Moving just like you: motor interference depends on similar motility of agent and observer

Recent findings in neuroscience suggest an overlap between brain regions involved in the execution of movement and perception of another's movement. This so-called "action-perception coupling" is supposed to serve our ability to automatically infer the goals and intentions of others by internal simulation of their actions. A consequence of this coupling is motor interference (MI), the effect of movement observation on the trajectory of one's own movement. Previous studies emphasized that various features of the observed agent determine the degree of MI, but could not clarify how human-like an agent has to be for its movements to elicit MI and, more importantly, what 'human-like' means in the context of MI. Thus, we investigated in several experiments how different aspects of appearance and motility of the observed agent influence motor interference (MI). Participants performed arm movements in horizontal and vertical directions while observing videos of a human, a humanoid robot, or an industrial robot arm with either artificial (industrial) or human-like joint configurations. Our results show that, given a human-like joint configuration, MI was elicited by observing arm movements of both humanoid and industrial robots. However, if the joint configuration of the robot did not resemble that of the human arm, MI could longer be demonstrated. Our findings present evidence for the importance of human-like joint configuration rather than other human-like features for perception-action coupling when observing inanimate agents.     

Complementary systems for understanding action intentions

How humans understand the intention of others' actions remains controversial. Some authors have suggested that intentions are recognized by means of a motor simulation of the observed action with the mirror-neuron system [1-3]. Others emphasize that intention recognition is an inferential process, often called "mentalizing" or employing a "theory of mind," which activates areas well outside the motor system [4-6]. Here, we assessed the contribution of brain regions involved in motor simulation and mentalizing for understanding action intentions via functional brain imaging. Results show that the inferior frontal gyrus (part of the mirror-neuron system) processes the intentionality of an observed action on the basis of the visual properties of the action, irrespective of whether the subject paid attention to the intention or not. Conversely, brain areas that are part of a "mentalizing" network become active when subjects reflect about the intentionality of an observed action, but they are largely insensitive to the visual properties of the observed action. This supports the hypothesis that motor simulation and mentalizing have distinct but complementary functions for the recognition of others' intentions.     

An interference effect of observed biological movement on action

It has been proposed that actions are intrinsically linked to perception and that imagining, observing, preparing, or in any way representing an action excites the motor programs used to execute that same action. There is neurophysiological evidence that certain brain regions involved in executing actions are activated by the mere observation of action (the so-called "mirror system;" ). However, it is unknown whether this mirror system causes interference between observed and simultaneously executed movements. In this study we test the hypothesis that, because of the overlap between action observation and execution, observed actions should interfere with incongruous executed actions. Subjects made arm movements while observing either a robot or another human making the same or qualitatively different arm movements. Variance in the executed movement was measured as an index of interference to the movement. The results demonstrate that observing another human making incongruent movements has a significant interference effect on executed movements. However, we found no evidence that this interference effect occurred when subjects observed a robotic arm making incongruent movements. These results suggest that the simultaneous activation of the overlapping neural networks that process movement observation and execution infers a measurable cost to motor control.     

The evolution of social cognition: goal familiarity shapes monkeys' action understanding

What is the evolutionary origin of the human ability to understand and predict the behavior of others? Recent studies suggest that human infants' early capacity for understanding others' goal-directed actions relies on nonmentalistic strategies [1-8]. However, there is no consensus about the nature of the mechanisms underpinning these strategies and their evolutionary history. Comparative studies can shed light on these controversial issues. We carried out three preferential looking-time experiments on macaques, modeled on previous work on human infants [1-5], to test whether macaques are sensitive to the functional efficacy of familiar goal-related hand motor acts performed by an experimenter in a given context and to examine to which extent this sensitivity also is present when observing non-goal-related or unusual goal-related motor acts. We demonstrate that macaque monkeys, similar to human infants, do indeed detect action efficacy by gazing longer at less efficient actions. However, they do so only when the observed behavior is directed to a perceptible and familiar goal. Our results show that the direct detection of the functional fitness of action, in relation to goals that have become familiar through previous experience, is the phylogenetic precursor of intentional understanding.     

