Somatic and motor components of action simulation

Seminal studies in monkeys report that the viewing of actions performed by other individuals activates frontal and parietal cortical areas typically involved in action planning and execution. That mirroring actions might rely on both motor and somatosensory components is suggested by reports that action observation and execution increase neural activity in motor and in somatosensory areas. This occurs not only during observation of naturalistic movements but also during the viewing of biomechanically impossible movements that tap the afferent component of action, possibly by eliciting strong somatic feelings in the onlooker. Although somatosensory feedback is inherently linked to action execution, information on the possible causative role of frontal and parietal cortices in simulating motor and sensory action components is lacking. By combining low-frequency repetitive and single-pulse transcranial magnetic stimulation, we found that virtual lesions of ventral premotor cortex (vPMc) and primary somatosensory cortex (S1) suppressed mirror motor facilitation contingent upon observation of possible and impossible movements, respectively. In contrast, virtual lesions of primary motor cortex did not influence mirror motor facilitation. The reported double dissociation suggests that vPMc and S1 play an active, differential role in simulating efferent and afferent components of observed actions.     

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.     

Nonvisual motor learning influences abstract action observation

Neuroimaging studies have recently provided support for the existence of a human equivalent of the "mirror-neuron" system as first described in monkeys [1], involved in both the execution of movements as well as the observation and imitation of actions performed by others (e.g., [2-6]). A widely held conception concerning this system is that the understanding of observed actions is mediated by a covert simulation process [7]. In the present fMRI experiment, this simulation process was probed by asking subjects to discriminate between visually presented trajectories that either did or did not match previously performed but unseen continuous movement sequences. A specific network of learning-related premotor and parietal areas was found to be reactivated when participants were confronted with their movements' visual counterpart. Moreover, the strength of these reactivations was dependent on the observers' experience with executing the corresponding movement sequence. These findings provide further support for the emerging view that embodied simulations during action observation engage widespread activations in cortical motor regions beyond the classically defined mirror-neuron system. Furthermore, the obtained results extend previous work by showing experience-dependent perceptual modulations at the neural systems level based on nonvisual motor learning.     

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.     

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.     

Somatosensory-Motor Adaptation of Orofacial Actions in Posterior Parietal and Ventral Premotor Cortices

Recent studies have provided evidence for sensory-motor adaptive changes and action goal coding of visually guided manual action in premotor and posterior parietal cortices. To extend these results to orofacial actions, devoid of auditory and visual feedback, we used a repetition suppression paradigm while measuring neural activity with functional magnetic resonance imaging during repeated intransitive and silent lip, jaw and tongue movements. In the motor domain, this paradigm refers to decreased activity in specific neural populations due to repeated motor acts and has been proposed to reflect sensory-motor adaptation. Orofacial movements activated a set of largely overlapping, common brain areas forming a core neural network classically involved in orofacial motor control. Crucially, suppressed neural responses during repeated orofacial actions were specifically observed in the left ventral premotor cortex, the intraparietal sulcus, the inferior parietal lobule and the superior parietal lobule. Since no visual and auditory feedback were provided during orofacial actions, these results suggest somatosensory-motor adaptive control of intransitive and silent orofacial actions in these premotor and parietal regions.     

Spatio-Temporal Dynamics of Human Intention Understanding in Temporo-Parietal Cortex: A Combined EEG/fMRI Repetition Suppression Paradigm

Inferring the intentions of other people from their actions recruits an inferior fronto-parietal action observation network as well as a putative social network that includes the posterior superior temporal sulcus (STS). However, the functional dynamics within and among these networks remains unclear. Here we used functional magnetic resonance imaging (fMRI) and high-density electroencephalogram (EEG), with a repetition suppression design, to assess the spatio-temporal dynamics of decoding intentions. Suppression of fMRI activity to the repetition of the same intention was observed in inferior frontal lobe, anterior intraparietal sulcus (aIPS), and right STS. EEG global field power was reduced with repeated intentions at an early (starting at 60 ms) and a later (∼330 ms) period after the onset of a hand-on-object encounter. Source localization during these two intervals involved right STS and aIPS regions highly consistent with RS effects observed with fMRI. These results reveal the dynamic involvement of temporal and parietal networks at multiple stages during the intention decoding and without a strict segregation of intention decoding between these networks.     

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.     

