Watching others' actions: mirror representations in the parietal cortex.

An observation that neurons in the motor cortex of the monkey are active both when the monkey performs a specific action and when he watches an actor executing the same action led to the mirror-system hypothesis. This hypothesis suggests that primates perceive and interpret others' actions by generating an internal motor representation (e.g., simulation). Recent evidence suggests that humans have a similar mirror system. In this review, we focus on the essential congruence between the motor and visual properties of an action. We summarize behavioral and imaging studies in humans that show that observing others' actions can interfere with our own motor execution. We discuss a framework for understanding such an internal representation and suggest that the activity in the parietal cortex during observation of others' actions is based on the sensory-to-motor remapping properties of this region, which are necessary for fine control of our own actions.     

Electrophysiology of action representation.

We continuously act on objects, on other individuals, and on ourselves, and actions represent the only way we have to manifest our own desires and goals. In the last two decades, electrophysiological experiments have demonstrated that actions are stored in the brain according to a goal-related organization. The authors review a series of experimental data showing that this "vocabulary of motor schemata" could also be used for non-strictly motor purposes. In the first section, they present data from monkey experiments describing the functional properties of inferior premotor cortex and, in more detail, the properties of visuomotor neurons responding to objects and others' actions observation (mirror neurons). In the second section, human data are reviewed, with particular regard to electrophysiological experiments aiming to investigate how action representations are stored and addressed. The specific facilitatory effect of motor imagery, action/object observation, and speech listening on motor excitability shown by these experiments provides strong evidence that the motor system is constantly involved whenever the idea of an action is evoked.     

One's motor performance predictably modulates the understanding of others' actions through adaptation of premotor visuo-motor neurons

Neurons firing both during self and other's motor behavior (mirror neurons) have been described in the brain of vertebrates including humans. The activation of somatic motor programs driven by perceived behavior has been taken as evidence for mirror neurons' contribution to cognition. The inverse relation, that is the influence of motor behavior on perception, is needed for demonstrating the long-hypothesized causal role of mirror neurons in action understanding. We provide here conclusive behavioral and neurophysiological evidence for that causal role by means of cross-modal adaptation coupled with a novel transcranial magnetic stimulation (TMS)-adaptation paradigm. Blindfolded repeated motor performance of an object-directed action (push or pull) induced in healthy participants a strong visual after-effect when categorizing others' actions, as a result of motor-to-visual adaptation of visuo-motor neurons. TMS over the ventral premotor cortex, but not over the primary motor cortex, suppressed the after-effect, thus localizing the population of adapted visuo-motor neurons in the premotor cortex. These data are exquisitely consistent in humans with the existence of premotor mirror neurons that have access to the action meaning. We also show that controlled manipulation of the firing properties of this neural population produces strong predictable changes in the way we categorize others' actions.     

Familiarity modulates mirror neuron and mentalizing regions during intention understanding

Recent research suggests that the inference of others' intentions from their observed actions is supported by two neural systems that perform complementary roles. The human putative mirror neuron system (pMNS) is thought to support automatic motor simulations of observed actions, with increased activity for previously experienced actions, whereas the mentalizing system provides reflective, non-intuitive reasoning of others' perspectives, particularly in the absence of prior experience. In the current fMRI study, we show how motor familiarity with an action and perceptual familiarity with the race of an actor uniquely modulate these two systems. Chinese participants were asked to infer the intentions of actors performing symbolic gestures, an important form of non-verbal communication that has been shown to activate both mentalizing and mirror neuron regions. Stimuli were manipulated along two dimensions: (1) actor's race (Caucasian vs. Chinese actors) and (2) participants' level of experience with the gestures (familiar or unfamiliar). We found that observing all gestures compared to observing still images was associated with increased activity in key regions of both the pMNS and mentalizing systems. In addition, observations of one's same race generated greater activity in the posterior pMNS-related regions and the insula than observations of a different race. Surprisingly, however, familiar gestures more strongly activated regions associated with mentalizing, while unfamiliar gestures more strongly activated the posterior region of the pMNS, a finding that is contrary to prior literature and demonstrates the powerful modulatory effects of both motor and perceptual familiarity on pMNS and mentalizing regions when asked to infer the intentions of intransitive gestures.     

