Annika Paukner

Capuchin Monkeys Display Affiliation Toward Humans Who Imitate Them

Monkey See Human Do Imitation has been put forth as one mechanism through which cultural learning occurs. Paukner et al. (p. 880; see the Perspective by Call and Carpenter) now demonstrate that imitation may also contribute to prosocial behaviors. Capuchin monkeys behaved in a more affiliative manner—as assessed by direction of gaze, physical proximity, and token exchange—toward humans who imitated them as compared to humans who performed the same movements, but did not do so simultaneously. The chameleon effect also operates in monkeys. 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 that facilitates group living and may be shared with other primate species. Here, we show that capuchin monkeys, a highly social primate species, prefer human imitators over non-imitators in a variety of ways: The monkeys 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 toward others may have been one of the mechanisms at the basis of altruistic behavioral tendencies in capuchins and in other primates, including humans.

Reciprocal Face-to-Face Communication between Rhesus Macaque Mothers and Their Newborn Infants

Human mothers interact emotionally with their newborns through exaggerated facial expressions, speech, mutual gaze, and body contact, a capacity that has long been considered uniquely human [1-4]. Current developmental psychological theories propose that this pattern of mother-infant exchange promotes the regulation of infant emotions [4-6] and serves as a precursor of more complex forms of social exchange including perspective taking and empathy. Here we report that in rhesus macaques, mother-infant pairs also communicate intersubjectively via complex forms of emotional exchanges including exaggerated lipsmacking, sustained mutual gaze, mouth-mouth contacts, and neonatal imitation. Infant macaques solicit their mothers affiliative responses and actively communicate to her. However, this form of communication disappears within the infants first month of life. Our data challenge the view that the mother-infant communicative system functions in order to sustain proximity and that infants are simply passive recipients in such interaction. Thus, emotional communication between mother and infant is not uniquely human. Instead, we can trace back to macaques the evolutionary foundation of those behaviors that are crucial for the establishment of a functional capacity to socially exchange with others.

Video-induced yawning in stumptail macaques (Macaca arctoides)

This study reports the first experimental exploration of possible contagious yawning in monkeys. Twenty-two stumptail macaques (Macaca arctoides) were presented with video clips of either yawns or control mouth movements by conspecifics. At a group level, monkeys yawned significantly more often during and just after the yawn tape than the control tape. Supplementary analysis revealed that the yawn tape also elicited significantly more self-directed scratching responses than the control tape, which suggests that yawning might have been caused by tension arising from viewing the yawn tape. Understanding to what extent the observed effect resembles contagious yawning as found in humans and chimpanzees requires more detailed experimentation.

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 EEG from 1- to 7-day-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 nonbiological 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.

Interindividual Differences in Neonatal Imitation and the Development of Action Chains in Rhesus Macaques

The capacity to imitate facial gestures is highly variable in rhesus macaques and this variability may be related to differences in specific neurobehavioral patterns of development. This study evaluated the differential neonatal imitative response of 41 macaques in relation to the development of sensory, motor, and cognitive skills throughout the 1st month of life. The results show that infants who imitate facial gestures display more developed skills in goal-directed movements (reaching-grasping and fine hand motor control) than nonimitators. These differences might reflect, at least in part, the differential maturation of motor chains in the parietal and motor cortices, which partly overlap with those of the mirror neuron system. Thus, neonatal imitation appears to be a predictor of future neurobehavioral development.

Inhaled oxytocin increases positive social behaviors in newborn macaques

Significance Oxytocin promotes positive social behaviors in several species and therefore may be a therapeutic tool for neurodevelopmental disorders. It remains untested, however, whether oxytocin may affect infants, and whether effects may vary depending on infants’ social skills or interest. To test these predictions, we administered nebulized oxytocin to rhesus macaque newborns. Macaques, like humans, engage in complex face-to-face mother–infant interactions. Oxytocin increased infants’ affiliative communicative gestures and decreased salivary cortisol, and higher oxytocin levels were associated with greater social interest. Infants with stronger imitative skills were most positively influenced by oxytocin, suggesting that oxytocin sensitivity may underlie early social motivation. These results suggest that oxytocin may be a promising early intervention for infants at risk for abnormal social functions. 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.

Personality structure in brown capuchin monkeys (Sapajus apella): comparisons with chimpanzees (Pan troglodytes), orangutans (Pongo spp.), and rhesus macaques (Macaca mulatta).

