Contextual movement constraints of others modulate motor preparation in the observer

Previous research demonstrated that observing an action seems to automatically activate a corresponding motor representation in the observer. It has been argued that this direct matching of observed on executed actions is modulated by contextual factors. An open question is whether observing another person being physically restrained has an influence on action execution in the observer. Using performance measures we found a slowing of response times when perceiving others’ hands being physically restrained (Experiment 1). We did not find a slowing effect when participants responded with their feet ruling out a general perceptual interpretation of the present findings (Experiment 2). To further test our hypothesis, we measured event-related brain potentials (ERPs). The ERP results demonstrate that the observed slowing effect is reflected in a decrease of motor-related ERP components (Experiment 3). Perceiving others’ hands physically restrained impairs motor preparation in the observer. Our findings suggest that observed environmental constraints are automatically mapped onto the observer's motor system. Such a mapping of motor restraints might facilitate action understanding.     

Hands on the future: facilitation of cortico‐spinal hand‐representation when reading the future tense of hand‐related action verbs

Reading action‐related verbs brings about sensorimotor neural activity, suggesting that the linguistic representation of actions impinges upon neural structures largely overlapping with those involved in actual action execution. While studies of direct action observation indicate that motor mirroring is inherently anticipatory, no information is currently available on whether deriving action‐related knowledge from language also takes into account the temporal deployment of actions. Using transcranial magnetic stimulation, here we sought to determine whether reading action verbs conjugated in the future induced higher cortico‐spinal activity with respect to when the same verbs were conjugated in the past tense. We recorded motor‐evoked potentials (MEPs) from relaxed hand and leg muscles of healthy subjects who were reading silently hand‐ or leg‐related action, sensorial (non‐somatic) and abstract verbs conjugated either in future or past tense. The amplitude of MEPs recorded from the hand was higher during reading hand‐related action verbs conjugated in the future than in the past. No future‐related modulation of leg muscles activity was found during reading leg‐related action verbs. In a similar vein, no future‐related change of hand or leg muscles reactivity was found for abstract or sensorial verbs. These results indicate that the anticipatory mirroring of hand actions may be triggered by linguistic representations and not only by direct action observation.     

Action intentions modulate visual processing during action perception

The current debate on mechanisms of action understanding and recognition has re-opened the question of how perceptual and motor systems are linked. It has been proposed that the human motor system has a role in action perception; however, there is still no direct evidence that actions can modulate early neural processes associated with perception of meaningful actions. Here we show that plans for action modulate the perceptual processing of observed actions within 200 ms of stimulus onset. We examined event-related potentials to images of hand gestures presented while participants planned either a matching (congruent) or non-matching (incongruent) gesture. The N170/VPP, representing visual processing of hand gestures, was reliably altered when participants concurrently planned congruent versus incongruent actions. In a second experiment, we showed that this congruency effect was specific to action planning and not to more general semantic aspects of action representation. Our findings demonstrate that actions encoded via the motor system have a direct effect on visual processing, and thus imply a bi-directional link between action and perception in the human brain. We suggest that through forward modelling, intended actions can facilitate the encoding of sensory inputs that would be expected as a consequence of the action.     

Interpreting actions: the goal behind mirror neuron function

Crucial to our everyday social functioning is an ability to interpret the behaviors of others. This process involves a rapid understanding of what a given action is not only in a physical sense (e.g., a precision grip around the stem of a wine glass) but also in a semantic sense (e.g., an invitation to "cheers"). The functional properties of fronto-parietal mirror neurons (MNs), which respond to both observed and executed actions, have been a topic of much debate in the cognitive neuroscience literature. The controversy surrounds the role of the "mirror neuron system" in action understanding: do MNs allow us to comprehend others' actions by allowing us to internally represent their behaviors or do they simply activate a direct motor representation of the perceived act without recourse to its meaning? This review outlines evidence from both human and primate literatures, indicating the importance of end-goals in action representations within the motor system and their predominance in influencing action plans. We integrate this evidence with recent views regarding the complex and dynamic nature of the mirror neuron system and its ability to respond to broad motor outcomes.     

Sensorimotor cortex as a critical component of an 'extended' mirror neuron system: Does it solve the development,correspondence, and control problems in mirroring?

