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.     

The infant mirror neuron system studied with high density EEG

The mirror neuron system has been suggested to play a role in many social capabilities such as action understanding, imitation, language and empathy. These are all capabilities that develop during infancy and childhood, but the human mirror neuron system has been poorly studied using neurophysiological measures. This study measured the brain activity of 6-month-old infants and adults using a high-density EEG net with the aim of identifying mirror neuron activity. The subjects viewed both goal-directed movements and non-goal-directed movements. An independent component analysis was used to extract the sources of cognitive processes. The desynchronization of the mu rhythm in adults has been shown to be a marker for activation of the mirror neuron system and was used as a criterion to categorize independent components between subjects. The results showed significant mu desynchronization in the adult group and significantly higher ERP activation in both adults and 6-month-olds for the goal-directed action observation condition. This study demonstrate that infants as young as 6 months display mirror neuron activity and is the first to present a direct ERP measure of the mirror neuron system in infants.     

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.     

Weak imitative performance is not due to a functional 'mirroring' deficit in adults with Autism Spectrum Disorders

A large number of studies have demonstrated impaired performance on a range of imitation tasks among individuals with Autism Spectrum Disorders (ASD). The theory which suggests that these impairments are caused by a mirror system deficit has become increasingly prominent. Under this view, the capacity to match observed with executed actions or to 'mirror' is impaired in individuals with ASD. This study investigated the extent to which any impaired performance on imitation tasks is due to a functional mirroring deficit by comparing the performance of adults with ASD on imitative and non-imitative versions of the 'pen-and-cups' task. Participants in this task are required to observe transitive actions and to imitate them as fast as possible. Experiment 1 revealed impaired performance by high functioning adults with ASD on the imitative version of the task compared to IQ matched controls. The same participants then completed two non-imitative versions of the task in Experiment 2. The 'geometric' version of the task required participants to perform actions specified by the movement of abstract geometric shapes. The 'verbal' version of the task required participants to describe the observed actions. Adults with ASD were as impaired on each non-imitative version of the task as they were on the imitative version, suggesting that the impaired performance on the imitation task was not due to a functional mirroring deficit. Instead, more general factors contributed to the poor performance on this task. These findings add to the weight of evidence suggesting that impairments in imitation skills should not be cited as evidence consistent with a 'mirror system deficit theory' of ASD.     

Goal-Directed and Goal-Less Imitation in Autism Spectrum Disorder

To investigate how people with Autism are affected by the presence of goals during imitation, we conducted a study to measure movement kinematics and eye movements during the imitation of goal-directed and goal-less hand movements. Our results showed that a control group imitated changes in movement kinematics and increased the level that they tracked the hand with their eyes, in the goal-less compared to goal-direction condition. In contrast, the ASD group exhibited more goal-directed eye movements, and failed to modulate the observed movement kinematics successfully in either condition. These results increase the evidence for impaired goal-less imitation in ASD, and suggest that there is a reliance on goal-directed strategies for imitation in ASD, even in the absence of visual goals.     

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.     

The role of selective attention in matching observed and executed actions

Substantial evidence suggests that observed actions can engage their corresponding motor representations within the observer. It is currently believed that this process of observation-execution matching occurs relatively automatically, without the need for top-down control. In this study we tested the susceptibility of the observation-execution matching process to selective attention. We used a Go/NoGo paradigm to investigate the phenomenon of ‘automatic imitation’, in which participants are faster to initiate a hand movement that is congruent with a concurrently observed action, relative to one that is incongruent. First, we replicated previous findings of automatic imitation, and excluded the possibility that spatial compatibility effects might explain these results (Experiment 1). We then presented participants with the same goal-directed actions while directing their attention to an imperative stimulus that spatially overlapped, but was distinct from, the observed actions (Experiment 2). Crucially, automatic imitation no longer occurred when participants directed their attention away from the displayed actions and towards the spatially overlapping stimulus. In a final experiment, we examined whether the automatic imitation of grasp persists when participants attend to an irrelevant feature of the observed action, such as whether it is performed by a left or right hand (Experiment 3). Here we found that automatic imitation is contingent on participants attending to the feature of the observed hand that was relevant to their responses. Together these findings demonstrate the importance of selective mechanisms in the filtering of task-irrelevant actions, and indicate a role for top-down control in limiting the motoric simulation of observed actions.     

The role of motor contagion in the prediction of action

It has been proposed that actions are intrinsically linked to perception. The idea behind these theories is that observing, imagining or in any way representing an action excites the motor programs used to execute that same action. There is neurophysiological evidence that neurons in premotor cortex of monkeys respond both during movement execution and during the observation of goal-directed action ('mirror neurons'). In humans, a proportion of the brain regions involved in executing actions are activated by the mere observation of action (the 'mirror system'). In this paper, we briefly review recent empirical studies of the mirror system, and discuss studies demonstrating interference effects between observed and executed movements. This interference, which might be a form of 'motor contagion', seems to arise specifically from the observation of biological movements, whether or not these movements are goal-directed. We suggest that this crude motor contagion is the first step in a more sophisticated predictive system that allows us to infer goals from the observation of actions.     

