Fronto-parietal mirror neuron system modeling: Visuospatial transformations support imitation learning independently of imitator perspective

Although the human mirror neuron system (MNS) is critical for action observation and imitation, most MNS investigations overlook the visuospatial transformation processes that allow individuals to interpret and imitate actions observed from differing perspectives. This problem is not trivial since accurately reaching for and grasping an object requires a visuospatial transformation mechanism capable of precisely remapping fine motor skills where the observer’s and imitator’s arms and hands may have quite different orientations and sizes. Accordingly, here we describe a novel neural model to investigate the dynamics between the fronto-parietal MNS and visuospatial processes during observation and imitation of a reaching and grasping action. Our model encompasses i) the inferior frontal gyrus (IFG) and inferior parietal lobule (IPL), regions that are postulated to produce neural drive and sensory predictions, respectively; ii) the middle temporal (MT) and middle superior temporal (MST) regions that are postulated to process visual motion of a particular action; and iii) the superior parietal lobule (SPL) and intra-parietal sulcus (IPS) that are hypothesized to encode the visuospatial transformations enabling action observation/imitation based on different visuospatial viewpoints. The results reveal that when a demonstrator executes an action, an imitator can reproduce it with similar kinematics, independently of differences in anthropometry, distance, and viewpoint. As with prior empirical findings, similar model synaptic activity was observed during both action observation and execution along with the existence of both view-independent and view-dependent neural populations in the frontal MNS. Importantly, this work generates testable behavioral and neurophysiological predictions. Namely, the model predicts that i) during observation/imitation the response time increases linearly as the rotation angle of the observed action increases but remain similar when performing both clockwise and counterclockwise rotation and ii) IPL embeds essentially view-independent neurons while SPL/IPS includes both view-independent and view-dependent neurons. Overall, this work suggests that MT/MST visuomotion processes combined with the SPL/IPS allow the MNS to observe and imitate actions independently of demonstrator-imitator spatial relationships.     

Recognizing the role of perception in action at 6 months

The present research examined whether infants as young as 6 months of age would consider what objects a human agent could perceive when interpreting her actions on the objects. In two experiments, the infants took the agent's actions of repeatedly reaching for and grasping one of two possible objects as suggesting her preference for that object only when the agent could detect both objects, not when the agent's perceptual access to the second object was absent, either because a large screen hid the object from the agent ( Experiment 1 ), or because the agent sat with her back toward the object ( Experiment 2 ). These results suggest that young infants recognize the role of perception in constraining an agent's goal‐actions.     

Does how I look at what you're doing depend on what I'm doing?

Previous studies showed that people proactively gaze at the target of another's action by taking advantage of their own motor representation of that action. But just how selectively is one's own motor representation implicated in another's action processing? If people observe another's action while performing a compatible or an incompatible action themselves, will this impact on their gaze behaviour? We recorded proactive eye movements while participants observed an actor grasping small or large objects. The participants' right hand either freely rested on the table or held with a suitable grip a large or a small object, respectively. Proactivity of gaze behaviour significantly decreased when participants observed the actor reaching her target with a grip that was incompatible with respect to that used by them to hold the object in their own hand. This indicates that effective observation of action may depend on what one is actually doing, being actions observed best when the suitable motor representations may be readily recruited.     

Let’s get it together: Infants generate visual predictions based on collaborative goals

Infants engage in social interactions that include multiple partners from very early in development. A growing body of research shows that infants visually predict the outcomes of an individual’s intentional actions, such as a person reaching towards an object (e.g., Krogh-Jespersen & Woodward, 2014), and even show sophistication in their predictions regarding failed actions (e.g., Brandone, Horwitz, Aslin, & Wellman, 2014). Less is known about infants’ understanding of actions involving more than one individual (e.g., collaborative actions), which require representing each partners’ actions in light of the shared goal. Using eye-tracking, Study 1 examined whether 14-month-old infants visually predict the actions of an individual based on her previously shared goal. Infants viewed videos of two women engaged in either a collaborative or noncollaborative interaction. At test, only one woman was present and infants’ visual predictions regarding her future actions were measured. Fourteen-month-olds anticipated an individual’s future actions based on her past collaborative behavior. Study 2 revealed that 11-month-old infants only visually predict higher-order shared goals after engaging in a collaborative intervention. Together, our results indicate that by the second year after birth, infants perceive others’ collaborative actions as structured by shared goals and that active engagement in collaboration strengthens this understanding in young infants.     