A core assumption of how humans understand and infer the intentions and beliefs of others is the existence of a functional self-other distinction. At least two neural systems have been proposed to manage such a critical distinction. One system, part of the classic motor system, is specialized for the preparation and execution of motor actions that are self realized and voluntary, while the other appears primarily involved in capturing and understanding the actions of non-self or others. The latter system, of which the mirror neuron system is part, is the canonical action 'resonance' system in the brain that has evolved to share many of the same circuits involved in motor control. Mirroring or 'shared circuit systems' are assumed to be involved in resonating, imitating, and/or simulating the actions of others. A number of researchers have proposed that shared representations of motor actions may form a foundational cornerstone for higher order social processes, such as motor learning, action understanding, imitation, perspective taking, understanding facial emotions, and empathy. However, mirroring systems that evolve from the classic motor system present at least three problems: a development, a correspondence, and a control problem. Developmentally, the question is how does a mirroring system arise? How do humans acquire the ability to simulate through mapping observed onto executed actions? Are mirror neurons innate and therefore genetically programmed? To what extent is learning necessary? In terms of the correspondence problem, the question is how does the observer agent know what the observed agent's resonance activation pattern is? How does the matching of motor activation patterns occur? Finally, in terms of the control problem, the issue is how to efficiently control a mirroring system when it is turned on automatically through observation? Or, as others have stated the problem more succinctly: "Why don't we imitate all the time?" In this review, we argue from an anatomical, physiological, modeling, and functional perspectives that a critical component of the human mirror neuron system is sensorimotor cortex. Not only are sensorimotor transformations necessary for computing the patterns of muscle activation and kinematics during action observation but they provide potential answers to the development, correspondence and control problems.     

Mirroring avatars: dissociation of action and intention in human motor resonance

Observation of others' actions induces a subliminal activation of motor pathways (motor resonance) that is mediated by the mirror neuron system and reflects the motor program encoding the observed action. Whether motor resonance represents the movements composing an action or also its motor intention remains of debate, as natural actions implicitly contain their motor intentions. Here, action and intention are dissociated using a natural and an impossible action with the same grasping intention: subjects observe an avatar grasping a ball using either a natural hand action ('palmar' finger flexion) or an impossible hand action ('dorsal' finger flexion). Motor-evoked potentials (MEPs), elicited by single transcranial magnetic stimulation of the hand area in the primary motor cortex, were used to measure the excitability modulation of motor pathways during observation of the two different hand actions. MEPs were recorded from the opponens pollicis (OP), abductor digiti minimi (ADM) and extensor carpi radialis (ECR) muscles. A significant MEP facilitation was found in the OP, during observation of the grasping phase of the natural action; MEPs in the ADM were facilitated during observation of the hand opening phase of the natural action and of both opening and grasping phases of the impossible action. MEPs in the ECR were not affected. As different resonant responses are elicited by the observation of the two different actions, despite their identical intention, we conclude that the mirror neuron system cannot utilize the observer's subliminal motor program in the primary motor cortex to encode action intentions.     

How are observed actions mapped to the observer's motor system? Influence of posture and perspective

Previous studies using transcranial magnetic stimulation (TMS) have shown that during the observation of actions performed by others, the observer's primary motor cortex (M1) becomes facilitated in a highly muscle specific fashion. Here, we used TMS to explore the effect of posture, perspective and body side on muscle specific facilitation of left M1. Subjects viewed video's showing left and right hand extension (palm-down) movements from a first person or third person perspective with their hand posture either congruent (palm-down) or incongruent (palm-up) to the posture of the observed model. Data indicated that facilitation of left M1 was substantially different for observing actions executed with the right (contralateral) or left (ipsilateral) hand. For right hand actions, facilitation of left M1 was shown to be highly specific to the muscle used in the observed action ('intrinsic mapping'). During the observation of left hand stimuli, only half of the subjects displayed this muscle specific facilitation, whereas in the other half, M1 was facilitated according to the observed movement direction ('extrinsic mapping'). Absolute effect magnitude was particularly high when right hand actions were observed from a first person perspective, whereas, for left hand actions, the third person perspective was more efficient. The degree of postural congruency between body parts of the observer and observed model only mildly influenced M1 facilitation. Since action observation is increasingly considered in rehabilitation therapies, the present findings may help identifying the most effective conditions for stimulating the motor system during action observation.     