Effects of Context on Visuomotor Interference Depends on the Perspective of Observed Actions

Visuomotor interference occurs when the execution of an action is facilitated by the concurrent observation of the same action and hindered by the concurrent observation of a different action. There is evidence that visuomotor interference can be modulated top-down by higher cognitive functions, depending on whether own performed actions or observed actions are selectively attended. Here, we studied whether these effects of cognitive context on visuomotor interference are also dependent on the point-of-view of the observed action. We employed a delayed go/no-go task known to induce visuomotor interference. Static images of hand gestures in either egocentric or allocentric perspective were presented as “go” stimuli after participants were pre-cued to prepare either a matching (congruent) or non-matching (incongruent) action. Participants performed this task in two different cognitive contexts: In one, they focused on the visual image of the hand gesture shown as the go stimulus (image context), whereas in the other they focused on the hand gesture they performed (action context). We analyzed reaction times to initiate the prepared action upon presentation of the gesture image and found evidence of visuomotor interference in both contexts and for both perspectives. Strikingly, results show that the effect of cognitive context on visuomotor interference also depends on the perspective of observed actions. When focusing on own-actions, visuomotor interference was significantly less for gesture images in allocentric perspective than in egocentric perspective; when focusing on observed actions, visuomotor interference was present regardless of the perspective of the gesture image. Overall these data suggest that visuomotor interference may be modulated by higher cognitive processes, so that when we are specifically attending to our own actions, images depicting others’ actions (allocentric perspective) have much less interference on our own actions.     

Observational learning of new movement sequences is reflected in fronto-parietal coherence

Mankind is unique in her ability for observational learning, i.e. the transmission of acquired knowledge and behavioral repertoire through observation of others' actions. In the present study we used electrophysiological measures to investigate brain mechanisms of observational learning. Analysis investigated the possible functional coupling between occipital (alpha) and motor (mu) rhythms operating in the 10 Hz frequency range for translating "seeing" into "doing". Subjects observed movement sequences consisting of six consecutive left or right hand button presses directed at one of two target-buttons for subsequent imitation. Each movement sequence was presented four times, intervened by short pause intervals for sequence rehearsal. During a control task subjects observed the same movement sequences without a requirement for subsequent reproduction. Although both alpha and mu rhythms desynchronized during the imitation task relative to the control task, modulations in alpha and mu power were found to be largely independent from each other over time, arguing against a functional coupling of alpha and mu generators during observational learning. This independence was furthermore reflected in the absence of coherence between occipital and motor electrodes overlaying alpha and mu generators. Instead, coherence analysis revealed a pair of symmetric fronto-parietal networks, one over the left and one over the right hemisphere, reflecting stronger coherence during observation of movements than during pauses. Individual differences in fronto-parietal coherence were furthermore found to predict imitation accuracy. The properties of these networks, i.e. their fronto-parietal distribution, their ipsilateral organization and their sensitivity to the observation of movements, match closely with the known properties of the mirror neuron system (MNS) as studied in the macaque brain. These results indicate a functional dissociation between higher order areas for observational learning (i.e. parts of the MNS as reflected in 10 Hz coherence measures) and peripheral structures (i.e. lateral occipital gyrus for alpha; central sulcus for mu) that provide low-level support for observation and motor imagery of action sequences.     

Interpersonal Liking Modulates Motor-Related Neural Regions

Observing someone perform an action engages brain regions involved in motor planning, such as the inferior frontal, premotor, and inferior parietal cortices. Recent research suggests that during action observation, activity in these neural regions can be modulated by membership in an ethnic group defined by physical differences. In this study we expanded upon previous research by matching physical similarity of two different social groups and investigating whether likability of an outgroup member modulates activity in neural regions involved in action observation. Seventeen Jewish subjects were familiarized with biographies of eight individuals, half of the individuals belonged to Neo-Nazi groups (dislikable) and half of which did not (likable). All subjects and actors in the stimuli were Caucasian and physically similar. The subjects then viewed videos of actors portraying the characters performing simple motor actions (e.g. grasping a water bottle and raising it to the lips), while undergoing fMRI. Using multivariate pattern analysis (MVPA), we found that a classifier trained on brain activation patterns successfully discriminated between the likable and dislikable action observation conditions within the right ventral premotor cortex. These data indicate that the spatial pattern of activity in action observation related neural regions is modulated by likability even when watching a simple action such as reaching for a cup. These findings lend further support for the notion that social factors such as interpersonal liking modulate perceptual processing in motor-related cortices.     

