Social cognition: imitation, imitation, imitation

Monkeys recognize when they are being imitated, but they seem unable to learn by imitation. These facts make sense if imitation is seen as two different capacities: social mirroring, when actions are matched and have social benefits; and learning by copying, when new behavioural routines are acquired by observation.     

Action generation and action perception in imitation: an instance of the ideomotor principle

We review a series of behavioural experiments on imitation in children and adults that test the predictions of a new theory of imitation. Most of the recent theories of imitation assume a direct visual-to-motor mapping between perceived and imitated movements. Based on our findings of systematic errors in imitation, the new theory of goal-directed imitation (GOADI) instead assumes that imitation is guided by cognitively specified goals. According to GOADI, the imitator does not imitate the observed movement as a whole, but rather decomposes it into its separate aspects. These aspects are hierarchically ordered, and the highest aspect becomes the imitator's main goal. Other aspects become sub-goals. In accordance with the ideomotor principle, the main goal activates the motor programme that is most strongly associated with the achievement of that goal. When executed, this motor programme sometimes matches, and sometimes does not, the model's movement. However, the main goal extracted from the model movement is almost always imitated correctly.     

<Emphasis Type="Italic">Cebus apella</Emphasis> Tolerate Intermittent Unreliability in Human Experimenters

Monkeys form expectations for outcomes based on interactions with human experimenters. Capuchins, a cooperative New World monkey species, not only anticipate receiving rewards that the experimenter indicates, but also apparently anticipate rewards based on what the experimenter has given to their partners. However, this could be due to subjects responding to either outcomes or experimenters. Here we examine whether capuchins will continue to interact with human experimenters who are occasionally unreliable. We tested 10 monkeys with a series of familiar human experimenters using an exchange task. The experimenters had never before participated in exchange studies with these monkeys, hence the monkeys learned about their behavior during the course of testing. Occasionally experimenters were unreliable, failing to give a reward after the monkey returned the token. The monkeys did recognize these interactions as different, responding much more quickly in trials following those that were nonrewarded than in other situations with the same experimenter. However, subjects did not change their preference for experimenters when given the opportunity to choose between the unreliable exchanger and another exchanger, nor did subjects learn to prefer reliable experimenters from watching other monkeys’ interactions. Instead, subjects returned the tokens to the same location from which they received it. These results indicate that capuchins may not be sensitive to isolated instances in which experimenters are unreliable, possibly because of a strong bias to returning the token to the location from which it was donated.     

Automatic Imitation in Rhythmical Actions: Kinematic Fidelity and the Effects of Compatibility,Delay, and Visual Monitoring

We demonstrate that observation of everyday rhythmical actions biases subsequent motor execution of the same and of different actions, using a paradigm where the observed actions were irrelevant for action execution. The cycle time of the distractor actions was subtly manipulated across trials, and the cycle time of motor responses served as the main dependent measure. Although distractor frequencies reliably biased response cycle times, this imitation bias was only a small fraction of the modulations in distractor speed, as well as of the modulations produced when participants intentionally imitated the observed rhythms. Importantly, this bias was not only present for compatible actions, but was also found, though numerically reduced, when distractor and executed actions were different (e.g., tooth brushing vs. window wiping), or when the dominant plane of movement was different (horizontal vs. vertical). In addition, these effects were equally pronounced for execution at 0, 4, and 8 s after action observation, a finding that contrasts with the more short-lived effects reported in earlier studies. The imitation bias was also unaffected when vision of the hand was occluded during execution, indicating that this effect most likely resulted from visuomotor interactions during distractor observation, rather than from visual monitoring and guidance during execution. Finally, when the distractor was incompatible in both dimensions (action type and plane) the imitation bias was not reduced further, in an additive way, relative to the single-incompatible conditions. This points to a mechanism whereby the observed action’s impact on motor processing is generally reduced whenever this is not useful for motor planning. We interpret these findings in the framework of biased competition, where intended and distractor actions can be represented as competing and quasi-encapsulated sensorimotor streams.     

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.     

Discrimination of macaques by macaques: the case of Sulawesi species

A series of work by the first author have demonstrated that many macaque species show a visual preference for the pictures of their own species when the monkeys actively press a lever to see the pictures. We expanded this study to Sulawesi macaques kept as a pet by local people with slight modification. All seven species of Sulawesi macaques were passively exposed to a variety of colored slides of Sulawesi macaques. The experimenter recorded the duration of visual fixation onto the pictures. Male monkeys of all the seven species clearly watched the pictures of their own species for longer duration than those of the other species. Such visual preference suggested that the seven Sulawesi macaques discriminate each other species and, thus, they may not be integrated into fewer number of species. This visual preference may work to prevent overall intergradation of the Sulawesi macaques who sometimes have hybrid zones only in limited areas. This preference was in general weaker in female monkeys. In one species,Macaca ochreata, females actively avoided to see the pictures of conspecifics. These results may be related to how female monkeys interact with other individuals.     