Neurophysiological distinction of verb categories

Neurophysiological brain responses to subcategories of action verbs were recorded using high resolution EEG. Starting 240 ms after word onset, topographies of event-related potentials distinguished between verbs referring to different action types. Current source density estimates revealed that verbs referring to actions executed with the legs (to kick) produced an activity focus close to the vertex, above motor areas involved in the programming of leg movements, whereas face-related verbs (to speak) produced a focus at left-lateral recordings, above perisylvian areas and the cortical representation of the face and articulators. This is evidence that brain mechanisms involved in word processing can differ even between fine-grained lexico-semantic subcategories and already within the first quarter of a second after word onset. We offer an explanation of the data in neurobiological terms.     

Impaired imitation of meaningless gestures in ideomotor apraxia: a conceptual problem not a disorder of action control? A single case investigation

A defining characteristic of ideomotor apraxia is an inability to imitate meaningless gestures. This is widely interpreted as being due to difficulties in the formulation or execution of motor programs for complex action, but an alternative view is that there is a higher level cognitive problem in conceptualisation of the target posture. In a single case with inferior left parietal and temporal damage, severely impaired imitation was accompanied by preserved motor skill and spatial awareness but inability to make a conceptual match between the fingers of his own hand and an observed hand. Also, he was able to match pictures of visually similar gestures but not cartoon drawings of gestures which were conceptually the same but visually dissimilar. Knowledge of body structure seemed largely intact as he was only slightly inaccurate in showing correspondences between locations on drawings of a human figure and his own body, or a visually dissimilar figure. This indicated that difficulty on matching gestures was specific to representation of body posture rather than body structure, or that gesture imitation tasks place higher demand on a structural representation of the body. These data imply that for at least some cases of ideomotor apraxia, impaired gesture imitation is due to a deficit in representing the observed posture and is not a deficit in memory for action or of motor control.     

The observation and hearing of eating actions activates motor programs related to eating in macaque monkeys

The observation of actions can lead, in some cases, to the repetition of those same actions. In other words, motor programs similar to those observed can be recruited. Since this phenomenon is expressed when in the presence of another individual, it has been named social facilitation. In the present study we investigated whether the observation and/or hearing of eating actions facilitate eating behaviors in observing/listening pig-tailed macaques. In experiment 1, the observation of an eating room mate significantly enhanced eating behavior in the observer. Similar results were obtained (experiment 2) in response to the sound of eating actions but not to control sounds (experiment 3). We propose that eating facilitation triggered by observation or listening of eating actions can rely on the mirror neuron system of ventral premotor cortex that provides a matching between the observed/listened action and the executed action. This matching system can subsequently trigger the motor programs necessary for repeating the observed/heard actions.     

The motor cortex is causally related to predictive eye movements during action observation

We examined the hypothesis that predictive gaze during observation of other people's actions depends on the activation of corresponding action plans in the observer. Using transcranial magnetic stimulation and eye-tracking technology we found that stimulation of the motor hand area, but not of the leg area, slowed gaze predictive behavior (compared to no TMS). This result shows that predictive eye movements to others' action goals depend on a somatotopical recruitment of the observer's motor system. The study provides direct support for the view that a direct matching process implemented in the mirror-neuron system plays a functional role for real-time goal prediction.     

Motor facilitation during action observation: topographic mapping of the target muscle and influence of the onlooker's posture

Transcranial magnetic stimulation (TMS) studies report that viewing a given action performed by a model activates the neural representation of the onlooker's muscles that are activated during the actual execution of the observed action. Here we sought to determine whether this mirror observation-execution facilitation reflects only muscular specificity or whether it is also influenced by postural congruency between onlooker/model body parts. We recorded motor potentials evoked by single-pulse TMS from the first dorsal interosseous (FDI) and abductor digiti minimi (ADM) muscles during observation of the right index and little finger abduction/adduction movements of models who kept their hands in a palm-down or palm-up position. Moreover, in different experiments observers kept their right hand palm down or palm up. Selective motor facilitation was observed during observation of movements that map the motor function of the targeted muscles, regardless of the posture of the observed hand. Modulation of FDI, however, was obtained only when participants kept their hand palm down; by contrast, modulation of ADM was obtained only when participants kept their hand palm up. Interestingly, electromyographic recordings showed that FDI is mostly active when index abduction/adduction movements are performed in the palm-down position, whereas ADM is mostly active when little finger abduction/adduction movements are performed in the palm-up position. Results show that the influence of the onlooker's hand posture is comparable in action execution and observation, thus indicating a fine-grain functional correspondence between these two processes.     