Seeing or Doing? Influence of Visual and Motor Familiarity in Action Observation

The human brain contains specialized circuits for observing and understanding actions. Previous studies have not distinguished whether this "mirror system" uses specialized motor representations or general processes of visual inference and knowledge to understand observed actions. We report the first neuroimaging study to distinguish between these alternatives. Purely motoric influences on perception have been shown behaviorally, but their neural bases are unknown. We used fMRI to reveal the neural bases of motor influences on action observation. We controlled for visual and knowledge effects by studying expert dancers. Some ballet moves are performed by only one gender. However, male and female dancers train together and have equal visual familiarity with all moves. Male and female dancers viewed videos of gender-specific male and female ballet moves. We found greater premotor, parietal, and cerebellar activity when dancers viewed moves from their own motor repertoire, compared to opposite-gender moves that they frequently saw but did not perform. Our results show that mirror circuits have a purely motor response over and above visual representations of action. We understand actions not only by visual recognition, but also motorically. In addition, we confirm that the cerebellum is part of the action observation network.     

Motor simulation and the bodily self

Previous studies demonstrated the human ability to implicitly recognize their own body. When submitted to a visual matching task, participants showed the so-called self-advantage, that is, a better performance with self rather than others' body or body parts. Here, we investigated whether the body self-advantage relies upon a motor representation of one's body. Participants were submitted to a laterality judgment of self and others' hands (Experiment 1 and 3), which involves a sensory-motor mental simulation. Moreover, to investigate whether the self-advantage emerges also when an explicit self processing is required, the same participants were submitted to an explicit self-body recognition task (Experiment 2). Participants showed the self-advantage when performing the laterality judgment, but not when self-recognition was explicitly required. Thus, implicit and explicit recognition of the bodily self dissociate and only an implicit recognition of the bodily self, mapped in motor terms, allows the self-advantage to emerge.     

Human motor cortex excitability during the perception of others' action

Neuroscience research during the past ten years has fundamentally changed the traditional view of the motor system. In monkeys, the finding that premotor neurons also discharge during visual stimulation (visuomotor neurons) raises new hypotheses about the putative role played by motor representations in perceptual functions. Among visuomotor neurons, mirror neurons might be involved in understanding the actions of others and might, therefore, be crucial in interindividual communication. Functional brain imaging studies enabled us to localize the human mirror system, but the demonstration that the motor cortex dynamically replicates the observed actions, as if they were executed by the observer, can only be given by fast and focal measurements of cortical activity. Transcranial magnetic stimulation enables us to instantaneously estimate corticospinal excitability, and has been used to study the human mirror system at work during the perception of actions performed by other individuals. In the past ten years several TMS experiments have been performed investigating the involvement of motor system during others' action observation. Results suggest that when we observe another individual acting we strongly 'resonate' with his or her action. In other words, our motor system simulates underthreshold the observed action in a strictly congruent fashion. The involved muscles are the same as those used in the observed action and their activation is temporally strictly coupled with the dynamics of the observed action.     

Are you approaching me? Motor execution influences perceived action orientation

Human observers are especially sensitive to the actions of conspecifics that match their own actions. This has been proposed to be critical for social interaction, providing the basis for empathy and joint action. However, the precise relation between observed and executed actions is still poorly understood. Do ongoing actions change the way observers perceive others' actions? To pursue this question, we exploited the bistability of depth-ambiguous point-light walkers, which can be perceived as facing towards the viewer or as facing away from the viewer. We demonstrate that point-light walkers are perceived more often as facing the viewer when the observer is walking on a treadmill compared to when the observer is performing an action that does not match the observed behavior (e.g., cycling). These findings suggest that motor processes influence the perceived orientation of observed actions: Acting observers tend to perceive similar actions by conspecifics as oriented towards themselves. We discuss these results in light of the possible mechanisms subtending action-induced modulation of perception.     

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.     

Self-recognition of avatar motion: how do I know it's me?