Effect of others' attentional states on vocalizations in Japanese monkeys (Macaca fuscata)

We investigated the effects of other's attentional states on vocalizations in monkeys. The subjects were 14 Japanese monkeys (Macaca fuscata), which vocalized spontaneously in the feeding context. In the initial experiment, an experimenter moved towards and away from the subject monkeys. The monkeys vocalized more frequently when the experimenter moved away rather than towards them. To examine the effects of the experimenter's body orientations and moving directions separately, additional experiments were conducted. When the experimenter stood facing towards and facing away from the subject monkeys, the monkeys vocalized more frequently when the experimenter stood facing away rather than facing towards. When the experimenter moved towards and away from the subject monkeys while facing them, the monkeys vocalized more frequently when the experimenter moved away from them rather than towards them. These results suggested that the monkeys vocalized more frequently when the situation changed to that where the monkeys were not likely get food from the experimenter. It seems that monkeys recognize the attentional states of others by body orientation and modify their vocalizing behavior accordingly.     

Posterior parietal cortex neurons encode target motion in world-centered coordinates

The motion areas of posterior parietal cortex extract information on visual motion for perception as well as for the guidance of movement. It is usually assumed that neurons in posterior parietal cortex represent visual motion relative to the retina. Current models describing action guided by moving objects work successfully based on this assumption. However, here we show that the pursuit-related responses of a distinct group of neurons in area MST of monkeys are at odds with this view. Rather than signaling object image motion on the retina, they represent object motion in world-centered coordinates. This representation may simplify the coordination of object-directed action and ego motion-invariant visual perception.     

Seeing Touches Early in Life

The sense of touch provides fundamental information about the surrounding world, and feedback about our own actions. Although touch is very important during the earliest stages of life, to date no study has investigated infants’ abilities to process visual stimuli implying touch. This study explores the developmental origins of the ability to visually recognize touching gestures involving others. Looking times and orienting responses were measured in a visual preference task, in which participants were simultaneously presented with two videos depicting a touching and a no-touching gesture involving human body parts (face, hand) and/or an object (spoon). In Experiment 1, 2-day-old newborns and 3-month-old infants viewed two videos: in one video a moving hand touched a static face, in the other the moving hand stopped before touching it. Results showed that only 3-month-olds, but not newborns, differentiated the touching from the no-touching gesture, displaying a preference for the former over the latter. To test whether newborns could manifest a preferential visual response when the touched body part is different from the face, in Experiment 2 newborns were presented with touching/no-touching gestures in which a hand or an inanimate object—i.e., a spoon- moved towards a static hand. Newborns were able to discriminate a hand-to-hand touching gesture, but they did not manifest any preference for the object-to-hand touch. The present findings speak in favour of an early ability to visually recognize touching gestures involving the interaction between human body parts.     

When and how well can human‐socialized capuchins match actions demonstrated by a familiar human?

Capuchin monkeys have provided uneven evidence of matching actions they observe others perform. In accord with theories emphasizing the attentional salience of object movement and spatial relationships, we predicted that human-reared monkeys would better match events in which a human demonstrator moved an object into a new relation with another object or surface than other kinds of actions. Three human-reared capuchins were invited repeatedly by a familiar human to perform a fixed set of actions upon objects or upon their bodies, using the "Do as I do" procedure. Actions directed at the body were matched less reliably than actions involving objects, and actions were matched best when the monkey looked at the demonstration for at least 2 sec and performed its action within a few seconds after the demonstration. The most commonly matched actions were those that one monkey performed relatively often when the experiment began. One monkey partially reproduced three novel actions (out of 48 demonstrations), all three involving moving or placing objects, and two of which it also performed following other demonstrations. These findings contribute convergent evidence that capuchin monkeys display social facilitation of activity, enhanced interest in particular objects and emulation of spatial outcomes. This pattern can support the development of shared manipulative skills, as evident in traditions of foraging and tool use in natural settings. The findings do not suggest that human rearing substantively altered capuchins' ability or interest in matching the actions of a familiar human, although visual attention to the human demonstrator may have been greater in these monkeys than in normally reared monkeys.     

