and of age-matched unrelated macaques. The difference in facial measurements between related macaques was significantly smaller than the difference in facial measurements of either group of unrelated macaques, constituting an objective measure of facial similarity in macaque kin. These results indicate that kinship information is contained in the rhesus macaque face and suggest that nonhuman primates may rely in part on facial similarity to distinguish kin

A new look at neurobehavioral development in rhesus monkey neonates (Macaca mulatta)

The Brazelton Neonatal Behavioral Assessment Scale (NBAS) evaluates a newborn infant’s autonomic, motor, state, temperament, and social-attentional systems, which can help to identify infants at risk of developmental problems. Given the prevalence of rhesus monkeys being used as an animal model for human development, here we aimed to validate a standardized test battery modelled after the NBAS for use with non-human primates called the Infant Behavioral Assessment Scale (IBAS), employing exploratory structural equation modeling using a large sample of rhesus macaque neonates (N=1056). Furthermore, we examined the repeated assessments of the common factors within the same infants to describe any changes in performance over time, taking into account two independent variables (infant sex and rearing condition) that can potentially affect developmental outcomes. Results revealed three factors (Orientation, State Control, and Motor Activity) that all increased over the first month of life. While infant sex did not have an effect on any factor, nursery-rearing led to higher scores on Orientation but lower scores on State Control and Motor Activity. These results validate the IBAS as a reliable and valuable research tool for use with rhesus macaque infants and suggest that differences in rearing conditions can affect developmental trajectories and potentially pre-expose infants to heightened levels of cognitive and emotional deficiencies

Sensitivity to first-order relations of facial elements in infant rhesus macaques: first-order relations of facial elements in infant macaques

Faces are visually attractive to both human and nonhuman primates. Human neonates are thought to have a broad template for faces at birth and prefer face-like to non-face-like stimuli. To better compare developmental trajectories of face processing phylogenetically, here we investigated preferences for face-like stimuli in infant rhesus macaques using photographs of real faces. We presented infant macaques aged 15–25days with human, macaque, and abstract faces with both normal and linear arrangements of facial features, and measured infants’ gaze durations, number of fixations, and latency to look to each face using eye-tracking technology. There was an overall preference for normal over linear facial arrangements for abstract and monkey faces, but not human faces. Moreover, infant macaques looked less at monkey faces than at abstract or human faces. These results suggest that species and facial configurations affect face processing in infant macaques, and we discuss potential explanations for these findings. Further, carefully controlled studies are required to ascertain whether infant macaques’ face template can be considered as broad as human infants’ face template

Evolutionary relevance and experience contribute to face discrimination in infant macaques (Macaca mulatta)

In human children and adults, familiar face types—typically own-age and own-species faces—are discriminated better than other face types; however, human infants do not appear to exhibit an own-age bias but instead better discriminate adult faces, which they see more often. There are two possible explanations for this pattern: Perceptual attunement predicts advantages in discrimination for the most experienced face types. Additionally or alternatively, there may be an experience-independent bias for infants to discriminate own-species faces, an adaptation for evolutionarily relevant faces. These possibilities have not been disentangled in studies thus far, and these studies did not control infants’ early experiences with faces. In the present study, we tested these predictions in infant macaques (Macaca mulatta) reared under controlled environments, not exposed to adult conspecifics. We measured newborns’ (15–25 days; n = 27) and 6- to 7-month-olds’ (n = 35) discrimination of human and macaque faces at 3 ages—young infants, old infants, and adults—in a visual paired comparison task. We found that 6- to 7-month-olds were the best at discriminating adult macaque faces; however, in the first few seconds of looking, tthey additionally discriminated familiar face types—same-aged peer and adult human faces—thereby highlighting the importance of experience with certain face categories. The present data suggest that macaque infants possess both experience-independent and experientially tuned face biases. In human infants, early face skills may likewise be driven by both experience and evolutionary relevance; future studies should consider both of these factors

Capuchin monkeys display affiliation toward humans who imitate them

During social interactions, humans often unconsciously and unintentionally imitate the behaviors of others, which increases rapport, liking, and empathy between interaction partners. This effect is thought to be an evolutionary adaptation facilitating group living, and may therefore be shared with other primate species. Here we show that capuchin monkeys, a highly social primate species, prefer human imitators in a variety of ways: they look longer at imitators, spend more time in proximity to imitators, and choose to interact more frequently with imitators in a token exchange task. These results demonstrate that imitation can promote affiliation in nonhuman primates. Behavior matching that leads to prosocial behaviors towards others may have been one of the mechanisms at the basis of altruistic behavioral tendencies in capuchins and in other primates including humans

A modified mark test for own-body recognition in pig-tailed macaques (Macaca nemestrina)