When motion is isolated from form cues and viewed from third-person perspectives, individuals are able to recognize their own whole body movements better than those of friends. Because we rarely see our own bodies in motion from third-person viewpoints, this self-recognition advantage may indicate a contribution to perception from the motor system. Our first experiment provides evidence that recognition of self-produced and friends' motion dissociate, with only the latter showing sensitivity to orientation. Through the use of selectively disrupted avatar motion, our second experiment shows that self-recognition of facial motion is mediated by knowledge of the local temporal characteristics of one's own actions. Specifically, inverted self-recognition was unaffected by disruption of feature configurations and trajectories, but eliminated by temporal distortion. While actors lack third-person visual experience of their actions, they have a lifetime of proprioceptive, somatosensory, vestibular and first-person-visual experience. These sources of contingent feedback may provide actors with knowledge about the temporal properties of their actions, potentially supporting recognition of characteristic rhythmic variation when viewing self-produced motion. In contrast, the ability to recognize the motion signatures of familiar others may be dependent on configural topographic cues.     

The frames of reference of the motor-visual aftereffect

Repeatedly performing similar motor acts produces short-term adaptive changes in the agent's motor system. One striking use-dependent effect is the motor-to-visual aftereffect (MVA), a short-lasting negative bias in the conceptual categorization of visually-presented training-related motor behavior. The MVA is considered the behavioral counterpart of the adaptation of visuomotor neurons that code for congruent executed and observed motor acts. Here we characterize which features of the motor training generate the MVA, along 3 main dimensions: a) the relative role of motor acts vs. the semantics of the task-set; b) the role of muscular-specific vs. goal-specific training and c) the spatial frame of reference with respect to the whole body. Participants were asked to repeatedly push or pull some small objects in a bowl as we varied different components of adapting actions across three experiments. The results show that a) the semantic value of the instructions given to the participant have no role in generating the MVA, which depends only on the motor meaning of the training act; b) both intrinsic body movements and extrinsic action goals contribute simultaneously to the genesis of the MVA and c) changes in the relative position of the acting hand compared to the observed hand, when they do not involve changes to the movement performed or to the action meaning, do not have an effect on the MVA. In these series of experiments we confirm that recent motor experiences produce measurable changes in how humans see each others' actions. The MVA is an exquisite motor effect generated by two distinct motor sub-systems, one operating in an intrinsic, muscular specific, frame of reference and the other operating in an extrinsic motor space.     

Your own action influences how you perceive another person's action

A growing body of neuroimaging and neurophysiology studies has demonstrated the motor system's involvement in the observation of actions, but the functional significance of this is still unclear. One hypothesis suggests that the motor system decodes observed actions. This hypothesis predicts that performing a concurrent action should influence the perception of an observed action. We tested this prediction by asking subjects to judge the weight of a box lifted by an actor while the subject either lifted or passively held a light or heavy box. We found that actively lifting a box altered the perceptual judgment; an observed box was judged to be heavier when subjects were lifting the light box, and it was judged to be lighter when they were lifting the heavy box. This result is surprising because previous studies have found facilitating effects of movement on perceptual judgments and facilitating effects of observed actions on movements, but here we found the opposite. We hypothesize that this effect can be understood in terms of overlapping neural systems for motor control and action-understanding if multiple models of possible observed and performed actions are processed.     

Representation of others' action by neurons in monkey medial frontal cortex

Successful social interaction depends on not only the ability to identify with others but also the ability to distinguish between aspects of self and others. Although there is considerable knowledge of a shared neural substrate between self-action and others' action, it remains unknown where and how in the brain the action of others is uniquely represented. Exploring such agent-specific neural codes is important because one's action and intention can differ between individuals. Moreover, the assignment of social agency breaks down in a range of mental disorders. Here, using two monkeys monitoring each other's action for adaptive behavioral planning, we show that the medial frontal cortex (MFC) contains a group of neurons that selectively encode others' action. These neurons, observed in both dominant and submissive monkeys, were significantly more prevalent in the dorsomedial convexity region of the MFC including the pre-supplementary motor area than in the cingulate sulcus region of the MFC including the rostral cingulate motor area. Further tests revealed that the difference in neuronal activity was not due to gaze direction or muscular activity. We suggest that the MFC is involved in self-other differentiation in the domain of motor action and provides a fundamental neural signal for social learning.     