Species comparisons of personality structure (i.e., how many personality dimensions and the characteristics of those dimensions) can facilitate questions about the adaptive function of personality in nonhuman primates. Here we investigate personality structure in the brown capuchin monkey (Sapajus apella), a New World primate species, and compare this structure to those of chimpanzees (Pan troglodytes), orangutans (Pongo spp.), and rhesus macaques (Macaca mulatta). Brown capuchins evolved behavioral and cognitive traits that are qualitatively similar to those of great apes, and individual differences in behavior and cognition often reflect differences in personality. Thus, we hypothesized that brown capuchin personality structure would overlap more with great apes than with rhesus macaques. We obtained personality ratings from seven sites, including 127 brown capuchin monkeys. Principal-components analysis identified five personality dimensions (Assertiveness, Openness, Neuroticism, Sociability, and Attentiveness), which were reliable across raters and, in a subset of subjects, significantly correlated with relevant behaviors up to a year later. Comparisons between species revealed that brown capuchins and great apes overlapped in personality structure, particularly chimpanzees in the case of Neuroticism. However, in some respects (i.e., capuchin Sociability and Openness) the similarities between capuchins and great apes were not significantly greater than those between capuchins and rhesus macaques. We discuss the relevance of our results to brown capuchin behavior and the evolution of personality structure in primates.

Stereotypic head twirls, but not pacing, are related to a ‘pessimistic’-like judgment bias among captive tufted capuchins (Cebus apella)

Abnormal stereotypic behaviour is widespread among captive non-human primates and is generally associated with jeopardized well-being. However, attributing the same significance to all of these repetitive, unvarying and apparently functionless behaviours may be misleading, as some behaviours may be better indicators of stress than others. Previous studies have demonstrated that the affective state of the individual can be inferred from its bias in appraising neutral stimuli in its environment. Therefore, in the present study, in order to assess the emotional state of stereotyping individuals, 16 captive tufted capuchins (Cebus apella) were tested on a judgment bias paradigm and their faecal corticoid levels were measured in order to assess the intensity of the emotional state. Capuchins with higher levels of stereotypic head twirls exhibited a negative bias while judging ambiguous stimuli and had higher levels of faecal corticoids compared to subjects with lower levels of head twirls. Levels of stereotypic pacing, however, were not correlated with the monkeys’ emotional state. This study is the first to reveal a positive correlation between levels of stereotypic behaviour and a ‘pessimistic’-like judgment bias in a non-human primate by employing a recently developed cognitive approach. Combining cognitive tests that evaluate the animals’ affective valence (positive or negative) with hormonal measurements that provide information on the strength of the emotional state conduces to a better understanding of the animals’ affective state and therefore to their well-being.

Some stereotypic behaviors in rhesus macaques (Macaca mulatta) are correlated with both perseveration and the ability to cope with acute stressors

The most prevalent sub-group of abnormal repetitive behaviors among captive animals is that of stereotypies. Previous studies have demonstrated some resemblance between stereotypy in captive animals and in humans, including the involvement of neurological malfunctions that lead to the expression of stereotypies. This malfunction can be evaluated through the use of neuropsychological tasks that assess perseveration as implying a failure of the basal ganglia (BG) to operate properly. Other studies, in contrast, have suggested that stereotypies are the product of neurologically intact individuals reacting to the abnormal nature of their surroundings, and are possibly characterized by an adaptive feature that enables the subject to cope with such adversity. Employing neuropsychological tests and also measuring the levels of fecal corticoids in captive rhesus macaques, we tested the hypothesis that stereotypies are related both to brain pathology and to a coping mechanism with stress, resembling accounts by autistic individuals exhibiting basal ganglia malfunction, and who report a sense of relief when performing stereotypies. Self-directed and fine-motor stereotypies exhibited by the monkeys were positively correlated with perseveration, suggesting BG malfunction; while self-directed stereotypies were also negatively correlated with an increase in fecal corticoids following a stress challenge, suggesting a related coping mechanism. We therefore suggest that not all repetitive, unvarying, and apparently functionless behaviors should be regarded as one homogeneous group of stereotypic behaviors; and that, reflecting reports from autistic individuals, self-directed stereotypies in captive rhesus monkeys are related both to brain pathology, and to an adaptive mechanism that allows those that express them to better cope with acute stressors.

Monkey lipsmacking develops like the human speech rhythm

Across all languages studied to date, audiovisual speech exhibits a consistent rhythmic structure. This rhythm is critical to speech perception. Some have suggested that the speech rhythm evolved de novo in humans. An alternative account--the one we explored here--is that the rhythm of speech evolved through the modification of rhythmic facial expressions. We tested this idea by investigating the structure and development of macaque monkey lipsmacks and found that their developmental trajectory is strikingly similar to the one that leads from human infant babbling to adult speech. Specifically, we show that: (1) younger monkeys produce slower, more variable mouth movements and as they get older, these movements become faster and less variable; and (2) this developmental pattern does not occur for another cyclical mouth movement--chewing. These patterns parallel human developmental patterns for speech and chewing. They suggest that, in both species, the two types of rhythmic mouth movements use different underlying neural circuits that develop in different ways. Ultimately, both lipsmacking and speech converge on a ~5 Hz rhythm that represents the frequency that characterizes the speech rhythm of human adults. We conclude that monkey lipsmacking and human speech share a homologous developmental mechanism, lending strong empirical support to the idea that the human speech rhythm evolved from the rhythmic facial expressions of our primate ancestors.