Classic mirror self-recognition mark tests involve familiarizing the subject with its mirror image, surreptitiously applying a mark on the subject’s eyebrow, nose, or ear, and measuring self-directed behaviors towards the mark. For many non-human primate species, however, direct gaze at the face constitutes an aggressive and threatening signal. It is therefore possible that monkeys fail the mark test because they do not closely inspect their faces in a mirror and hence they have no expectations about their physical appearance. In the current study we prevented 2 pig-tailed macaques (Macaca nemestrina) from seeing their own faces in a mirror and we adopted a modified version of the classic mark test in which monkeys were marked on the chest, a body region to which they normally have direct visual access but that in the current study was visible only via a mirror. Neither monkey tried to touch the mark on its chest, possibly due to a failure to understand the mirror as a reflective surface. To further the monkeys’ understanding of the mirror image, we trained them to reach for food using the mirror as the only source of information. After both monkeys had learned mirror-mediated reaching, we replicated the mark test. In this latter phase of the study, only 1 monkey scratched the red dye on the chest once. The results are consistent with other findings suggesting that monkeys are not capable of passing a mark test, and imply that face and body recognition rely on the same cognitive abilities

Distinct EEG amplitude suppression to facial gestures as evidence for a mirror mechanism in newborn monkeys

At birth, human infants and newborns of other primate species demonstrate the capacity to attend and to respond to facial stimuli provided by a caregiver. Newborn infants are also capable of exhibiting a range of facial expressions. Identification of the neural underpinnings of these capacities represents a formidable challenge in understanding social development. One possible neuronal substrate is the mirror-neuron system assumed to activate shared motor cortical representations for both observation and production of actions. We tested this hypothesis by recording scalp electroencephalogram (EEG) from 1–7 days old newborn rhesus macaques who were observing and producing facial gestures. We found that 5–6 Hz EEG activity was suppressed both when the infants produced facial gestures and while they were observing facial gestures of a human experimenter, but not when they were observing non-biological stimuli. These findings demonstrate the presence of neural reactivity for biological, communicatively-relevant stimuli which may be a likely signature of neuronal mirroring. The basic elements of the mirror-neuron system appear to operate from the very first days of life and contribute to the encoding of socially relevant stimuli

Socially-mediated arousal and contagion within domestic chick broods

Emotional contagion – an underpinning valenced feature of empathy – is made up of simpler, potentially dissociable social processes which can include socially-mediated arousal and behavioural/physiological contagion. Previous studies of emotional contagion have often conflated these processes rather than examining their independent contribution to empathic response. We measured socially-mediated arousal and contagion in 9-week old domestic chicks (n = 19 broods), who were unrelated but raised together from hatching. Pairs of observer chicks were exposed to two conditions in a counterbalanced order: air puff to conspecifics (AP) (during which an air puff was applied to three conspecifics at 30 s intervals) and control with noise of air puff (C) (during which the air puff was directed away from the apparatus at 30 s intervals). Behaviour and surface eye temperature of subjects and observers were measured throughout a 10-min pre-treatment and 10-min treatment period. Subjects and observers responded to AP with increased freezing, and reduced preening and ground pecking. Subjects and observers also showed reduced surface eye temperature - indicative of stress-induced hyperthermia. Subject-Observer behaviour was highly correlated within broods during both C and AP conditions, but with higher overall synchrony during AP. We demonstrate the co-occurrence of socially-mediated behavioural and physiological arousal and contagion; component features of emotional contagion

Neonatal face-to-face interactions promote later social behaviour in infant rhesus monkeys

In primates, including humans, mothers engage in face-to-face interactions with their infants, with frequencies varying both within and across species. However, the impact of this variation in face-to-face interactions on infant social development is unclear. Here we report that infant monkeys (Macaca mulatta) who engaged in more neonatal face-to-face interactions with mothers have increased social interactions at 2 and 5 months. In a controlled experiment, we show that this effect is not due to physical contact alone: monkeys randomly assigned to receive additional neonatal face-to-face interactions (mutual gaze and intermittent lip-smacking) with human caregivers display increased social interest at 2 months, compared with monkeys who received only additional handling. These studies suggest that face-to-face interactions from birth promote young primate social interest and competenc

Inhaled oxytocin increases positive social behaviors in newborn macaques

Early caregiver–infant interactions are critical for infants’ socioemotional and cognitive development. Several hormones and neuromodulators, including oxytocin, affect these interactions. Exogenous oxytocin promotes social behaviors in several species, including human and nonhuman primates. Although exogenous oxytocin increases social function in adults—including expression recognition and affiliation—it is unknown whether oxytocin can increase social interactions in infants. We hypothesized that nebulized oxytocin would increase affiliative social behaviors and such effects would be modulated by infants’ social skills, measured earlier in development. We also hypothesized that oxytocin’s effects on social behaviors may be due to its anxiolytic effects. We tested these hypotheses in a blind study by nebulizing 7- to 14-d-old macaques (n = 28) with oxytocin or saline. Following oxytocin administration, infants’ facial gesturing at a human caregiver increased, and infants’ salivary oxytocin was positively correlated with the time spent in close proximity to a caregiver. Infants’ imitative skill (measured earlier in development: 1–7 d of age) predicted oxytocin-associated increases in affiliative behaviors—lip smacking, visual attention to a caregiver, and time in close proximity to a caregiver—suggesting that infants with higher propensities for positive social interactions are more sensitive to exogenous oxytocin. Oxytocin also decreased salivary cortisol, but not stress-related behaviors (e.g., scratching), suggesting the possibility of some anxiolytic effects. To our knowledge, this study provides the first evidence that oxytocin increases positive social behaviors in newborns. This information is of critical importance for potential interventions aimed at ameliorating inadequate social behaviors in infants with higher likelihood of developing neurodevelopmental disorder