The reliability of a model influences 14-month-olds’ imitation

Human infants have an enormous amount to learn from others to become full-fledged members of their culture. Thus, it is important that they learn from reliable, rather than unreliable, models. In two experiments, we investigated whether 14-month-olds (a) imitate instrumental actions and (b) adopt the individual preferences of a model differently depending on the model’s previous reliability. Infants were shown a series of videos in which a model acted on familiar objects either competently or incompetently. They then watched as the same model demonstrated a novel action on an object (imitation task) and preferentially chose one of two novel objects (preference task). Infants’ imitation of the novel action was influenced by the model’s previous reliability; they copied the action more often when the model had been reliable. However, their preference for one of the novel objects was not influenced by the model’s previous reliability. We conclude that already by 14 months of age, infants discriminate between reliable and unreliable models when learning novel actions.     

Goal saliency boosts infants’ action prediction for human manual actions,but not for mechanical claws

Previous research indicates that infants’ prediction of the goals of observed actions is influenced by own experience with the type of agent performing the action (i.e., human hand vs. non-human agent) as well as by action-relevant features of goal objects (e.g., object size). The present study investigated the combined effects of these factors on 12-month-olds’ action prediction. Infants’ (N = 49) goal-directed gaze shifts were recorded as they observed 14 trials in which either a human hand or a mechanical claw reached for a small goal area (low-saliency goal) or a large goal area (high-saliency goal). Only infants who had observed the human hand reaching for a high-saliency goal fixated the goal object ahead of time, and they rapidly learned to predict the action goal across trials. By contrast, infants in all other conditions did not track the observed action in a predictive manner, and their gaze shifts to the action goal did not change systematically across trials. Thus, high-saliency goals seem to boost infants’ predictive gaze shifts during the observation of human manual actions, but not of actions performed by a mechanical device. This supports the assumption that infants’ action predictions are based on interactive effects of action-relevant object features (e.g., size) and own action experience.     

Visually guided grasping of common objects: Effects of priming

Priming effects were tested on the planning of the grasping of common objects under full vision during action performance. Healthy participants took part in four experiments which manipulated the nature of the prime (objects, circular block, rectangular bar) and priming context (blocked vs. mixed). Each experiment relied on four priming conditions: (1) congruent orientation, (2) incongruent orientation, (3) neutral prime, and (4) no prime. Priming was observed to have a facilitating effect on visually guided grasping when the object to be grasped was primed by a congruently oriented identical object. This effect was rather independent of the priming context (experimental set-up). Our data suggest an object's functional identity may contribute to the priming effect, as well as its intrinsic (e.g., shape, size) and extrinsic (orientation) visual characteristics. We showed that the planning of visually guided grasping is influenced by prior visual experience, and thus that grasping is not based exclusively on real-time processing of visual information.     

Infants’ perception of goal-directed actions: A multi-lab replication reveals that infants anticipate paths and not goals

Influential developmental theories claim that infants rely on goals when visually anticipating actions. A widely noticed study suggested that 11-month-olds anticipate that a hand continues to grasp the same object even when it swapped position with another object (Cannon, E., & Woodward, A. L. (2012). Infants generate goal-based action predictions. Developmental Science, 15, 292–298.). Yet, other studies found such flexible goal-directed anticipations only from later ages on. Given the theoretical relevance of this phenomenon and given these contradicting findings, the current work investigated in two different studies and labs, whether infants indeed flexibly anticipate an action goal. Study 1 (N = 144) investigated by means of five experiments, under which circumstances (e.g., animated agent, human agent) 12-month-olds show flexible goal anticipation abilities. Study 2 (N = 104) presented 11-, 32-month-olds and adults both a human grasping action as well as a non-human action. In none of the experiments did infants flexibly anticipate the action based on the goal, but rather on the movement path, irrespective of the type of agent. Although one experiment contained a direct replication of Cannon and Woodward (2012), we were not able to replicate their findings. Overall our work challenges the view that infants are able to flexibly anticipate action goals from early on, but rather rely on movement patterns when processing other’s actions.     