The human premotor cortex is 'mirror' only for biological actions

Previous work has shown that both human adults and children attend to grasping actions performed by another person but not necessarily to those made by a mechanical device. According to recent neurophysiological data, the monkey premotor cortex contains "mirror" neurons that discharge both when the monkey performs specific manual grasping actions and when it observes another individual performing the same or similar actions. However, when a human model uses tools to perform grasping actions, the mirror neurons are not activated. A similar "mirror" system has been described in humans, but whether or not it is also tuned specifically to biological actions has never been tested. Here we show that when subjects observed manual grasping actions performed by a human model a significant neural response was elicited in the left premotor cortex. This activation was not evident for the observation of grasping actions performed by a robot model commanded by an experimenter. This result indicates for the first time that in humans the mirror system is biologically tuned. This system appears to be the neural substrate for biological preference during action coding.     

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.     

Inter-Brain Synchronization during Social Interaction

During social interaction, both participants are continuously active, each modifying their own actions in response to the continuously changing actions of the partner. This continuous mutual adaptation results in interactional synchrony to which both members contribute. Freely exchanging the role of imitator and model is a well-framed example of interactional synchrony resulting from a mutual behavioral negotiation. How the participants'' brain activity underlies this process is currently a question that hyperscanning recordings allow us to explore. In particular, it remains largely unknown to what extent oscillatory synchronization could emerge between two brains during social interaction. To explore this issue, 18 participants paired as 9 dyads were recorded with dual-video and dual-EEG setups while they were engaged in spontaneous imitation of hand movements. We measured interactional synchrony and the turn-taking between model and imitator. We discovered by the use of nonlinear techniques that states of interactional synchrony correlate with the emergence of an interbrain synchronizing network in the alpha-mu band between the right centroparietal regions. These regions have been suggested to play a pivotal role in social interaction. Here, they acted symmetrically as key functional hubs in the interindividual brainweb. Additionally, neural synchronization became asymmetrical in the higher frequency bands possibly reflecting a top-down modulation of the roles of model and imitator in the ongoing interaction.     

Helping behaviour and regard for others in capuchin monkeys (Cebus apella)

Altruism is an evolutionary puzzle. To date, much debate has focused on whether helping others without regard to oneself is a uniquely human behaviour, with a variety of empirical studies demonstrating a lack of altruistic behaviour in chimpanzees even when the demands of behaving altruistically seem minimal. By contrast, a recent experiment has demonstrated that chimpanzees will help a human experimenter to obtain an out-of-reach object, irrespective of whether or not they are offered a reward for doing so, suggesting that the cognitions underlying altruistic behaviour may be highly sensitive to situational demands. Here, we examine the cognitive demands of other-regarding behaviour by testing the conditions under which primates more distantly related to humans--capuchin monkeys--help an experimenter to obtain an out-of-reach object. Like chimpanzees, capuchin monkeys helped human experimenters even in the absence of a reward, but capuchins systematically failed to take into account the perspective of others when they stood to obtain food for themselves. These results suggest an important role for perspective taking and inhibition in altruistic behaviour and seem to reflect a significant evolutionary development in the roots of altruism, and specifically in other-regarding behaviour, between the divergence of New World monkeys and apes.     

Context-dependent model-based biases in cultural transmission: children's imitation is affected by model age over model knowledge state

Many animals, including humans, acquire information through social learning. Although such information can be acquired easily, its potential unreliability means it should not be used indiscriminately. Cultural ‘transmission biases’ may allow individuals to weigh their reliance on social information according to a model's characteristics. In one of the first studies to juxtapose two model-based biases, we investigated whether the age and knowledge state of a model affected the fidelity of children's copying. Eighty-five 5-year-old children watched a video demonstration of either an adult or child, who had professed either knowledge or ignorance regarding a tool-use task, extracting a reward from that task using both causally relevant and irrelevant actions. Relevant actions were imitated faithfully by children regardless of the model's characteristics, but children who observed an adult reproduced more irrelevant actions than those who observed a child. The professed knowledge state of the model showed a weaker effect on imitation of irrelevant actions. Overall, children favored the use of a ‘copy adults’ bias over a ‘copy task-knowledgeable individual’ bias, even though the latter could potentially have provided more reliable information. The use of such social learning strategies has significant implications for understanding the phenomenon of imitation of irrelevant actions (overimitation), instances of maladaptive information cascades, and cumulative culture.     

