Sensorimotor experience enhances automatic imitation of robotic action

Recent research in cognitive neuroscience has found that observation of human actions activates the 'mirror system' and provokes automatic imitation to a greater extent than observation of non-biological movements. The present study investigated whether this human bias depends primarily on phylogenetic or ontogenetic factors by examining the effects of sensorimotor experience on automatic imitation of non-biological robotic, stimuli. Automatic imitation of human and robotic action stimuli was assessed before and after training. During these test sessions, participants were required to execute a pre-specified response (e.g. to open their hand) while observing a human or robotic hand making a compatible (opening) or incompatible (closing) movement. During training, participants executed opening and closing hand actions while observing compatible (group CT) or incompatible movements (group IT) of a robotic hand. Compatible, but not incompatible, training increased automatic imitation of robotic stimuli (speed of responding on compatible trials, compared with incompatible trials) and abolished the human bias observed at pre-test. These findings suggest that the development of the mirror system depends on sensorimotor experience, and that, in our species, it is biased in favour of human action stimuli because these are more abundant than non-biological action stimuli in typical developmental environments.     

Automatic imitation in dogs

After preliminary training to open a sliding door using their head and their paw, dogs were given a discrimination task in which they were rewarded with food for opening the door using the same method (head or paw) as demonstrated by their owner (compatible group), or for opening the door using the alternative method (incompatible group). The incompatible group, which had to counterimitate to receive food reward, required more trials to reach a fixed criterion of discrimination performance (85% correct) than the compatible group. This suggests that, like humans, dogs are subject to ‘automatic imitation’; they cannot inhibit online the tendency to imitate head use and/or paw use. In a subsequent transfer test, where all dogs were required to imitate their owners'' head and paw use for food reward, the incompatible group made a greater proportion of incorrect, counterimitative responses than the compatible group. These results are consistent with the associative sequence learning model, which suggests that the development of imitation depends on sensorimotor experience and phylogenetically general mechanisms of associative learning. More specifically, they suggest that the imitative behaviour of dogs is shaped more by their developmental interactions with humans than by their evolutionary history of domestication.     

Influence of Action-Effect Associations Acquired by Ideomotor Learning on Imitation

According to the ideomotor theory, actions are represented in terms of their perceptual effects, offering a solution for the correspondence problem of imitation (how to translate the observed action into a corresponding motor output). This effect-based coding of action is assumed to be acquired through action-effect learning. Accordingly, performing an action leads to the integration of the perceptual codes of the action effects with the motor commands that brought them about. While ideomotor theory is invoked to account for imitation, the influence of action-effect learning on imitative behavior remains unexplored. In two experiments, imitative performance was measured in a reaction time task following a phase of action-effect acquisition. During action-effect acquisition, participants freely executed a finger movement (index or little finger lifting), and then observed a similar (compatible learning) or a different (incompatible learning) movement. In Experiment 1, finger movements of left and right hands were presented as action-effects during acquisition. In Experiment 2, only right-hand finger movements were presented during action-effect acquisition and in the imitation task the observed hands were oriented orthogonally to participants’ hands in order to avoid spatial congruency effects. Experiments 1 and 2 showed that imitative performance was improved after compatible learning, compared to incompatible learning. In Experiment 2, although action-effect learning involved perception of finger movements of right hand only, imitative capabilities of right- and left-hand finger movements were equally affected. These results indicate that an observed movement stimulus processed as the effect of an action can later prime execution of that action, confirming the ideomotor approach to imitation. We further discuss these findings in relation to previous studies of action-effect learning and in the framework of current ideomotor approaches to imitation.     