Dissociating object directed and non-object directed action in the human mirror system; implications for theories of motor simulation

Mirror neurons are single cells found in macaque premotor and parietal cortices that are active during action execution and observation. In non-human primates, mirror neurons have only been found in relation to object-directed movements or communicative gestures, as non-object directed actions of the upper limb are not well characterized in non-human primates. Mirror neurons provide important evidence for motor simulation theories of cognition, sometimes referred to as the direct matching hypothesis, which propose that observed actions are mapped onto associated motor schemata in a direct and automatic manner. This study, for the first time, directly compares mirror responses, defined as the overlap between action execution and observation, during object directed and meaningless non-object directed actions. We present functional MRI data that demonstrate a clear dissociation between object directed and non-object directed actions within the human mirror system. A premotor and parietal network was preferentially active during object directed actions, whether observed or executed. Moreover, we report spatially correlated activity across multiple voxels for observation and execution of an object directed action. In contrast to predictions made by motor simulation theory, no similar activity was observed for non-object directed actions. These data demonstrate that object directed and meaningless non-object directed actions are subserved by different neuronal networks and that the human mirror response is significantly greater for object directed actions. These data have important implications for understanding the human mirror system and for simulation theories of motor cognition. Subsequent theories of motor simulation must account for these differences, possibly by acknowledging the role of experience in modulating the mirror response.     

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.     

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.     

Eye-Head Coordination for Visual Cognitive Processing

We investigated coordinated movements between the eyes and head (“eye-head coordination”) in relation to vision for action. Several studies have measured eye and head movements during a single gaze shift, focusing on the mechanisms of motor control during eye-head coordination. However, in everyday life, gaze shifts occur sequentially and are accompanied by movements of the head and body. Under such conditions, visual cognitive processing influences eye movements and might also influence eye-head coordination because sequential gaze shifts include cycles of visual processing (fixation) and data acquisition (gaze shifts). In the present study, we examined how the eyes and head move in coordination during visual search in a large visual field. Subjects moved their eyes, head, and body without restriction inside a 360° visual display system. We found patterns of eye-head coordination that differed those observed in single gaze-shift studies. First, we frequently observed multiple saccades during one continuous head movement, and the contribution of head movement to gaze shifts increased as the number of saccades increased. This relationship between head movements and sequential gaze shifts suggests eye-head coordination over several saccade-fixation sequences; this could be related to cognitive processing because saccade-fixation cycles are the result of visual cognitive processing. Second, distribution bias of eye position during gaze fixation was highly correlated with head orientation. The distribution peak of eye position was biased in the same direction as head orientation. This influence of head orientation suggests that eye-head coordination is involved in gaze fixation, when the visual system processes retinal information. This further supports the role of eye-head coordination in visual cognitive processing.     

Predictive motor activation during action observation in human infants

Certain regions of the human brain are activated both during action execution and action observation. This so-called ‘mirror neuron system’ has been proposed to enable an observer to understand an action through a process of internal motor simulation. Although there has been much speculation about the existence of such a system from early in life, to date there is little direct evidence that young infants recruit brain areas involved in action production during action observation. To address this question, we identified the individual frequency range in which sensorimotor alpha-band activity was attenuated in nine-month-old infants'' electroencephalographs (EEGs) during elicited reaching for objects, and measured whether activity in this frequency range was also modulated by observing others'' actions. We found that observing a grasping action resulted in motor activation in the infant brain, but that this activity began prior to observation of the action, once it could be anticipated. These results demonstrate not only that infants, like adults, display overlapping neural activity during execution and observation of actions, but that this activation, rather than being directly induced by the visual input, is driven by infants'' understanding of a forthcoming action. These results provide support for theories implicating the motor system in action prediction.     

Granger causality mapping during joint actions reveals evidence for forward models that could overcome sensory-motor delays

Studies investigating joint actions have suggested a central role for the putative mirror neuron system (pMNS) because of the close link between perception and action provided by these brain regions [1], [2], [3]. In contrast, our previous functional magnetic resonance imaging (fMRI) experiment demonstrated that the BOLD response of the pMNS does not suggest that it directly integrates observed and executed actions during joint actions [4]. To test whether the pMNS might contribute indirectly to the integration process by sending information to brain areas responsible for this integration (integration network), here we used Granger causality mapping (GCM) [5]. We explored the directional information flow between the anterior sites of the pMNS and previously identified integrative brain regions. We found that the left BA44 sent more information than it received to both the integration network (left thalamus, right middle occipital gyrus and cerebellum) and more posterior nodes of the pMNS (BA2). Thus, during joint actions, two anatomically separate networks therefore seem effectively connected and the information flow is predominantly from anterior to posterior areas of the brain. These findings suggest that the pMNS is involved indirectly in joint actions by transforming observed and executed actions into a common code and is part of a generative model that could predict the future somatosensory and visual consequences of observed and executed actions in order to overcome otherwise inevitable neural delays.     