Motor cortex excitability is tightly coupled to observed movements

Although facilitation of the corticospinal (CS) system during action observation is a widely accepted phenomenon, it is still controversial if facilitation reflects the replica of observed movement kinematics or the tension to achieve a particular goal. In this study, transcranial magnetic stimulation (TMS)-induced motor evoked potentials (MEPs) were recorded from the abductor digiti minimi (ADM) and the first dorsal interosseus (FDI) muscles while participant-volunteers observed a model grasping a small target eliciting a precision grip or a large target eliciting a whole hand grasp directed toward an isolated object or flanked by different sized objects (i.e., distractor). A detailed movement analysis revealed that the model's kinematics were influenced by the distractor's size. Video clips filming the scene were edited in such a way that the distractor was removed from the scene. Participant-volunteers were asked to observe actions characterized by the same goal but performed using different kinematical patterns. Although the differences in movement kinematics were not noticed by the participant-volunteers, they nonetheless elicited distinct configurations of corticospinal activation. Detailed motor matching seems to recruit the same muscles in the onlooker as in the person actually carrying out the action during observation of grasping actions. These effects appear to be elicited by very subtle, imperceptible aspects of observed actions pointing to a finely tuned mechanism that specifically encodes body parts.     

Action verbs and the primary motor cortex: a comparative TMS study of silent reading, frequency judgments, and motor imagery

Single pulse transcranial magnetic stimulation (TMS) was applied to the hand area of the left primary motor cortex or, as a control, to the vertex (STIMULATION: TMS(M1) vs. TMS(vertex)) while right-handed volunteers silently read verbs related to hand actions. We examined three different tasks and time points for stimulation within the same experiment: subjects indicated with their left foot when they (i) had finished reading, (ii) had judged whether the corresponding movement involved a hand rotation after simulating the hand movement, and (iii) had judged whether they would frequently encounter the action verb in a newspaper (TASK: silent reading, motor imagery, and frequency judgment). Response times were compared between TMS(M1) and TMS(vertex), both applied at different time points after stimulus onset (DELAY: 150, 300, 450, 600, and 750 ms). TMS(M1) differentially modulated task performance: there was a significant facilitatory effect of TMS(M1) for the imagery task only (about 88 ms), with subjects responding about 10% faster (compared to TMS(vertex)). In contrast, response times for silent reading and frequency judgments were unaffected by TMS(M1). No differential effect of the time point of TMS(M1) was observed. The differential effect of TMS(M1) when subjects performed a motor imagery task (relative to performing silent reading or frequency judgments with the same set of verbs) suggests that the primary motor cortex is critically involved in processing action verbs only when subjects are simulating the corresponding movement. This task-dependent effect of hand motor cortex TMS on the processing of hand-related action verbs is discussed with respect to the notion of embodied cognition and the associationist theory.     

Modulation of premotor mirror neuron activity during observation of unpredictable grasping movements

Using transcranial magnetic stimulation, we explored the properties of premotor mirror neurons during the passive observation of a reaching-grasping movement in human subjects. Two different experiments were run using video-clips as visual stimuli. Video-clips showed a normally performed (control stimulus) or an anomalous reaching-grasping movement executed by delaying the time of the appearance of the maximal finger aperture (experiment 1), or substituting it with an unpredictable closure (experiment 2). Motor evoked potentials were recorded at different time-points during the observation of the video-clips. Profiles of cortical excitability were drawn and compared with the kinematic profiles of the corresponding movement. Passive observation of the natural movement evoked a profile of cortical excitability that is in concordance with the timing of the kinematic profile of the shown finger movements. Observation of the uncommon movements did not exert any modulation (experiment 1) or evoked an activity that matched, at the beginning, the modulation obtained with observation of the natural movement (experiment 2). Results show that the resonant motor plan is loaded as whole at the beginning of observation and once started tends to proceed to its completion regardless of changes to the visual cues. The results exclude the possibility of a temporal fragmentation of the resonant plan, because activation of different populations of mirror neurons for each phase of the ongoing action. They further support the notion of the role of the mirror system as neural substrate for the observing-execution matching system and extend the current knowledge regarding mechanisms that trigger the internal representation of an action.     

Imitation and action understanding in autistic spectrum disorders: how valid is the hypothesis of a deficit in the mirror neuron system?