How frontoparietal brain regions mediate imitative and complementary actions: an FMRI study

The 'mirror neuron system' (MNS), located within inferior parietal lobe (IPL) and inferior frontal gyrus (IFG), creates an internal motor representation of the actions we see and has been implicated in imitation. Recently, the MNS has been implicated in non-identical responses: when the actions we must execute do not match those that we observe. However, in such conflicting situations non action-specific cognitive control networks also located in frontoparietal regions may be involved. In the present functional magnetic resonance imaging (fMRI) study participants made both similar and dissimilar actions within two action contexts: imitative and complementary. We aimed to determine whether activity within IPL/IFG depends on (i) responding under an imitative versus complementary context (ii) responding with similar versus dissimilar responses, and (iii) observing hand actions versus symbolic arrow cue stimuli. Activity within rIPL/rIFG regions was largest during observation of hand actions compared with arrow cues. Specifically, rIPL/rIFG were recruited only during the imitative context, when participants responded with similar actions. When responding to symbolic arrow cues, rIPL/rIFG activity increased during dissimilar responses, reflecting increased demands placed on general cognitive control mechanisms. These results suggest a specific role of rIPL/rIFG during imitation of hand actions, and also a general role of frontoparietal areas in mediating dissimilar responses to both hand actions and symbolic stimuli. We discuss our findings in relation to recent work that has examined the role of frontoparietal brain structures in joint-actions and inter-actor cooperation. We conclude that the specific brain regions identified here to show increased activation during action observation conditions are likely to form part of a mechanism specifically involved in matching observed actions directly with internal motor plans. Conversely, observation of arrow cues recruited part of a wider cognitive control network involved in the rapid remapping of stimulus-response associations.     

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.     

Motor representation of actions in children with autism

Background

Children with Autistic Spectrum Disorders (ASD) are frequently hampered by motor impairment, with difficulties ranging from imitation of actions to recognition of motor intentions. Such a widespread inefficiency of the motor system is likely to interfere on the ontogeny of both motor planning and understanding of the goals of actions, thus delivering its ultimate effects on the emergence of social cognition.

Methodology/Principal Findings

We investigate the organization of action representation in 15 high functioning ASD (mean age: 8.11) and in two control samples of typically developing (TD) children: the first one, from a primary school, was matched for chronological age (CA), the second one, from a kindergarten, comprised children of much younger age (CY). We used nine newly designed behavioural motor tasks, aiming at exploring three domains of motor cognition: 1) imitation of actions, 2) production of pantomimes, and 3) comprehension of pantomimes. The findings reveal that ASD children fare significantly worse than the two control samples in each of the inspected components of the motor representation of actions, be it the imitation of gestures, the self-planning of pantomimes, or the (verbal) comprehension of observed pantomimes. In the latter task, owing to its cognitive complexity, ASD children come close to the younger TD children’s level of performance; yet they fare significantly worse with respect to their age-mate controls. Overall, ASD children reveal a profound damage to the mechanisms that control both production and pre-cognitive “comprehension” of the motor representation of actions.

Conclusions/Significance

Our findings suggest that many of the social cognitive impairments manifested by ASD individuals are likely rooted in their incapacity to assemble and directly grasp the intrinsic goal-related organization of motor behaviour. Such impairment of motor cognition might be partly due to an early damage of the Mirror Neuron Mechanism (MNM).     

Is there evidence for automatic imitation in a strategic context?

Over the past decade, a compelling number of studies reported that observing an action makes the imitation of that action more likely. The automatic character of human imitative behaviour was often claimed, but rarely tested. The demonstration of the absence of conscious control has been attempted in a recent report claiming that imitation can occur in the rock-paper-scissors (RPS) game, where strategic players should avoid imitating their opponents. This surprising result could serve as strong evidence that humans imitate each other unconsciously. We find, however, that this conclusion is problematic. In addition to reviewing the original methods, in this work, we also replicated the experiment with double the sample size. Thorough examination of the original analyses and the results of the present replication do not support the original conclusion. In our view, testing the theory of automatic imitation in RPS games is a potentially promising avenue of exploration, yet the interpretation of the data requires further understanding of the subsidiary effects controlling the behaviour of the players.     

