Secondary representational abilities in nonhuman primates (Macaca nemestrina, Cebus apella)

As human infants mature, their cognitive operations achieve increasing levels of complexity, which is thought to be based on an increasing complexity of their mental representational abilities. Perner (1991) proposed three different types of mental representations that are believed to underlie this development: primary representations, which represent reality accurately and faithfully; secondary representations, which are ‘detached’ from immediate reality and therefore capable of modelling past or future situations; and metarepresentations, which explicitly represent the relationship between the representation and its content. Numerous studies have provided evidence that in humans, primary representations appear to be present from birth, secondary representations emerge between 1.5-2 years, and metarepresentations develop between 4.5-5 years. Much less is known with regard to the phylogenetic development of representational abilities. Studies with nonhuman primates suggest the presence of primary and secondary representational abilities in great apes, but only primary representational abilities in monkeys. However, the current lack of evidence for secondary representational abilities in monkeys might be related to the limited number of studies addressing this issue and/or methodological limitations, thereby perhaps not reflecting a true negative. In order to contribute towards a more complete picture of nonhuman primates’ representational abilities, a series of studies was conducted to examine secondary representational abilities in two monkey species (Macaca nemestrina, Cebus apella). Pig-tailed macaques were tested for self-imitation, imitation recognition and mirror self-recognition; capuchin monkeys were tested for imitation recognition, mirror self-recognition and means-ends reasoning, all thought to be indicative of secondary representational abilities. Evidence for primary representations was found in both species, however none of the experiments provided strong evidence for secondary representational abilities. One possible exception is two pig-tailed macaques’ responses to marks on their heads during a classic mark test for self-recognition, but since these responses consisted of mere swipes to their heads and not intensive mirror-mediated responding, this finding cannot be regarded as conclusive. The absence of evidence for secondary representational abilities in monkeys in the present work therefore confirms previous research findings and may suggest that monkeys are limited to primary representational abilities. Replications and extensions of the present work are highly recommended and can significantly contribute to our understanding of the evolutionary origin of human and nonhuman primate cognition

Cued repetition of self-directed behaviors in macaques (Macaca nemestrina)

Two macaques were trained to perform three self-directed behaviors on signal, and to repeat behaviors after a ‘repeat’ signal. The cognitive processes underlying the monkeys’ repeat performance were evaluated using multiple repetitions of the repeat signal, extended delay periods between target behavior and repeat signal, and by transferring the repeat signal to novel behaviors. The monkeys appear to have used representations of their own past behaviors as a basis for repetition performance, but they mostly failed to correctly repeat target behaviors after extended delays and during transfer tasks. Implications for episodic memory abilities are discussed

Facial width-to-height ratio relates to alpha status and assertive personality in capuchin monkeys

Social dominance hierarchies play a pivotal role in shaping the behaviour of many species, and sex differences within these hierarchies often exist. To date, however, few physical markers of dominance have been identified. Such markers would be valuable in terms of understanding the etiology of dominant behaviour and changes in social hierarchies over time. Animals may also use such traits to evaluate the potential dominance of others relative to themselves (i.e. a physical “cue”). Facial width-to-height ratio (fWHR), for example, has been suggested as a cue to dominance in humans, with links to both dominant behaviour and the perception of dominance in other individuals. Whether this association is present in non-human animals is currently not known. Therefore, here we examine within-species links between fWHR and dominant behaviour in 64 brown capuchin monkeys (Sapajus spp.) aged between 2 and 40 years. fWHR was positively associated with alpha status and with a dimensional rating of assertive personality in both males and females. Moreover, fWHR showed significant sexual dimorphism in adults but not juveniles, suggesting a developmental change may occur during puberty. In a sub-sample, sex differences were mediated by weight, suggesting fWHR dimorphism does not exceed what would be expected by differences in body weight. This is the first report of an association between face shape and behaviour in a non-human species. Results are discussed in terms of the role that face-behaviour associations might play within capuchin societies, and the possible selective forces that might have led to the evolution of fWHR-dominance associations in humans

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

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

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

The mirror neuron system as revealed through neonatal imitation: presence from birth, predictive power, and evidence of plasticity

There is strong evidence that neonates imitate previously unseen behaviors. These behaviors are predominantly used in social interactions, demonstrating neonates’ ability and motivation to engage with others. Research on neonatal imitation can provide a wealth of information about the early mirror neuron system (MNS): namely, its functional characteristics, its plasticity from birth, and its relation to skills later in development. Though numerous studies document the existence of neonatal imitation in the laboratory, little is known about its natural occurrence during parent-infant interactions and its plasticity as a consequence of experience. We review these critical aspects of imitation, which we argue are necessary for understanding the early action-perception system. We address common criticisms and misunderstandings about neonatal imitation and discuss methodological differences among studies. Recent work reveals that individual differences in neonatal imitation positively correlate with later social, cognitive, and motor development. We propose that such variation in neonatal imitation could reflect important individual differences of the MNS. Although postnatal experience is not necessary for imitation, we present evidence that neonatal imitation is influenced by experience in the first week of life

Neonatal Imitation in Rhesus Macaques

The emergence of social behaviors early in life is likely crucial for the development of mother–infant relationships. Some of these behaviors, such as the capacity of neonates to imitate adult facial movements, were previously thought to be limited to humans and perhaps the ape lineage. Here we report the behavioral responses of infant rhesus macaques (Macaca mulatta) to the following human facial and hand gestures: lip smacking, tongue protrusion, mouth opening, hand opening, and opening and closing of eyes (control condition). In the third day of life, infant macaques imitate lip smacking and tongue protrusion. On the first day of life, the model's mouth openings elicited a similar matched behavior (lip smacking) in the infants. These imitative responses are present at an early stage of development, but they are apparently confined to a narrow temporal window. Because lip smacking is a core gesture in face-to-face interactions in macaques, neonatal imitation may serve to tune infants' affiliative responses to the social world. Our findings provide a quantitative description of neonatal imitation in a nonhuman primate species and suggest that these imitative capacities, contrary to what was previously thought, are not unique to the ape and human lineage. We suggest that their evolutionary origins may be traced to affiliative gestures with communicative functions

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 using complex forms of emotional exchanges including exaggerated lipsmacking, sustained mutual gaze, mouth-mouth contacts, and neonatal imitation. Infant macaques solicit their mother’s affiliative responses and actively communicate to her. However, this form of communication disappears within the infant’s 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

Delayed Imitation of Lipsmacking Gestures by Infant Rhesus Macaques (Macaca mulatta)

Human infants are capable of accurately matching facial gestures of an experimenter within a few hours after birth, a phenomenon called neonatal imitation. Recent studies have suggested that rather than being a simple reflexive-like behavior, infants exert active control over imitative responses and ‘provoke’ previously imitated gestures even after a delay of up to 24 h. Delayed imitation is regarded as the hallmark of a sophisticated capacity to control and flexibly engage in affective communication and has been described as an indicator of innate protoconversational readiness. However, we are not the only primates to exhibit neonatal imitation, and delayed imitation abilities may not be uniquely human. Here we report that 1-week-old infant rhesus macaques (Macaca mulatta) who show immediate imitation of a lipsmacking gesture also show delayed imitation of lipsmacking, facilitated by a tendency to refrain from lipsmacking toward a still face during baseline measurements. Individual differences in delayed imitation suggest that differentially matured cortical mechanisms may be involved, allowing some newborns macaques to actively participate in communicative exchanges from birth. Macaque infants are endowed with basic social competencies of intersubjective communication that indicate cognitive and emotional commonality between humans and macaques, which may have evolved to nurture an affective mother-infant relationship in primates