Reflections of other minds: how primate social cognition can inform the function of mirror neurons

Mirror neurons, located in the premotor cortex of macaque monkeys, are activated both by the performance and the passive observation of particular goal-directed actions. Although this property would seem to make them the ideal neural substrate for imitation, the puzzling fact is that monkeys simply do not imitate. Indeed, imitation appears to be a uniquely human ability. We are thus left with a fascinating question: if not imitation, what are mirror neurons for? Recent advances in the study of non-human primate social cognition suggest a surprising potential answer.     

Capuchin monkeys (<Emphasis Type="Italic">Cebus apella</Emphasis>) modify their own behaviors according to a conspecific’s emotional expressions

Understanding conspecifics’ emotional states is important for managing social interactions. We examined whether capuchin monkeys modify their own behaviors in response to a conspecific’s emotional expressions. Six monkeys saw a demonstrator monkey responding emotionally to an object in a container; the subject monkeys could not see the object. The subjects reached for the container more frequently when the demonstrator showed an emotionally positive expression than when she showed an emotionally neutral or negative expression. This is the first report that New World monkeys are sensitive to the emotional valence of conspecifics’ emotional expressions. The finding is consistent with the hypothesis that monkeys can recognize emotional meanings in others’ expressions, an ability previously attributed only to humans and great apes.     

To Beg,or Not to Beg? That Is the Question: Mangabeys Modify Their Production of Requesting Gestures in Response to Human’s Attentional States

Background

Although gestural communication is widespread in primates, few studies focused on the cognitive processes underlying gestures produced by monkeys.

Methodology/Principal Findings

The present study asked whether red-capped mangabeys (Cercocebus torquatus) trained to produce visually based requesting gestures modify their gestural behavior in response to human’s attentional states. The experimenter held a food item and displayed five different attentional states that differed on the basis of body, head and gaze orientation; mangabeys had to request food by extending an arm toward the food item (begging gesture). Mangabeys were sensitive, at least to some extent, to the human’s attentional state. They reacted to some postural cues of a human recipient: they gestured more and faster when both the body and the head of the experimenter were oriented toward them than when they were oriented away. However, they did not seem to use gaze cues to recognize an attentive human: monkeys begged at similar levels regardless of the experimenter’s eyes state.

Conclusions/Significance

These results indicate that mangabeys lowered their production of begging gestures when these could not be perceived by the human who had to respond to it. This finding provides important evidence that acquired begging gestures of monkeys might be used intentionally.     

Pointing Behavior in Infants Reflects the Communication Partner’s Attentional and Knowledge States: A Possible Case of Spontaneous Informing

Inferring the epistemic states of others is considered to be an essential requirement for humans to communicate; however, the developmental trajectory of this ability is unclear. The aim of the current study was to determine developmental trends in this ability by using pointing behavior as a dependent measure. Infants aged 13 to 18 months (n = 32, 16 females) participated in the study. The experiment consisted of two phases. In the Shared Experience Phase, both the participant and the experimenter experienced (played with) an object, and the participant experienced a second object while the experimenter was absent. In the Pointing Phase, the participant was seated on his/her mother’s lap, facing the experimenter, and the same two objects from the Shared Experience Phase were presented side-by-side behind the experimenter. The participants’ spontaneous pointing was analyzed from video footage. While the analysis of the Shared Experience Phase suggested that there was no significant difference in the duration of the participants’ visual attention to the two objects, the participants pointed more frequently to the object that could be considered “new” for the experimenter (in Experiment 1). This selective pointing was not observed when the experimenter could be considered unfamiliar with both of the objects (in Experiment 2). These findings suggest that infants in this age group spontaneously point, presumably to inform about an object, reflecting the partner’s attentional and knowledge states.     

Fragment-based learning of visual object categories in non-human primates

When we perceive a visual object, we implicitly or explicitly associate it with an object category we know. Recent research has shown that the visual system can use local, informative image fragments of a given object, rather than the whole object, to classify it into a familiar category. We have previously reported, using human psychophysical studies, that when subjects learn new object categories using whole objects, they incidentally learn informative fragments, even when not required to do so. However, the neuronal mechanisms by which we acquire and use informative fragments, as well as category knowledge itself, have remained unclear. Here we describe the methods by which we adapted the relevant human psychophysical methods to awake, behaving monkeys and replicated key previous psychophysical results. This establishes awake, behaving monkeys as a useful system for future neurophysiological studies not only of informative fragments in particular, but also of object categorization and category learning in general.