Automatic imitation in budgerigars

A fully automated procedure, involving computer-controlled stimulus presentation and computer-recorded response measurement, was used for the first time to study imitation in non-human animals. After preliminary training to peck and step on a manipulandum, budgerigars were given a discrimination task in which they were rewarded with food for pecking during observation of pecking and for stepping during observation of stepping (Compatible group), or for pecking while observing stepping and for stepping while observing pecking (Incompatible group). The Incompatible group, which had to counter-imitate for food reward, showed weaker discrimination performance than the Compatible group. This suggests that, like humans, budgerigars are subject to 'automatic imitation'; they cannot inhibit online the tendency to imitate pecking and/or stepping, even when imitation of these behaviours interferes with the performance of an ongoing task. The difference between the two groups persisted over 10 test sessions, but the Incompatible group eventually acquired the discrimination, making more counter-imitative than imitative responses in the final sessions. These results are consistent with the associative sequence learning model, which suggests that, across species, the development of imitation and the mirror system depends on sensorimotor experience and phylogenetically ancient mechanisms of associative learning.     

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.     

Automatic versus voluntary motor imitation: effect of visual context and stimulus velocity

Automatic imitation is the tendency to reproduce observed actions involuntarily. Though this topic has been widely treated, at present little is known about the automatic imitation of the kinematic features of an observed movement. The present study was designed to understand if the kinematics of a previously seen stimulus primes the executed action, and if this effect is sensitive to the kinds of stimuli presented. We proposed a simple imitation paradigm in which a dot or a human demonstrator moved in front of the participant who was instructed either to reach the final position of the stimulus or to imitate its motion with his or her right arm. Participants' movements were automatically contaminated by stimulus velocity when it moved according to biological laws, suggesting that automatic imitation was kinematic dependent. Despite that the performance, in term of reproduced velocity, improved in a context of voluntary imitation, subjects did not replicate the observed motions exactly. These effects were not affected by the kind of stimuli used, i.e., motor responses were influenced in the same manner after dot or human observation. These findings support the existence of low-level sensory-motor matching mechanisms that work on movement planning and represent the basis for higher levels of social interaction.     

Young children with autism spectrum disorder use predictive eye movements in action observation

Does a dysfunction in the mirror neuron system (MNS) underlie the social symptoms defining autism spectrum disorder (ASD)? Research suggests that the MNS matches observed actions to motor plans for similar actions, and that these motor plans include directions for predictive eye movements when observing goal-directed actions. Thus, one important question is whether children with ASD use predictive eye movements in action observation. Young children with ASD as well as typically developing children and adults were shown videos in which an actor performed object-directed actions (human agent condition). Children with ASD were also shown control videos showing objects moving by themselves (self-propelled condition). Gaze was measured using a corneal reflection technique. Children with ASD and typically developing individuals used strikingly similar goal-directed eye movements when observing others’ actions in the human agent condition. Gaze was reactive in the self-propelled condition, suggesting that prediction is linked to seeing a hand–object interaction. This study does not support the view that ASD is characterized by a global dysfunction in the MNS.     

A Bayesian Developmental Approach to Robotic Goal-Based Imitation Learning

A fundamental challenge in robotics today is building robots that can learn new skills by observing humans and imitating human actions. We propose a new Bayesian approach to robotic learning by imitation inspired by the developmental hypothesis that children use self-experience to bootstrap the process of intention recognition and goal-based imitation. Our approach allows an autonomous agent to: (i) learn probabilistic models of actions through self-discovery and experience, (ii) utilize these learned models for inferring the goals of human actions, and (iii) perform goal-based imitation for robotic learning and human-robot collaboration. Such an approach allows a robot to leverage its increasing repertoire of learned behaviors to interpret increasingly complex human actions and use the inferred goals for imitation, even when the robot has very different actuators from humans. We demonstrate our approach using two different scenarios: (i) a simulated robot that learns human-like gaze following behavior, and (ii) a robot that learns to imitate human actions in a tabletop organization task. In both cases, the agent learns a probabilistic model of its own actions, and uses this model for goal inference and goal-based imitation. We also show that the robotic agent can use its probabilistic model to seek human assistance when it recognizes that its inferred actions are too uncertain, risky, or impossible to perform, thereby opening the door to human-robot collaboration.     