Precision and power grip priming by observed grasping

The coupling of hand grasping stimuli and the subsequent grasp execution was explored in normal participants. Participants were asked to respond with their right- or left-hand to the accuracy of an observed (dynamic) grasp while they were holding precision or power grasp response devices in their hands (e.g., precision device/right-hand; power device/left-hand). The observed hand was making either accurate or inaccurate precision or power grasps and participants signalled the accuracy of the observed grip by making one or other response depending on instructions. Responses were made faster when they matched the observed grip type. The two grasp types differed in their sensitivity to the end-state (i.e., accuracy) of the observed grip. The end-state influenced the power grasp congruency effect more than the precision grasp effect when the observed hand was performing the grasp without any goal object (Experiments 1 and 2). However, the end-state also influenced the precision grip congruency effect (Experiment 3) when the action was object-directed. The data are interpreted as behavioural evidence of the automatic imitation coding of the observed actions. The study suggests that, in goal-oriented imitation coding, the context of an action (e.g., being object-directed) is more important factor in coding precision grips than power grips.     

Self produced and observed actions influence emotion: the roles of action fluency and eye gaze

Affective responses to objects can be influenced by cognitive processes such as perceptual fluency. Here we investigated whether the quality of motor interaction with an object influences affective response to the object. Participants grasped and moved objects using either a fluent action or a non-fluent action (avoiding an obstacle). Liking ratings were higher for objects in the fluent condition. Two further studies investigated whether the fluency of another person’s actions influences affective response. Observers watched movie clips of the motor actions described above, in conditions where the observed actor could be seen to be looking towards the grasped object, or where the actor’s head and gaze were not visible. Two results were observed: First, when the actor’s gaze cannot be seen, liking ratings of the objects are reduced. Second, action fluency of observed actions does influence liking ratings, but only when the actor’s gaze towards the object is visible. These findings provide supporting evidence for the important role of observed eye gaze in action simulation, and demonstrate that non-emotive actions can evoke empathic states in observers. This research was supported by Economic and Social Research Council grant RES-000-23-0429 awarded to S. P. Tipper and A. E. Hayes.     

I don't get you. Action observation effects inverted by kinematic variation

Recent studies have reported an intricate interplay between affordance and mirror effects (the imitation of another agent) when participants attend to the concurrent presentation of an object and another agent interacting with it. In the present paper, we compare two experimental settings in which an observed action was presented as a prime for a task involving the categorization of a graspable object. In experiment 1a, the action depicted a reach and grasp gesture whereas in experiment 1b, only the reach phase was presented. This modification led to very different outcomes. Experiment 1a reflected the traditional imitation effect elicited by human motion. Conversely, experiment 1b showed the facilitation of contralateral responses. Affordance effects were found in experiment 1a only for the RVF. Our results support the view that motor simulation processes underlying imitation or joint actions are extremely sensitive to specific phase kinematics.     

Relations between infants’ emerging reach‐grasp competence and event‐related desynchronization in EEG

Recent reports of similar patterns of brain electrical activity (electroencephalogram: EEG) during action execution and observation, recorded from scalp locations over motor‐related regions in infants and adults, have raised the possibility that two foundational abilities – controlling one's own intentional actions and perceiving others’ actions – may be integrally related during ontogeny. However, to our knowledge, there are no published reports of the relations between developments in motor skill (i.e. recording actual motor skill performance) and EEG during both action execution and action observation. In the present study we collected EEG from 21 9‐month‐olds who were given opportunities to reach for toys and who also observed an experimenter reach for toys. Event‐related desynchronization (ERD) was computed from the EEG during the reaching events. We assessed infants’ reaching‐grasping competence, including reach latency, errors, preshaping of the hand, and bimanual reaches, and found that desynchronization recorded in scalp electrodes over motor‐related regions during action observation was associated with action competence during execution. Infants who were more competent reachers, compared to less competent reachers, exhibited greater ERD while observing reaching‐grasping. These results provide initial evidence for an early emerging neural system integrating one's own actions with the perception of others’ actions.     