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.     

Is the human primary motor cortex activated by muscular or direction-dependent features of observed movements?

Previous Transcranial Magnetic Stimulation (TMS) studies have shown that the observer's motor system is facilitated by the sole observation of motor actions. However, it has not been possible so far to decide whether the observer's motor system resonates primarily with the observed movement direction or the observed muscle activity, as both factors usually co-varied in these action observation studies. Here, we applied TMS to the wrist extensor and flexor during the observation of wrist motions such that the posture of the observer and the model in the video were either congruent or incongruent. Due to this manipulation, it was possible to disentangle whether the observer's primary motor cortex (M1) is facilitated in accordance to either the observed movement direction or the observed muscle activation. Findings revealed that M1 resonated predominantly according to muscle-specific rather than direction-specific parameters of observed movements. More specifically, muscle-specific facilitation was maximal during congruent postures and remained evident, even though to a lower extent, during incongruent postures in which muscle activation and movement direction parameters were discordant. Our findings support the hypothesis that M1 contributes to action observation, by representing the observed movement in intrinsic, muscle-related coordinates. This transformation from extrinsic to intrinsic coordinates might be an important prerequisite for action understanding and imitation. Additionally, our data offer a neurophysiological explanation for interference that emerges when an action is performed while an incongruent action is observed.     

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.     

Interference effect of observed human movement on action is due to velocity profile of biological motion

It has previously been shown that observing an action made by a human, but not by a robot, interferes with executed actions (Kilner, Paulignan, & Blakemore, 2003). Here, we investigated what aspect of human movement causes this interference effect. Subjects made arm movements while observing a video of either a human making an arm movement or a ball moving across the screen. Both human and ball videos contained either biological (minimum jerk) or non-biological (constant velocity) movements. The executed and observed arm movements were either congruent (same direction) or incongruent (tangential direction) with each other. The results showed that observed movements are processed differently according to whether they are made by a human or a ball. For the ball videos, both biological and non-biological incongruent movements interfered with executed arm movements. In contrast, for the human videos, the velocity profile of the movement was the critical factor: only incongruent, biological human movements interfered with executed arm movements. We propose that the interference effect could be due either to the information the brain has about different types of movement stimuli or to the impact of prior experience with different types of form and motion.     

The human mirror neuron system in a population with deficient self-awareness: an fMRI study in alexithymia

The mirror neuron system (MNS) is considered crucial for human imitation and language learning and provides the basis for the development of empathy and mentalizing. Alexithymia (ALEX), which refers to deficiencies in the self-awareness of emotional states, has been reported to be associated with poor ability in various aspects of social cognition such as mentalizing, cognitive empathy, and perspective-taking. Using functional magnetic resonance imaging (fMRI), we measured the hemodynamic signal to examine whether there are functional differences in the MNS activity between participants with ALEX (n = 16) and without ALEX (n = 13), in response to a classic MNS task (i.e., the observation of video clips depicting goal-directed hand movements). Both groups showed increased neural activity in the premotor and the parietal cortices during observation of hand actions. However, activation was greater for the ALEX group than the non-ALEX group. Furthermore, activation in the left premotor area was negatively correlated with perspective-taking ability as assessed with the interpersonal reactivity index. The signal in parietal cortices was negatively correlated with cognitive facets assessed by the stress coping inventory and positively correlated with the neuroticism scale from the NEO five factor personality scale. In addition, in the ALEX group, activation in the right superior parietal region showed a positive correlation with the severity of ALEX as measured by a structured interview. These results suggest that the stronger MNS-related neural response in individuals scoring high on ALEX is associated with their insufficient self-other differentiation.     

Cortical and subcortical mechanisms at the core of imitation

Imitation is thought to require a perception-action matching process that utilizes the "mirror neuron" system, but other cognitive functions such as error detection may also be required for even simple imitation. We sought to explore the core neural substrate of imitation by examining the imitation of simple finger actions using fMRI. Participants observed one of two actions and were instructed to imitate the action they observed, or to perform the alternative non-matching action. The contrast between imitation and non-matching actions was associated with activation in areas previously associated with imitation and "mirror neuron" functioning, including insula, intraparietal sulcus, dorsal premotor cortex, and superior temporal gyrus. Imitation was also specifically associated with activity in areas of prefrontal cortex, lateral orbitofrontal cortex (OFC), amygdala, red nucleus, thalamus, hippocampus, and substantia nigra. We suggest that lateral OFC responds to action-perception mismatch and other clusters reflect working memory, motor planning, associative learning, and visuo-motor integration of goal-directed action. Although computational models have predicted integration of these functions to enable imitation, their specific brain bases have not previously been identified. Together they offer a potentially powerful means through which matching one's actions to those of others can lead to behavioral modification and development.     