Motor Imagery in Asperger Syndrome: Testing Action Simulation by the Hand Laterality Task

Asperger syndrome (AS) is a neurodevelopmental condition within the Autism Spectrum Disorders (ASD) characterized by specific difficulties in social interaction, communication and behavioural control. In recent years, it has been suggested that ASD is related to a dysfunction of action simulation processes, but studies employing imitation or action observation tasks provided mixed results. Here, we addressed action simulation processes in adolescents with AS by means of a motor imagery task, the classical hand laterality task (to decide whether a rotated hand image is left or right); mental rotation of letters was also evaluated. As a specific marker of action simulation in hand rotation, we assessed the so-called biomechanical effect, that is the advantage for judging hand pictures showing physically comfortable versus physically awkward positions. We found the biomechanical effect in typically-developing participants but not in participants with AS. Overall performance on both hand laterality and letter rotation tasks, instead, did not differ in the two groups. These findings demonstrated a specific alteration of motor imagery skills in AS. We suggest that impaired mental simulation and imitation of goal-less movements in ASD could be related to shared cognitive mechanisms.     

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.     

A Bayesian Model of the Uncanny Valley Effect for Explaining the Effects of Therapeutic Robots in Autism Spectrum Disorder

One of the core features of autism spectrum disorder (ASD) is impaired reciprocal social interaction, especially in processing emotional information. Social robots are used to encourage children with ASD to take the initiative and to interact with the robotic tools to stimulate emotional responses. However, the existing evidence is limited by poor trial designs. The purpose of this study was to provide computational evidence in support of robot-assisted therapy for children with ASD. We thus propose an emotional model of ASD that adapts a Bayesian model of the uncanny valley effect, which holds that a human-looking robot can provoke repulsion and sensations of eeriness. Based on the unique emotional responses of children with ASD to the robots, we postulate that ASD induces a unique emotional response curve, more like a cliff than a valley. Thus, we performed numerical simulations of robot-assisted therapy to evaluate its effects. The results showed that, although a stimulus fell into the uncanny valley in the typical condition, it was effective at avoiding the uncanny cliff in the ASD condition. Consequently, individuals with ASD may find it more comfortable, and may modify their emotional response, if the robots look like deformed humans, even if they appear “creepy” to typical individuals. Therefore, we suggest that our model explains the effects of robot-assisted therapy in children with ASD and that human-looking robots may have potential advantages for improving social interactions in ASD.     

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.     

Human primary motor cortex is both activated and stabilized during observation of other person's phasic motor actions

When your favourite athlete flops over the high-jump bar, you may twist your body in front of the TV screen. Such automatic motor facilitation, ‘mirroring’ or even overt imitation is not always appropriate. Here, we show, by monitoring motor-cortex brain rhythms with magnetoencephalography (MEG) in healthy adults, that viewing intermittent hand actions of another person, in addition to activation, phasically stabilizes the viewer''s primary motor cortex, with the maximum of half a second after the onset of the seen movement. Such a stabilization was evident as enhanced cortex–muscle coherence at 16–20 Hz, despite signs of almost simultaneous suppression of rolandic rhythms of approximately 7 and 15 Hz as a sign of activation of the sensorimotor cortex. These findings suggest that inhibition suppresses motor output during viewing another person''s actions, thereby withholding unintentional imitation.     

Macaques (Macaca nemestrina) recognize when they are being imitated

This study investigated whether monkeys recognize when a human experimenter imitates their actions towards an object. Two experimenters faced 10 pigtailed macaques, who were given access to an interesting object. One experimenter imitated the monkeys' object-directed actions, the other performed temporally contingent but structurally different object-directed actions. Results show a significant visual preference for the imitator during manual object manipulations, but not mouthing actions. We argue that the ability to match actions could be based on both visual-visual and kinaesthetic-visual matching skills, and that mirror neurons, which have both visual and motor properties, could serve as a neural basis for recognizing imitation. However, imitation recognition as assessed by visual preference does not necessarily imply the capacity to attribute imitative intentionality to the imitator. The monkeys might implicitly recognize when they are being imitated without deeper insight into the mental processes of others.