Children's Representation and Imitation of Events: How Goal Organization Influences 3‐Year‐Old Children's Memory for Action Sequences

Children's imitation of adults plays a prominent role in human cognitive development. However, few studies have investigated how children represent the complex structure of observed actions which underlies their imitation. We integrate theories of action segmentation, memory, and imitation to investigate whether children's event representation is organized according to veridical serial order or a higher level goal structure. Children were randomly assigned to learn novel event sequences either through interactive hands‐on experience (Study 1) or via storybook (Study 2). Results demonstrate that children's representation of observed actions is organized according to higher level goals, even at the cost of representing the veridical temporal ordering of the sequence. We argue that prioritizing goal structure enhances event memory, and that this mental organization is a key mechanism of social‐cognitive development in real‐world, dynamic environments. It supports cultural learning and imitation in ecologically valid settings when social agents are multitasking and not demonstrating one isolated goal at a time.     

Fourteen‐Month‐Olds' Imitation of Differently Aged Models

Studies comparing adult and peer imitation are rare and have to date provided mixed results. The aim of the present study was to investigate 14‐month‐olds' imitation of different actions (novel versus familiar) performed by televised models of different age groups (peers, older children or adults). In two experiments, we investigated infants' imitative performance when observing a novel action (Experiment 1) and familiar actions (Experiment 2). The results showed that the likelihood of imitating a novel action increased as the age of the model increased. The opposite was true for familiar actions where infants imitated the peer more frequently than either the older child or the adult model. These findings are discussed in relation to infants' ability to take into account a model's characteristics such as age when imitating actions. Copyright © 2011 John Wiley & Sons, Ltd.     

Toddlers’ social evaluations of agents who act on false beliefs

Mature social evaluations privilege agents’ intentions over the outcomes of their actions, but young children often privilege outcomes over intentions in verbal tasks probing their social evaluations. In three experiments (N = 118), we probed the development of intention-based social evaluation and mental state reasoning using nonverbal methods with 15-month-old toddlers. Toddlers viewed scenarios depicting a protagonist who sought to obtain one of two toys, each inside a different box, as two other agents observed. Then, the boxes’ contents were switched in the absence of the protagonist and either in the presence or the absence of the other agents. When the protagonist returned, one agent opened the box containing the protagonist's desired toy (a positive outcome), and the other opened the other box (a neutral outcome). When both agents had observed the toys move to their current locations, the toddlers preferred the agent who opened the box containing the desired toy. In contrast, when the agents had not seen the toys move and therefore should have expected the desired toy's location to be unchanged, the toddlers preferred the agent who opened the box that no longer contained the desired toy. Thus, the toddlers preferred the agent who intended to make the protagonist's desired toy accessible, even when its action, guided by a false belief concerning that toy's location, did not produce a positive outcome. Well before children connect beliefs to social behavior in verbal tasks, toddlers engage in intention-based evaluations of social agents with false beliefs.     

“Should I or shouldn’t I?” Imitation of undesired versus allowed actions from peer and adult models by 18- and 24-month-old toddlers

Imitation is a common way of acquiring novel behaviors in toddlers. However, little is known about toddlers’ imitation of undesired actions. Here we investigated 18- and 24-month-olds’ (N = 110) imitation of undesired and allowed actions from televised peer and adult models. Permissiveness of the demonstrated actions was indicated by the experimenter’s response to their execution (angry or neutral). Analyses revealed that toddlers’ imitation scores were higher after demonstrations of allowed versus undesired actions, regardless of the age of the model. In agreement with prior research, these results suggest that third-party reactions to a model’s actions can be a powerful cue for toddlers to engage in or refrain from imitation. In the context of the present study, third-party reactions were more influential on imitation than the model’s age. Considering the relative influence of different social cues for imitation can help to gain a fuller understanding of early observational learning.     