The motor mirror neuron system supports imitation and goal understanding in typical adults. Recently, it has been proposed that a deficit in this mirror neuron system might contribute to poor imitation performance in children with autistic spectrum disorders (ASD) and might be a cause of poor social abilities in these children. We aimed to test this hypothesis by examining the performance of 25 children with ASD and 31 typical children of the same verbal mental age on four action representation tasks and a theory of mind battery. Both typical and autistic children had the same tendency to imitate an adult's goals, to imitate in a mirror fashion and to imitate grasps in a motor planning task. Children with ASD showed superior performance on a gesture recognition task. These imitation and gesture recognition tasks all rely on the mirror neuron system in typical adults, but performance was not impaired in children with ASD. In contrast, the ASD group were impaired on the theory of mind tasks. These results provide clear evidence against a general imitation impairment and a global mirror neuron system deficit in children with autism. We suggest this data can best be understood in terms of multiple brain systems for different types of imitation and action understanding, and that the ability to understand and imitate the goals of hand actions is intact in children with ASD.     

Understanding motor resonance

The discovery of mirror neurons in monkeys, and the finding of motor activity during action observation in humans are generally regarded to support motor theories of action understanding. These theories take motor resonance to be essential in the understanding of observed actions and the inference of action goals. However, the notions of "resonance," "action understanding," and "action goal" appear to be used ambiguously in the literature. A survey of the literature on mirror neurons and motor resonance yields two different interpretations of the term "resonance," three different interpretations of action understanding, and again three different interpretations of what the goal of an action is. This entails that, unless it is specified what interpretation is used, the meaning of any statement about the relation between these concepts can differ to a great extent. By discussing an experiment we will show that more precise definitions and use of the concepts will allow for better assessments of motor theories of action understanding and hence a more fruitful scientific debate. Lastly, we will provide an example of how the discussed experimental setup could be adapted to test other interpretations of the concepts.     

The origin of thalamic inputs to the "hand" representation in the primary motor cortex.

We used retrograde transport of WGA-HRP to examine the origin of thalamic inputs to the "hand" representation in the primary motor cortex of macaques (Macaca nemestrina). Injections were placed in either the crest of the precentral gyrus or the rostral bank of the central sulcus. The sites for injection in the sulcus were determined by using intracortical stimulation to map the location of hand representation. We found that the precentral gyrus and central sulcus receive their predominant input from different subdivisions of the ventrolateral thalamus. Ventralis posterior lateralis pars oralis (VPLo) provides the most substantial input to a portion of the hand representation on the gyrus. In contrast, Ventralis lateralis pars oralis (VLo) provides the most substantial input to a portion of the hand representation in the sulcus. Prior studies have shown that VPLo is a major site of termination of cerebellar efferents and that VLo is a major site of termination of pallidal efferents. Thus, our results indicate that both the basal ganglia and the cerebellum "directly" influence the "hand" representation of the primary motor cortex.     

Understanding 'what' others do: mirror mechanisms play a crucial role in action perception

Neurophysiological and imaging studies suggest that the inferior frontal cortex (IFC) implements a mechanism that matches perceived actions to one's motor representation of similar actions (mirror mechanism) and recent lesion studies have also established that IFC is critical for action perception. However, to date causative evidence that action perception requires activation within the same populations of IFC neurons involved in action execution is lacking. In this issue, Cattaneo and colleagues provide the first direct evidence that mirror mechanisms in IFC influence action perception. We discuss the implications of these findings for the understanding of the functional role of mirror mechanisms.     

Anterior intraparietal cortex codes complexity of observed hand movements

Human and monkey studies clearly show that the anterior intraparietal area (AIP) is crucial for hand-related visuomotor transformations. Human AIP activates also during observation of hand actions, involving it in the mirror system. It is not known, however, whether its activation can also reflect a difference in the complexity of the observed action. In the present study we used functional magnetic resonance imaging (fMRI) to explore the activation of human area AIP during the observation of complex object-manipulation tasks (e.g. inserting a key in a lock and turning it) as compared to simple tasks (whole hand grasping of an object) executed with the left and the right hand in a first person perspective. The results show that, in general, both complex and simple tasks produced an activation of the fronto-parietal mirror system and that the activity of AIP in each hemisphere was higher during observation of the contralateral hand (hand identity effect). A Region-Of-Interest (ROI) analysis of the parietal activations responding to hand identity showed that each AIP was more active during the observation of complex with respect to simple tasks. In the right AIP this effect was stronger during observation of the contralateral hand, in the left AIP was strong during observation of both hands. This complexity-related property was not observed in the other activated areas. These findings support the concept that the observation of motor acts retrieves the internal representation of those same acts in the observer's motor system (direct-matching hypothesis based on the mirror neuron mechanism).