EEG evidence for mirror neuron dysfunction in autism spectrum disorders

Autism spectrum disorders (ASD) are largely characterized by deficits in imitation, pragmatic language, theory of mind, and empathy. Previous research has suggested that a dysfunctional mirror neuron system may explain the pathology observed in ASD. Because EEG oscillations in the mu frequency (8-13 Hz) over sensorimotor cortex are thought to reflect mirror neuron activity, one method for testing the integrity of this system is to measure mu responsiveness to actual and observed movement. It has been established that mu power is reduced (mu suppression) in typically developing individuals both when they perform actions and when they observe others performing actions, reflecting an observation/execution system which may play a critical role in the ability to understand and imitate others' behaviors. This study investigated whether individuals with ASD show a dysfunction in this system, given their behavioral impairments in understanding and responding appropriately to others' behaviors. Mu wave suppression was measured in ten high-functioning individuals with ASD and ten age- and gender-matched control subjects while watching videos of (1) a moving hand, (2) a bouncing ball, and (3) visual noise, or (4) moving their own hand. Control subjects showed significant mu suppression to both self and observed hand movement. The ASD group showed significant mu suppression to self-performed hand movements but not to observed hand movements. These results support the hypothesis of a dysfunctional mirror neuron system in high-functioning individuals with ASD.     

Is it really my turn? An event-related fMRI study of task sharing

Acting together with others is a fundamental human ability. This raises the possibility that we take others' actions into account whenever somebody acts around us. Event-related fMRI was used to identify brain regions responsive to changes in cognitive processing when one and the same go-nogo task is performed alone or together with a co-actor performing a complementary task. Reaction times showed that participants integrated the potential action of their co-actor in their own action planning. Increased activation in ventral premotor cortex was found when participants acted upon stimuli referring to their own action alternative, but only when their partner performed a complementary task. This suggests that knowing about the potential actions of a partner increases the relevance of stimuli referring to oneself. Acting in the presence of a co-actor was also associated with increased orbitofrontal activation, indicating that participants monitored their performance more closely to make sure it really was their turn. These results suggest that our default mode is to interact with others.     

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.     

Viewpoint (in)dependence of action representations: an MVPA study

The discovery of mirror neurons-neurons that code specific actions both when executed and observed-in area F5 of the macaque provides a potential neural mechanism underlying action understanding. To date, neuroimaging evidence for similar coding of specific actions across the visual and motor modalities in human ventral premotor cortex (PMv)-the putative homologue of macaque F5-is limited to the case of actions observed from a first-person perspective. However, it is the third-person perspective that figures centrally in our understanding of the actions and intentions of others. To address this gap in the literature, we scanned participants with fMRI while they viewed two actions from either a first- or third-person perspective during some trials and executed the same actions during other trials. Using multivoxel pattern analysis, we found action-specific cross-modal visual-motor representations in PMv for the first-person but not for the third-person perspective. Additional analyses showed no evidence for spatial or attentional differences across the two perspective conditions. In contrast, more posterior areas in the parietal and occipitotemporal cortex did show cross-modal coding regardless of perspective. These findings point to a stronger role for these latter regions, relative to PMv, in supporting the understanding of others' actions with reference to one's own actions.     

Through the looking glass: counter-mirror activation following incompatible sensorimotor learning

The mirror system, comprising cortical areas that allow the actions of others to be represented in the observer's own motor system, is thought to be crucial for the development of social cognition in humans. Despite the importance of the human mirror system, little is known about its origins. We investigated the role of sensorimotor experience in the development of the mirror system. Functional magnetic resonance imaging was used to measure neural responses to observed hand and foot actions following one of two types of training. During training, participants in the Compatible (control) group made mirror responses to observed actions (hand responses were made to hand stimuli and foot responses to foot stimuli), whereas the Incompatible group made counter-mirror responses (hand to foot and foot to hand). Comparison of these groups revealed that, after training to respond in a counter-mirror fashion, the relative action observation properties of the mirror system were reversed; areas that showed greater responses to observation of hand actions in the Compatible group responded more strongly to observation of foot actions in the Incompatible group. These results suggest that, rather than being innate or the product of unimodal visual or motor experience, the mirror properties of the mirror system are acquired through sensorimotor learning.     

