Lipsmacking Imitation Skill in Newborn Macaques Is Predictive of Social Partner Discrimination

Newborn rhesus macaques imitate facial gestures even after a delay, revealing the flexible nature of their early communicative exchanges. In the present study we examined whether newborn macaques are also sensitive to the identities of the social partners with whom they are interacting. We measured infant monkeys'' (n = 90) lipsmacking and tongue protrusion gestures in a face-to-face interaction task with a human experimenter in the first week of life. After a one-minute delay, the same person who previously presented gestures or a different person returned and presented a still face to infants. We had two primary predictions: (1) infants would demonstrate higher rates of overall gesturing, and especially lipsmacking—an affiliative gesture—to a familiar person, compared to a novel person, and (2) infants'' imitative skills would positively correlate with gestures to familiar, but not unfamiliar, social partners, as both abilities may reflect a strong general social interest. We found that overall infants did not produce more gestures or more lipsmacking when approached by a familiar person compared to a novel person; however, we did find individual differences in infants'' social responsiveness: lipsmacking imitation was positively correlated with lipsmacking during the return period when the person was the same (p = .025), but not when the person was novel (p = .44). These findings are consistent with the notion that imitative skill is reflective of infants'' more general interest in social interactions.     

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.     

Imitation and conventional communication

To the extent that language is conventional, non-verbal individuals, including human infants, must participate in conventions in order to learn to use even simple utterances of words. This raises the question of which varieties of learning could make this possible. In this paper I defend Tomasello’s (The cultural origins of human cognition. Harvard UP, Cambridge, 1999, Origins of human communication. MIT, Cambridge, 2008) claim that knowledge of linguistic conventions could be learned through imitation. This is possible because Lewisian accounts of convention have overstated what one must know to participate in conventions; and because the required knowledge could be learned imitatively. The imitation claim that I defend is consistent with what we know about both the proliferation of conventional behaviours in human children, who are skilful imitators, and the comparative absence of such behaviours in non-human great apes, who are poor at imitative learning.     

A “Bat” Is Easier to Learn than a “Tab”: Effects of Relative Phonotactic Frequency on Infant Word Learning

Many studies have shown that during the first year of life infants start learning the prosodic, phonetic and phonotactic properties of their native language. In parallel, infants start associating sound sequences with semantic representations. However, the question of how these two processes interact remains largely unknown. The current study explores whether (and when) the relative phonotactic probability of a sound sequence in the native language has an impact on infants’ word learning. We exploit the fact that Labial-Coronal (LC) words are more frequent than Coronal-Labial (CL) words in French, and that French-learning infants prefer LC over CL sequences at 10 months of age, to explore the possibility that LC structures might be learned more easily and thus at an earlier age than CL structures. Eye movements of French-learning 14- and 16-month-olds were recorded while they watched animated cartoons in a word learning task. The experiment involved four trials testing LC sequences and four trials testing CL sequences. Our data reveal that 16-month-olds were able to learn the LC and CL words, while14-month-olds were only able to learn the LC words, which are the words with the more frequent phonotactic pattern. The present results provide evidence that infants’ knowledge of their native language phonotactic patterns influences their word learning: Words with a frequent phonotactic structure could be acquired at an earlier age than those with a lower probability. Developmental changes are discussed and integrated with previous findings.     

Imitation of facial gestures by an infant chimpanzee

A nursery-reared infant chimpanzee (Pan troglodytes) was tested for the ability to imitate human facial gestures, following the procedure ofMeltzoff andMoore (1977). The subject was observed between 5 to 15 weeks of ages. The results showed that the subject could imitate tongue protrusion in the age of 5–10 weeks and mouth opening between the ages of 5–11 weeks. However, from 12 to 15 weeks, the infant did not imitate the facial gestures. The present study clearly demonstrated that the infant chimpanzee could imitate human facial gestures in a particular period.     

The predictive nature of individual differences in early associative learning and emerging social behavior

Across the first year of life, infants achieve remarkable success in their ability to interact in the social world. The hierarchical nature of circuit and skill development predicts that the emergence of social behaviors may depend upon an infant's early abilities to detect contingencies, particularly socially-relevant associations. Here, we examined whether individual differences in the rate of associative learning at one month of age is an enduring predictor of social, imitative, and discriminative behaviors measured across the human infant's first year. One-month learning rate was predictive of social behaviors at 5, 9, and 12 months of age as well as face-evoked discriminative neural activity at 9 months of age. Learning was not related to general cognitive abilities. These results underscore the importance of early contingency learning and suggest the presence of a basic mechanism underlying the ontogeny of social behaviors.     

Why Do Child-Directed Interactions Support Imitative Learning in Young Children?