Mirror neuron dysfunction in autism spectrum disorders

Autism spectrum disorders (ASDs) are developmental conditions characterized by deficits in social interaction, verbal and nonverbal communication and obsessive/stereotyped patterns of behaviour. Although there is no reliable neurophysiological marker associated with ASDs, dysfunction of the parieto-frontal mirror neuron system has been suggested as a disturbance linked to the disorder. Mirror neurons (MNs) are visuomotor neurons which discharge both when performing and observing a goal directed action. Research suggests MNs may have a role in imitation, empathy, theory of mind and language. Although the research base is small, evidence from functional MRI, transcranial magnetic stimulation, and an electroencephalographic component called the mu rhythm suggests MNs are dysfunctional in subjects with ASD. These deficits are more pronounced when ASD subjects complete tasks with social relevance, or that are emotional in nature. Promising research has identified that interventions targeting MN related functions such as imitation can improve social functioning in ASDs. Boosting the function of MNs may improve the prognosis of ASDs, and contribute to diagnostic clarity.     

Cortical and subcortical mechanisms at the core of imitation

Abstract

Imitation is thought to require a perception–action matching process that utilizes the “mirror neuron” system, but other cognitive functions such as error detection may also be required for even simple imitation. We sought to explore the core neural substrate of imitation by examining the imitation of simple finger actions using fMRI. Participants observed one of two actions and were instructed to imitate the action they observed, or to perform the alternative non-matching action. The contrast between imitation and non-matching actions was associated with activation in areas previously associated with imitation and “mirror neuron” functioning, including insula, intraparietal sulcus, dorsal premotor cortex, and superior temporal gyrus. Imitation was also specifically associated with activity in areas of prefrontal cortex, lateral orbitofrontal cortex (OFC), amygdala, red nucleus, thalamus, hippocampus, and substantia nigra. We suggest that lateral OFC responds to action–perception mismatch and other clusters reflect working memory, motor planning, associative learning, and visuo-motor integration of goal-directed action. Although computational models have predicted integration of these functions to enable imitation, their specific brain bases have not previously been identified. Together they offer a potentially powerful means through which matching one's actions to those of others can lead to behavioral modification and development.     

Neural mechanisms of imitation and 'mirror neuron' functioning in autistic spectrum disorder

An association between autistic spectrum disorder and imitative impairment might result from dysfunction in mirror neurons (MNs) that serve to relate observed actions to motor codings. To explore this hypothesis, we employed a functional magnetic resonance imaging (fMRI) protocol previously used to identify the neural substrate of imitation, and human MN function, to compare 16 adolescent males of normal intelligence with autistic spectrum disorder (ASD) and age, sex and IQ matched controls. In the control group, in accord with previous findings, we identified activity attributable to MNs in areas of the right parietal lobe. Activity in this area was less extensive in the ASD group and was absent during non-imitative action execution. Broca's area was minimally active during imitation in controls. Differential patterns of activity during imitation and action observation in ASD and controls were most evident in an area at the right temporo-parietal junction also associated with a 'theory of mind' (ToM) function. ASD participants also failed to show modulation of left amygdala activity during imitation that was evident in the controls. This may have implications for understanding the imitation of emotional stimuli in ASD. Overall, we suggest that ASD is associated with altered patterns of brain activity during imitation, which could stem from poor integration between areas serving visual, motor, proprioceptive and emotional functions. Such poor integration is likely to adversely affect the development of ToM through imitation as well as other aspects of social cognitive function in ASD.     

Action observation and imitation in autism spectrum disorders: an ALE meta-analysis of fMRI studies

Previous studies have shown that the mirror neuron system (MNS) plays an important role in action understanding. However, whether and how the MNS activity is different in individuals with autism spectrum disorders (ASD) and typically developed (TD) individuals are still unclear. The current study used activation likelihood estimation to conduct a meta-analysis of functional magnetic resonance imaging studies that investigated action observation and imitation in ASD and TD individuals. Thirteen studies were selected, and the contrasts focused on the brain effects in ASD and TD participants and the differences between the two groups. The results showed that compared with TD individuals, ASD individuals exhibited stronger effects in the anterior inferior parietal lobule, a part of the putative human MNS. In addition, the ASD group demonstrated altered effects in the occipital cortex, dorsolateral prefrontal cortex, cingulate cortex, and insula. These results suggest that ASD individuals demonstrate dysfunction of the MNS during action observation and imitation. Furthermore, brain regions involved in visual processing, executive function, and social cognitive function might also show dysfunction during action task performance.     

Neural mechanism of conflict control in a number interference task

The electrophysiological bases of conflict control in a number interference task was measured in 21 healthy study participants using event-related brain potentials (ERPs). In the number interference task, participants were instructed to ignore the number words meaning and to report the number of the number words. The number words were 'two', 'three', or 'four'. We focused on the differences between the incongruent condition (e.g. 'two' written four times) and the congruent condition (e.g. four written four times). Scalp ERP analysis revealed that the incongruent condition elicited a more negative ERP deflection (N350-470) than the congruent condition between 350 and 470 ms, and a more late positive deflection (LPC) than the congruent condition between 550 and 650 ms. N350-470 was a critical sign of conflict monitoring in the early phase, and LPC mirrored conflict resolution in the terminal stage. The results provided evidence for the dissociation between conflict monitoring and conflict resolution in the number interference task.