Action representation in patients with bilateral vestibular impairments

During mental actions subjects feel themselves performing a movement without any corresponding motor output. Although broad information is available regarding the influence of central lesions on action representation, little is known about how peripheral damages affect mental events. In the current study, we investigated whether lack of vestibular information influences action representation. Twelve healthy adults and twelve patients with bilateral vestibular damage actually performed and mentally simulated walking and drawing. The locomotor paths implied one (first walking task) and four (second walking task) changes in the walking direction. In the drawing task, participants drew on a sheet of paper a path that was similar to that of the second walking task. We recorded and compared between the two groups the timing of actual and mental movements. We found significant temporal discrepancies between actual and mental walking movements in the group of patients. Conversely, drawing actual and drawing mental durations were similar. For the control group, an isochrony between mental and actual movements was observed for the three tasks. This result denotes an inconsistency between action representation and action execution following vestibular damage, which is specific to walking movements, and emphasizes the role of the vestibular system upon mental states of actions. This observation may have important clinical implications. During action planning vestibular patients may overestimate the capacity of their motor system (imaging faster, executing slower) with harmful consequences for their health.     

Action Processing and Mirror Neuron Function in Patients with Amyotrophic Lateral Sclerosis: An fMRI Study

Amyotrophic lateral sclerosis (ALS) is a highly debilitating and rapidly fatal neurodegenerative disease. It has been suggested that social cognition may be affected, such as impairment in theory of mind (ToM) ability. Despite these findings, research in this area is scarce and the investigation of neural mechanisms behind such impairment is absent. Nineteen patients with ALS and eighteen healthy controls participated in this study. Because the mirror neuron system (MNS) is thought to be involved in theory of mind, we first implemented a straightforward action-execution and observation task to assess basic MNS function. Second, we examined the social-cognitive ability to understand actions of others, which is a component of ToM. We used fMRI to assess BOLD activity differences between groups during both experiments. Theory of mind was also measured behaviorally using the Reading the Mind in the Eyes test (RME). ALS patients displayed greater BOLD activity during the action-execution and observation task, especially throughout right anterior cortical regions. These areas included the right inferior operculum, premotor and primary motor regions, and left inferior parietal lobe. A conjunction analysis showed significantly more co-activated voxels during both the observation and action-execution conditions in the patient group throughout MNS regions. These results support a compensatory response in the MNS during action processing. In the action understanding experiment, healthy controls performed better behaviorally and subsequently recruited greater regions of activity throughout the prefrontal cortex and middle temporal gyrus. Lastly, action understanding performance was able to cluster patients with ALS into high and lower performing groups, which then differentiated RME performance. Collectively, these data suggest that social cognition, particularly theory of mind, may be affected in a subset of patients with ALS. This impairment may be related to functioning of the MNS and other regions related to action processing and understanding. Implications for future research are discussed.     

Motor simulation without motor expertise: enhanced corticospinal excitability in visually experienced dance spectators

The human "mirror-system" is suggested to play a crucial role in action observation and execution, and is characterized by activity in the premotor and parietal cortices during the passive observation of movements. The previous motor experience of the observer has been shown to enhance the activity in this network. Yet visual experience could also have a determinant influence when watching more complex actions, as in dance performances. Here we tested the impact visual experience has on motor simulation when watching dance, by measuring changes in corticospinal excitability. We also tested the effects of empathic abilities. To fully match the participants' long-term visual experience with the present experimental setting, we used three live solo dance performances: ballet, Indian dance, and non-dance. Participants were either frequent dance spectators of ballet or Indian dance, or "novices" who never watched dance. None of the spectators had been physically trained in these dance styles. Transcranial magnetic stimulation was used to measure corticospinal excitability by means of motor-evoked potentials (MEPs) in both the hand and the arm, because the hand is specifically used in Indian dance and the arm is frequently engaged in ballet dance movements. We observed that frequent ballet spectators showed larger MEP amplitudes in the arm muscles when watching ballet compared to when they watched other performances. We also found that the higher Indian dance spectators scored on the fantasy subscale of the Interpersonal Reactivity Index, the larger their MEPs were in the arms when watching Indian dance. Our results show that even without physical training, corticospinal excitability can be enhanced as a function of either visual experience or the tendency to imaginatively transpose oneself into fictional characters. We suggest that spectators covertly simulate the movements for which they have acquired visual experience, and that empathic abilities heighten motor resonance during dance observation.