Child-directed cues support imitation of novel actions at 18 months, but not at two years of age. The current studies explore the mechanisms that underlie the propensity that children have to copy others at 18 months, and how the value of child-directed communication changes over development. We ask if attentional allocation accounts for children''s failure to imitate observed actions at 18 months, and their success at two years of age, and we explore the informational value child-directed contexts may provide across ontogeny. Eighteen-month-old (Study 1) and two-year-old (Study 2) children viewed causally non-obvious actions performed by child-directed (Study 1 & 2), observed (Study 1 & 2), or non-interactive (Study 2) actors, and their visual attention and imitative behaviors were assessed. Results demonstrated that child-directed contexts supported imitative learning for 18-month-old children, independent of their effects on proximal attention. However, by two years of age, neither directness nor communication between social partners was a necessary condition for supporting social imitation. These findings suggest that developmental changes in children''s propensity to extract information from observation cannot be accounted for by changes in children''s interpretation of what counts as child-directed information, and are likely not due to changes in how children allocate attention to observed events.     

Scaffolding Imitation in Capoeira: Physical Education and Enculturation in an Afro-Brazilian Art

ABSTRACT  Imitation plays a crucial role in apprenticeship in the Afro-Brazilian performance genre capoeira, as in many skills across cultures. In this article, I examine the interactional dynamics of imitative pedagogy in capoeira to better understand physical education as a form of bodily enculturation. The ability to learn through imitation is widely considered a hallmark of our species. Imitative ability, however, is a social accomplishment rather than a capacity of the learner in isolation. Human models often provide assistance to novices seeking to imitate, including a variety of forms of what educational theorists call "scaffolding," which are astutely structured to a novice's ability, perceptions, and even neurology. Scaffolding techniques vary. I here examine how instructors reduce students' degrees of movement freedom, reorient their model in perceptual space, and parse complex sequences into component gestures. Close analysis of pedagogical interaction highlights the divergence between forms of instruction and practical skills being taught.     

The ethological analysis of imitation

Theorists and experimental researchers have long debated whether animals are able to imitate. A variety of definitions of imitation have been proposed to describe this complex form of social learning. Experimental research on imitation has often been hampered by either a too loose 'anthropomorphic' approach or by too narrow 'behaviourist' definitions. At present neither associative nor cognitive theories are able to offer an exhaustive explanation of imitation in animals. An ethological approach to imitation offers a different perspective. By integrating questions on function, mechanism, development and evolution one can identify possible directions for future research. At present, however, we are still far from developing a comprehensive theory of imitation. A functional approach to imitation shows that, despite some evidence for imitative learning in food processing in apes, such learning has not been shown to be involved in the social transmission of either tool-use skills or communicative signals. Recently developed procedures offer possible ways of clarifying the role of imitation in tool use and visual communication. The role of imitation in explorative play in apes is also investigated and the available data suggest that copying during play might represent a behavioural homologue of human imitation. It is proposed that the ability to copy the behaviour of a companion is under a strong genetic influence in many social species. Many important factors have not been examined experimentally, e.g. the effect of the demonstrator, the influence of attention and memory and the ability to generalize. The potential importance of reinforcement raises the possibility that copying abilities serving divergent functions might be partly under the control of different mechanisms.     

Homo imitans? Seven reasons why imitation couldn't possibly be associative

Many comparative and developmental psychologists believe that we are Homo imitans; humans are more skilled and prolific imitators than other animals, because we have a special, inborn ‘intermodal matching’ mechanism that integrates representations of others with representations of the self. In contrast, the associative sequence learning (ASL) model suggests that human infants learn to imitate using mechanisms that they share with other animals, and the rich resources provided by their sociocultural environments. This article answers seven objections to the ASL model: (i) it presents evidence that newborns do not imitate; (ii) argues that infants receive a plentiful supply of the kind of experience necessary for learning to imitate; (iii) suggests that neither infants nor adults can imitate elementally novel actions; (iv) explains why non-human animals have a limited capacity for imitation; (v) discusses the goal-directedness of imitation; (vi) presents evidence that improvement in imitation depends on visual feedback; and (vii) reflects on the view that associative theories steal ‘the soul of imitation’. The empirical success of the ASL model indicates that the mechanisms which make imitation possible, by aligning representations of self with representations of others, have been tweaked by cultural evolution, not built from scratch by genetic evolution.     