Development of the Correspondence Between Real and Imagined Fine and Gross Motor Actions

The development of the correspondence between real and imagined motor actions was investigated in 2 experiments. Experiment 1 evaluated whether children imagine body position judgments of fine motor actions in the same way as they perform them. Thirty-two 8-year-old children completed a task in which an object was presented in different orientations, and children were asked to indicate the position of their hand as they grasped and imagined grasping the object. Children’s hand position was almost identical for the imagined- and real-grasping trials. Experiment 2 replicated this result with 8-year-olds as well as 6-year-olds and also assessed the development of the correspondence of the chronometry of real and imagined gross motor actions. Sixteen 6-year-old children and seventeen 8-year-old children participated in the fine motor grasping task from Experiment 1 and a gross motor task that measured the time it took for children to walk and imagine walking different distances. Six-year-olds showed more of a difference between real and imagined walking than did 8-year-olds. However, there were strong correlations between real and imagined grasping and walking for both 6- and 8-year-old children, suggesting that by at least 6 years of age, motor imagery and real action may involve common internal representations and that motor imagery is important for motor control and planning.     

The early development of human mirror mechanisms: evidence from electromyographic recordings at 3 and 6 months

In primates and adult humans direct understanding of others' action is provided by mirror mechanisms matching action observation and action execution (e.g. Casile, Caggiano & Ferrari, 2011). Despite the growing body of evidence detailing the existence of these mechanisms in the adult human brain, their origins and early development are largely unknown. In this study, for the first time, electromyographic (EMG) measures were used to shed light on the emergence of mirror motor mechanisms in infancy. EMG activity was recorded while 6‐ and 3‐month‐old infants watched two videos displaying an agent reaching for, grasping and bringing an object either to the mouth or to the head. Results indicate that the motor system of 6‐month‐olds, but not 3‐month‐olds, was recruited and selectively modulated during observation of the goal‐directed actions, favoring the idea that mirror mechanisms driving action understanding gradually emerge during early development.     

Observation of another's action but not eye gaze triggers allocentric visual perspective

In the present paper, we investigated whether observation of bodily cues—that is, hand action and eye gaze—can modulate the onlooker's visual perspective taking. Participants were presented with scenes of an actor gazing at an object (or straight ahead) and grasping an object (or not) in a 2?×?2 factorial design and a control condition with no actor in the scene. In Experiment 1, two groups of subjects were explicitly required to judge the left/right location of the target from their own (egocentric group) or the actor's (allocentric group) point of view, whereas in Experiment 2 participants did not receive any instruction on the point of view to assume. In both experiments, allocentric coding (i.e., the actor's point of view) was triggered when the actor grasped the target, but not when he gazed towards it, or when he adopted a neutral posture. In Experiment 3, we demonstrate that the actor's gaze but not action affected participants' attention orienting. The different effects of others' grasping and eye gaze on observers' behaviour demonstrated that specific bodily cues convey distinctive information about other people's intentions.     

A kinematic examination of dual-route processing for action imitation

The dual-route model of imitation suggests that meaningful and meaningless actions are processed through either an indirect or a direct route, respectively. Evidence indicates that the direct route is more cognitively demanding since it relies on mapping visuospatial properties of the observed action on to a performed one. These cognitive demands might negatively influence reaction time and accuracy for actions performed following a meaningless action under time constraints. However, how meaningful and meaningless action imitation processing is reflected in movement kinematics is not yet clear. We wanted to confirm whether meaningless action performance incurs a reaction time cost, whether the cost is reflected in kinematics, and, more generally, to examine kinematic markers of emblematic meaningful and meaningless action imitation. We examined participants’ reaction time and wrist movements when they imitated emblematic meaningful or matched meaningless gestures in either blocks of the same action type or mixed blocks. Meaningless actions were associated with a greater correction period at the end of the movement, possibly reflecting a strategy designed to ensure accurate completion for less familiar actions under time constraints. Furthermore, in mixed blocks, trials following meaningless actions had a significantly increased reaction time, supporting previous claims that route selection for action imitation may be stimulus-driven. However, there was only convincing evidence for this effect with an interval of ~2,948ms, but not ~3,573ms or ~2,553ms, between movements. Future work motion-tracking the entire hand to assess imitation accuracy, and more closely examining the influence of duration between movements, may help to explain these effects.