When Passive Feels Active - Delusion-Proneness Alters Self-Recognition in the Moving Rubber Hand Illusion

Psychotic patients have problems with bodily self-recognition such as the experience of self-produced actions (sense of agency) and the perception of the body as their own (sense of ownership). While it has been shown that such impairments in psychotic patients can be explained by hypersalient processing of external sensory input it has also been suggested that they lack normal efference copy in voluntary action. However, it is not known how problems with motor predictions like efference copy contribute to impaired sense of agency and ownership in psychosis or psychosis-related states. We used a rubber hand illusion based on finger movements and measured sense of agency and ownership to compute a bodily self-recognition score in delusion-proneness (indexed by Peters’ Delusion Inventory - PDI). A group of healthy subjects (n=71) experienced active movements (involving motor predictions) or passive movements (lacking motor predictions). We observed a highly significant correlation between delusion-proneness and self-recognition in the passive conditions, while no such effect was observed in the active conditions. This was seen for both ownership and agency scores. The result suggests that delusion-proneness is associated with hypersalient external input in passive conditions, resulting in an abnormal experience of the illusion. We hypothesize that this effect is not present in the active condition because deficient motor predictions counteract hypersalience in psychosis proneness.     

Mirror adaptation in sensory-motor simultaneity

Background

When one watches a sports game, one may feel her/his own muscles moving in synchrony with the player''s. Such parallels between observed actions of others and one''s own has been well supported in the latest progress in neuroscience, and coined “mirror system.” It is likely that due to such phenomena, we are able to learn motor skills just by observing an expert''s performance. Yet it is unknown whether such indirect learning occurs only at higher cognitive levels, or also at basic sensorimotor levels where sensorimotor delay is compensated and the timing of sensory feedback is constantly calibrated.

Methodology/Principal Findings

Here, we show that the subject''s passive observation of an actor manipulating a computer mouse with delayed auditory feedback led to shifts in subjective simultaneity of self mouse manipulation and auditory stimulus in the observing subjects. Likewise, self adaptation to the delayed feedback modulated the simultaneity judgment of the other subjects manipulating a mouse and an auditory stimulus. Meanwhile, subjective simultaneity of a simple visual disc and the auditory stimulus (flash test) was not affected by observation of an actor nor self-adaptation.

Conclusions/Significance

The lack of shift in the flash test for both conditions indicates that the recalibration transfer is specific to the action domain, and is not due to a general sensory adaptation. This points to the involvement of a system for the temporal monitoring of actions, one that processes both one''s own actions and those of others.     

Action Possibility Judgments of People with Varying Motor Abilities Due to Spinal Cord Injury

Predictions about one''s own action capabilities as well as the action capabilities of others are thought to be based on a simulation process involving linked perceptual and motor networks. Given the central role of motor experience in the formation of these networks, one''s present motor capabilities are thought to be the basis of their perceptual judgments about actions. However, it remains unknown whether the ability to form these action possibility judgments is affected by performance related changes in the motor system. To determine if judgments of action capabilities are affected by long-term changes in one''s own motor capabilities, participants with different degrees of upper-limb function due to their level (cervical vs. below cervical) of spinal cord injury (SCI) were tested on a perceptual-motor judgment task. Participants observed apparent motion videos of reciprocal aiming movements with varying levels of difficulty. For each movement, participants determined the shortest movement time (MT) at which they themselves and a young adult could perform the task while maintaining accuracy. Participants also performed the task. Analyses of MTs revealed that perceptual judgments for participant''s own movement capabilities were consistent with their actual performance- people with cervical SCI had longer judged and actual MTs than people with below cervical SCI. However, there were no between-group differences in judged MTs for the young adult. Although it is unclear how the judgments were adjusted (altered simulation vs. threshold modification), the data reveal that people with different motor capabilities due to SCI are not completely biased by their present capabilities and can effectively adjust their judgments to estimate the actions of others.     