Neural systems for preparatory control of imitation

Humans have an automatic tendency to imitate others. Previous studies on how we control these tendencies have focused on reactive mechanisms, where inhibition of imitation is implemented after seeing an action. This work suggests that reactive control of imitation draws on at least partially specialized mechanisms. Here, we examine preparatory imitation control, where advance information allows control processes to be employed before an action is observed. Drawing on dual route models from the spatial compatibility literature, we compare control processes using biological and non-biological stimuli to determine whether preparatory imitation control recruits specialized neural systems that are similar to those observed in reactive imitation control. Results indicate that preparatory control involves anterior prefrontal, dorsolateral prefrontal, posterior parietal and early visual cortices regardless of whether automatic responses are evoked by biological (imitative) or non-biological stimuli. These results indicate both that preparatory control of imitation uses general mechanisms, and that preparatory control of imitation draws on different neural systems from reactive imitation control. Based on the regions involved, we hypothesize that preparatory control is implemented through top-down attentional biasing of visual processing.     

Brain responses in 4-month-old infants are already language specific

Language is the most important faculty that distinguishes humans from other animals. Infants learn their native language fast and effortlessly during the first years of life, as a function of the linguistic input in their environment. Behavioral studies reported the discrimination of melodic contours [1] and stress patterns [2, 3] in 1-4-month-olds. Behavioral [4, 5] and brain measures [6-8] have shown language-independent discrimination of phonetic contrasts at that age. Language-specific discrimination, however, has been reported for phonetic contrasts only for 6-12-month-olds [9-12]. Here we demonstrate language-specific discrimination of stress patterns in 4-month-old German and French infants by using electrophysiological brain measures. We compare the processing of disyllabic words differing in their rhythmic structure, mimicking German words being stressed on the first syllable, e.g., pápa/daddy[13], and French ones being stressed on the second syllable, e.g., papá/daddy. Event-related brain potentials reveal that experience with German and French differentially affects the brain responses of 4-month-old infants, with each language group displaying a processing advantage for the rhythmic structure typical in its native language. These data indicate language-specific neural representations of word forms in the infant brain as early as 4 months of age.     

Imitative behavior. A theoretical view

This article reviews the results of experimental studies on imitative behavior reported by various investigators, and then discusses the possible brain mechanisms responsible for this behavior. It was found that human infants in their first hours of life were already capable of spontaneous imitation of simple motor acts demonstrated by an adult, without previous training or reward; these observations suggest that imitative behavior is an innate process that can be considered an unconditional reflex of imitation. It was also found that satiated animals resumed eating when they saw their companions eating. In the latter case, the imitative reflex triggered the previously acquired feeding behavior. Similar mechanisms could be responsible for the phenomenon of eating more in the presence of companions than in their absence, as well as that of preferring the food chosen by companions. When followed by a reward, the imitative act can be learned--that is, transformed into an instrumental conditional response; learning by imitation of simple motor acts was observed in animals, and that of complex motor acts was observed in children who had already achieved a certain developmental stage. In animals, learning complex motor tasks was facilitated by previous observation of a companion performing this task. In this case, the presence of the observer during the session could lead to habituation of the experimental situation and production of associations between this situation and stimuli or emotions related to the reward or punishment, and might result in more efficient learning later. The imitative behavior can be inhibited by stimuli producing responses antagonistic to the act of imitation.     

What imitation tells us about social cognition: a rapprochement between developmental psychology and cognitive neuroscience

Both developmental and neurophysiological research suggest a common coding between perceived and generated actions. This shared representational network is innately wired in humans. We review psychological evidence concerning the imitative behaviour of newborn human infants. We suggest that the mechanisms involved in infant imitation provide the foundation for understanding that others are 'like me' and underlie the development of theory of mind and empathy for others. We also analyse functional neuroimaging studies that explore the neurophysiological substrate of imitation in adults. We marshal evidence that imitation recruits not only shared neural representations between the self and the other but also cortical regions in the parietal cortex that are crucial for distinguishing between the perspective of self and other. Imitation is doubly revealing: it is used by infants to learn about adults, and by scientists to understand the organization and functioning of the brain.     

Human Toddlers’ Attempts to Match Two Simple Behaviors Provide No Evidence for an Inherited,Dedicated Imitation Mechanism

Influential theories of imitation have proposed that humans inherit a neural mechanism – an “active intermodal matching “ (AIM) mechanism or a mirror neuron system - that functions from birth to automatically match sensory input from others’ actions to motor programs for performing those same actions, and thus produces imitation. To test these proposals, 160 1- to 2½-year-old toddlers were asked to imitate two simple movements– bending the arm to make an elbow, and moving the bent elbow laterally. Both behaviors were almost certain to be in each child’s repertoire, and the lateral movement was goal-directed (used to hit a plastic cup). Thus, one or both behaviors should have been imitable by toddlers with a functioning AIM or mirror neuron system. Each child saw the two behaviors repeated 18 times, and was encouraged to imitate. Children were also asked to locate their own elbows. Almost no children below age 2 imitated either behavior. Instead, younger children gave clear evidence of a developmental progression, from reproducing only the outcome of the models’ movements (hitting the object), through trying (but failing) to reproduce the model’s arm posture and/or the arm-cup relations they had seen, to accurate imitation of arm bending by age 2 and of both movements by age 2½. Across age levels, almost all children who knew the word ‘elbow’ imitated both behaviors: very few who did not know the word imitated either behavior. The evidence is most consistent with a view of early imitation as the product of a complex system of language, cognitive, social, and motor competencies that develop in infancy. The findings do not rule out a role for an inherited neural mechanism, but they suggest that such a system would not by itself be sufficient to explain imitation at any age.     