Reflecting on the mirror neuron system in autism: A systematic review of current theories

There is much interest in the claim that dysfunction of the mirror neuron system in individuals with autism spectrum condition causes difficulties in social interaction and communication. This paper systematically reviews all published studies using neuroscience methods (EEG/MEG/TMS/eyetracking/EMG/fMRI) to examine the integrity of the mirror system in autism. 25 suitable papers are reviewed. The review shows that current data are very mixed and that studies using weakly localised measures of the integrity of the mirror system are hard to interpret. The only well localised measure of mirror system function is fMRI. In fMRI studies, those using emotional stimuli have reported group differences, but studies using non-emotional hand action stimuli do not. Overall, there is little evidence for a global dysfunction of the mirror system in autism. Current data can be better understood under an alternative model in which social top-down response modulation is abnormal in autism. The implications of this model and future research directions are discussed.     

Modulation of cortical motor outputs by the symbolic meaning of visual stimuli

The observation of an action modulates motor cortical outputs in specific ways, in part through mediation of the mirror neuron system. Sometimes we infer a meaning to an observed action based on integration of the actual percept with memories. Here, we conducted a series of experiments in healthy adults to investigate whether such inferred meanings can also modulate motor cortical outputs in specific ways. We show that brief observation of a neutral stimulus mimicking a hand does not significantly modulate motor cortical excitability (Study 1) although, after prolonged exposure, it can lead to a relatively nonspecific modulation (Study 2). However, when such a neutral stimulus is preceded by exposure to a hand stimulus, the latter appears to serve as a prime, perhaps enabling meaning to the neutral stimulus, which then modulates motor cortical excitability in accordance with mirror neuron‐driving properties (Studies 2 and 3). Overall results suggest that a symbolic value ascribed to an otherwise neutral stimulus can modulate motor cortical outputs, revealing the influence of top‐down inputs on the mirror neuron system. These findings indicate a novel aspect of the human mirror neuron system: an otherwise neutral stimulus can acquire specific mirror neuron‐driving properties in the absence of a direct association between motor practice and perception. This significant malleability in the way that the mirror neuron system can code otherwise meaningless (i.e. arbitrarily associated) stimuli may contribute to coding communicative signals such as language. This may represent a mirror neuron system feature that is unique to humans.     

Functions of the mirror neuron system: implications for neurorehabilitation.

Mirror neurons discharge during the execution of hand object-directed actions and during the observation of the same actions performed by other individuals. These neurons were first identified in the ventral premotor cortex (area F5) and later on in the inferior parietal lobule of monkey brain, thus constituting the mirror neuron system. More recently, mirror neurons for mouth object-directed actions have also been found in the monkey. Several pieces of experimental data demonstrate that a mirror neuron system devoted to hand, mouth, and foot actions is also present in humans. In the present paper we review the experimental evidence on the role of the mirror neuron system in action understanding, imitation learning of novel complex actions, and internal rehearsal (motor imagery) of actions. On the basis of features of the mirror neuron system and its role in action understanding and imitation, we discuss the possible use of action observation and imitation as an approach for systematic training in the rehabilitation of patients with motor impairment of the upper limb after stroke.     

Your goal is mine: unraveling mimetic desires in the human brain

The spread of desires among individuals is widely believed to shape motivational drives in human populations. However, objective evidence for this phenomenon and insights into the underlying brain mechanisms are still lacking. Here we show that participants rated objects as more desirable once perceived as the goals of another agent's action. We then unravel the mechanisms underpinning such goal contagion, using functional neuroimaging. As expected, observing goal-directed actions activated a parietofrontal network known as the mirror neuron system (MNS), whereas subjective desirability ratings were represented in a ventral striatoprefrontal network known as the brain valuation system (BVS). Crucially, the induction of mimetic desires through action observation involved the modulation of BVS activity through MNS activity. Furthermore, MNS-BVS effective connectivity predicted individual susceptibility toward mimetic desires. We therefore suggest that MNS-BVS interaction represents a fundamental mechanism explaining how nonverbal behavior propagates desires without the need for explicit, intentional communication.     

Interaction of sound and sight during action perception: Evidence for shared modality-dependent action representations

Seeing or hearing manual actions activates the mirror neuron system, i.e., specialized neurons within motor areas which fire not only when an action is performed but also when it is passively perceived. Although it has been shown that mirror neurons respond to either action-specific vision or sound, it remains a topic of debate whether and how vision and sound interact during action perception.Here we used transcranial magnetic stimulation to explore multimodal interactions in the human motor system, namely at the level of the primary motor cortex (M1). Corticomotor excitability in M1 was measured while subjects perceived unimodal visual (V), unimodal auditory (A), or multimodal (V + A) stimuli of a simple hand action. In addition, incongruent multimodal stimuli were included, in which incongruent vision or sound was presented simultaneously with the auditory or visual action stimulus. A selective response increase was observed to the congruent multimodal stimulus as compared to the unimodal and incongruent multimodal stimuli.These findings speak in favour of ‘shared’ action representations in the human motor system that are evoked in a ‘modality-dependent’ way, i.e., they are elicited most robustly by the simultaneous presentation of congruent auditory and visual stimuli. Multimodality in the perception of hand movements bears functional similarities to speech perception, suggesting that multimodal convergence is a generic feature of the mirror system which applies to action perception in general.     