Walking but not barking improves verb recovery: implications for action observation treatment in aphasia rehabilitation

Recent studies have shown that action observation treatment without concomitant verbal cue has a positive impact on the recovery of verb retrieval deficits in aphasic patients. In agreement with an embodied cognition viewpoint, a hypothesis has been advanced that gestures and language form a single communication system and words whose retrieval is facilitated by gestures are semantically represented through sensory-motor features. However, it is still an open question as to what extent this treatment approach works. Results from the recovery of motor deficits have suggested that action observation promotes motor recovery only for actions that are part of the motor repertoire of the observer. The aim of the present experiment was to further investigate the role of action observation treatment in verb recovery. In particular, we contrasted the effects induced by observing human actions (e.g. dancing, kicking, pointing, eating) versus non human actions (e.g. barking, printing). Seven chronic aphasic patients with a selective deficit in verb retrieval underwent an intensive rehabilitation training that included five daily sessions over two consecutive weeks. Each subject was asked to carefully observe 115 video-clips of actions, one at a time and, after observing them, they had to produce the corresponding verb. Two groups of actions were randomly presented: humans versus nonhuman actions. In all patients, significant improvement in verb retrieval was found only by observing video-clips of human actions. Moreover, follow-up testing revealed long-term verb recovery that was still present two months after the two treatments had ended. In support of the multimodal concept representation's proposal, we suggest that just the observation of actions pertaining to the human motor repertoire is an effective rehabilitation approach for verb recovery.     

The transfer of motor functional strategies via action observation

When someone is choosing one piece from a bowl full of fruit, many pieces are within reach and visible. Although the desired piece seems to govern the particular pattern and direction of that person's reaching movement, the selection process is not impervious to the presence of task-irrelevant information (i.e. the other fruits). Evidence suggests that the kinematics of reach-to-grasp actions for a desired object integrates the motor features of all the objects which might become potential targets. Transcranial magnetic stimulation (TMS) and motor-evoked potentials (MEPs) were used by us to establish if that motor integration process can be transferred to an onlooker. Our results indicate that observation of hybrid reach-to-grasp movement kinematics is reflected in the observer's pattern of MEP amplitudes. This effect can be defined as a form of motor resonance which operates by 'reading' the kinematics of an observed action. The brain's ability to mirror motor integration processes while observing someone else's action helps an onlooker to understand what the other person is doing and to predict his/her motor alternatives.     

Being Moved by the Self and Others: Influence of Empathy on Self-Motion Perception

Background

The observation of conspecifics influences our bodily perceptions and actions: Contagious yawning, contagious itching, or empathy for pain, are all examples of mechanisms based on resonance between our own body and others. While there is evidence for the involvement of the mirror neuron system in the processing of motor, auditory and tactile information, it has not yet been associated with the perception of self-motion.

Methodology/Principal Findings

We investigated whether viewing our own body, the body of another, and an object in motion influences self-motion perception. We found a visual-vestibular congruency effect for self-motion perception when observing self and object motion, and a reduction in this effect when observing someone else''s body motion. The congruency effect was correlated with empathy scores, revealing the importance of empathy in mirroring mechanisms.

Conclusions/Significance

The data show that vestibular perception is modulated by agent-specific mirroring mechanisms. The observation of conspecifics in motion is an essential component of social life, and self-motion perception is crucial for the distinction between the self and the other. Finally, our results hint at the presence of a “vestibular mirror neuron system”.     

What are you doing? How active and observational experience shape infants' action understanding

From early in life, infants watch other people''s actions. How do young infants come to make sense of actions they observe? Here, we review empirical findings on the development of action understanding in infancy. Based on this review, we argue that active action experience is crucial for infants'' developing action understanding. When infants execute actions, they form associations between motor acts and the sensory consequences of these acts. When infants subsequently observe these actions in others, they can use their motor system to predict the outcome of the ongoing actions. Also, infants come to an understanding of others’ actions through the repeated observation of actions and the effects associated with them. In their daily lives, infants have plenty of opportunities to form associations between observed events and learn about statistical regularities of others’ behaviours. We argue that based on these two forms of experience—active action experience and observational experience—infants gradually develop more complex action understanding capabilities.