Selective imitation in domestic dogs

The transmission of cultural knowledge requires learners to identify what relevant information to retain and selectively imitate when observing others' skills. Young human infants--without relying on language or theory of mind--already show evidence of this ability. If, for example, in a communicative context, a model demonstrates a head action instead of a more efficient hand action, infants imitate the head action only if the demonstrator had no good reason to do so, suggesting that their imitation is a selective, interpretative process [1]. Early sensitivity to ostensive-communicative cues and to the efficiency of goal-directed actions is thought to be a crucial prerequisite for such relevance-guided selective imitation [2]. Although this competence is thought to be human specific [2], here we show an analog capacity in the dog. In our experiment, subjects watched a demonstrator dog pulling a rod with the paw instead of the preferred mouth action. In the first group, using the "inefficient" action was justified by the model's carrying of a ball in her mouth, whereas in the second group, no constraints could explain the demonstrator's choice. In the first trial after observation, dogs imitated the nonpreferred action only in the second group. Consequently, dogs, like children, demonstrated inferential selective imitation.     

Facial displays in young tufted Capuchin monkeys (Cebus apella): appearance, meaning, context and target

Facial displays are important for communication, and their ontogeny has been studied primarily in chimpanzees and macaques. We investigated the ontogeny, communicative function and target of facial displays in Cebus apella. Our results show that facial displays are absent at birth and develop as infants grow older. Lip-smacking appears first (at about 1 month of age), followed by scalp-lifting, relaxed open-mouth, silent bared-teeth, open-mouth silent bared-teeth displays and finally the open-mouth threat face. Infants perform most facial displays in the same contexts as adults, with the exception of the silent bared-teeth display that young capuchins use primarily, or exclusively, in affiliative contexts. Interestingly, facial displays are exchanged very often with peers, less frequently with adults and almost never with the mother.     

Brain lesions that impair vocal imitation in adult budgerigars

Vocal imitation is a complex form of imitative learning that is well developed only in humans, dolphins, and birds. Among birds, only some species are able to imitate sounds in adulthood. Of these, the budgerigar (Melopsittacus undulatus) has been studied in most detail. Previous studies suggested that the vocal motor system in budgerigars receives auditory information from the lateral frontal neostriatum (NFl). In the present study, we confirm this hypothesis by showing that infusions of the GABA agonist muscimol into NFl reduce the strength of auditory responses in a telencephalic vocal motor nucleus, the central nucleus of the lateral neostriatum (NLc). To test whether the auditory information conveyed from NFl to NLc plays a role in vocal imitation, we lesioned parts of NFl and the overlying ventral hyperstriatum (HVl) in seven adult male budgerigars and then examined whether the lesioned males would imitate the calls of females with whom they were paired. We found that, compared to sham-lesioned controls, the lesioned birds were significantly impaired in their imitation of female calls. Yet, the lesioned males were clearly not deaf (e.g., their previously learned calls did not degrade as they do after deafening). Therefore, the data suggest that NFl/HVl lesions impair vocal imitation by reducing the amount of auditory information that reaches the vocal motor system. Interestingly, the females that were paired with lesioned males displayed more vocal plasticity than the females in the control group, and some even imitated their male's prepairing calls.     

Imitation as behaviour parsing

Non-human great apes appear to be able to acquire elaborate skills partly by imitation, raising the possibility of the transfer of skill by imitation in animals that have only rudimentary mentalizing capacities: in contrast to the frequent assumption that imitation depends on prior understanding of others' intentions. Attempts to understand the apes' behaviour have led to the development of a purely mechanistic model of imitation, the 'behaviour parsing' model, in which the statistical regularities that are inevitable in planned behaviour are used to decipher the organization of another agent's behaviour, and thence to imitate parts of it. Behaviour can thereby be understood statistically in terms of its correlations (circumstances of use, effects on the environment) without understanding of intentions or the everyday physics of cause-and-effect. Thus, imitation of complex, novel behaviour may not require mentalizing, but conversely behaviour parsing may be a necessary preliminary to attributing intention and cause.