Spatial bias in symbolic and non-symbolic numerical comparison in neglect

When asked to bisect mentally numerical intervals, neglect patients show a displacement of the numerical midpoint similar to the one observed in physical line bisection. This spatial-numerical bias has been taken as evidence of the spatial nature of numerical magnitude representations. However, to date, neuropsychological studies in neglect patients have only used symbolic numerical material. Here, we compare the results of patients with right-hemisphere damage with and without unilateral left neglect and age-matched healthy control participants in two numerical comparison tasks using symbolic and non-symbolic materials, in order to determine whether the representation of non-symbolic numerosities was altered or not by the presence of neglect. When asked to judge if an Arabic digit or a sequence of flashed dots was smaller or larger than a reference value (i.e., 5), the responses of neglect patients to smaller magnitudes (i.e., 4) were impaired. Moreover, only neglect patients presented an asymmetrical distance effect (i.e., an enhanced effect only for stimuli of smaller numerical magnitude than the reference). These results provide the first direct evidence of a spatial bias in non-symbolic numerosity in neglect patients, and support the existence of common processing mechanisms and/or a representational system for symbolic and non-symbolic inputs.     

Enhanced activation in the extrastriate body area by goal-directed actions

Aim:  Neuroimaging studies on biological motion have established the view that the posterior superior temporal sulcus (pSTS) is involved in detecting intention of others. Those studies have consistently reported other regions such as body-selective extrastriate body area (EBA) and motion-sensitive middle temporal, in close proximity to pSTS. Whether EBA responds only to static body parts or has a more extended role as part of a system for inferring intention of others has remained an elusive issue. The aim of the present study was to investigate the role of EBA in processing goal-directed actions.
Methods:  Twelve healthy volunteers participated in the present study. Using sports-related motions as visual stimuli, brain activations were examined during observation of goal-directed actions and non-goal-directed actions on functional magnetic resonance imaging.
Results:  Compared to non-goal-directed actions, goal-directed actions produced greater activations in EBA along with the mirror neuron system.
Conclusions:  EBA might contribute to understanding others' actions by representing the dynamic aspects of human motions.     

Action co-representation is tuned to other humans

The present study attempts to explore the process by which knowledge of another's intentional behavior in a joint-action scenario is represented through the action observation and execution network-also known as the common coding system. Participants (n = 18) were instructed to perform the complementary social Simon task under the implemented belief of interaction with either an unseen human (biological agent) or a computer program, where in fact, all response sequences from either "partner" were generated by computer. Results provide behavioral and neurophysiological evidence (P3 and S-LRP) that the believed intentionality of another person's actions is sufficient to facilitate a strong-enough agency-dependent social Simon effect to modulate action planning and anticipation. We suggest that the co-representation of human action may be an evolved biologically tuned default of the human motor system.     

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.     

Perception of dynamic action in patients with schizophrenia

Neuropsychological studies have revealed that schizophrenic (SZ) patients have severe impairments in the cognitive integration of static and moving perceptual stimuli. Research on knowledge structures has shown that sequences of continuous actions are represented in memory as clusters of goal-directed events in a hierarchical manner. In the present study, we investigated the ability to segment familiar sequences of dynamic goal-directed actions into small and large meaningful units in a group of patients with schizophrenia (N = 16) and a group of healthy control subjects (N = 17). While viewing two videotaped movies, participants were requested to detect the transitions between component events at both low and high levels of the action categorical structure. Both groups detected significantly more events under the small-oriented condition as compared to the large-oriented condition. Differently from normal controls, patients recalled the event scenes in a detailed and fragmentary manner and showed considerable difficulties in detecting large action units. Moreover, low performance on action boundary detection significantly correlated with higher levels of disorganisation symptoms in patients with schizophrenia. A defective conceptual organisation of perceptive action knowledge would help to explain the severe everyday difficulties of these patients both in monitoring their own actions and in understanding others' intentions.