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.     

What is simulated in the action observation network when we observe actions?

In the last decade there has been a great amount of research investigating the role of simulation in our ability to infer the underlying intentions of any observed action. The majority of studies have focussed on the role of mirror neurons and the network of cortical areas active during action observation (AON) in inferring the goal of an observed action. However, it remains unclear what precisely is simulated when we observe an action and how such simulations can enable the observer to infer the underlying intention of that action. In particular it is not known how simulation in the AON enables the inference of the same goal when the kinematics observed to achieve that goal differ, such as when reaching to grasp an object with the left or right hands. Here we performed a behavioural study with healthy human subjects to address this question. We show that the subjects were able to detect very subtle changes in the kinematics of an observed action. In addition, we fitted the behavioural responses with a model based on the predictive coding account of mirror neurons. This is a Bayesian account of action observation that can be explained by the free-energy principle. Here we show that we can model all the effects observed when the action observation system is considered within a predictive coding framework.     

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.     

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.     

Timecourse of mirror and counter-mirror effects measured with transcranial magnetic stimulation

The human mirror system has been the subject of much research over the past two decades, but little is known about the timecourse of mirror responses. In addition, it is unclear whether mirror and counter-mirror effects follow the same timecourse. We used single-pulse transcranial magnetic stimulation to investigate the timecourse of mirror and counter-mirror responses in the human brain. Experiment 1 demonstrated that mirror responses can be measured from around 200 ms after observed action onset. Experiment 2 demonstrated significant effects of counter-mirror sensorimotor training at all timepoints at which a mirror response was found in Experiment 1 (i.e. from 200 ms onward), indicating that mirror and counter-mirror responses follow the same timecourse. By suggesting similarly direct routes for mirror and counter-mirror responses, these results support the associative account of mirror neuron origins whereby mirror responses arise as a result of correlated sensorimotor experience during development. More generally, they contribute to theorizing regarding mirror neuron function by providing some constraints on how quickly mirror responses can influence social cognition.     

Mirror neurons and the social nature of language: the neural exploitation hypothesis

This paper discusses the relevance of the discovery of mirror neurons in monkeys and of the mirror neuron system in humans to a neuroscientific account of primates' social cognition and its evolution. It is proposed that mirror neurons and the functional mechanism they underpin, embodied simulation, can ground within a unitary neurophysiological explanatory framework important aspects of human social cognition. In particular, the main focus is on language, here conceived according to a neurophenomenological perspective, grounding meaning on the social experience of action. A neurophysiological hypothesis--the "neural exploitation hypothesis"--is introduced to explain how key aspects of human social cognition are underpinned by brain mechanisms originally evolved for sensorimotor integration. It is proposed that these mechanisms were later on adapted as new neurofunctional architecture for thought and language, while retaining their original functions as well. By neural exploitation, social cognition and language can be linked to the experiential domain of action.     

Sign language processing and the mirror neuron system

In this paper we review evidence for frontal and parietal lobe involvement in sign language comprehension and production, and evaluate the extent to which these data can be interpreted within the context of a mirror neuron system for human action observation and execution. We present data from three literatures--aphasia, cortical stimulation, and functional neuroimaging. Generally, we find support for the idea that sign language comprehension and production can be viewed in the context of a broadly-construed frontal-parietal human action observation/execution system. However, sign language data cannot be fully accounted for under a strict interpretation of the mirror neuron system. Additionally, we raise a number of issues concerning the lack of specificity in current accounts of the human action observation/execution system.     

The human mirror system: a motor resonance theory of mind-reading

Electrophysiological data confirm the existence of neurons that respond to both motor and sensory events in the macaque brain. These mirror neurons respond to execution and observation of goal-orientated actions. It has been suggested that they comprise a neural basis for encoding an internal representation of action. In this paper the evidence for a parallel system in humans is reviewed and the implications for human theory of mind processing are discussed. Different components of theory of mind are discussed; the evidence for mirror activity within subtypes is addressed. While there is substantial evidence for a human mirror system, there are weaknesses in the attempts to localize such a system in the brain. Preliminary evidence indicates that mirror neurons may be involved in theory of mind; however, these data by their very nature are reliant on the presence, and precise characterization, of the human mirror system.     

Mirror neurons and imitation: a computationally guided review.

Neurophysiology reveals the properties of individual mirror neurons in the macaque while brain imaging reveals the presence of 'mirror systems' (not individual neurons) in the human. Current conceptual models attribute high level functions such as action understanding, imitation, and language to mirror neurons. However, only the first of these three functions is well-developed in monkeys. We thus distinguish current opinions (conceptual models) on mirror neuron function from more detailed computational models. We assess the strengths and weaknesses of current computational models in addressing the data and speculations on mirror neurons (macaque) and mirror systems (human). In particular, our mirror neuron system (MNS), mental state inference (MSI) and modular selection and identification for control (MOSAIC) models are analyzed in more detail. Conceptual models often overlook the computational requirements for posited functions, while too many computational models adopt the erroneous hypothesis that mirror neurons are interchangeable with imitation ability. Our meta-analysis underlines the gap between conceptual and computational models and points out the research effort required from both sides to reduce this gap.     

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.     

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.     

Action co-representation: the joint SNARC effect

Traditionally, communication has been defined as the intentional exchange of symbolic information between individuals. In contrast, the mirror system provides a basis for nonsymbolic and nonintentional information exchange between individuals. We believe that understanding the role of the mirror system in joint action has the potential to serve as a bridge between these two domains. The present study investigates one crucial component of joint action: the ability to represent others' potential actions in the same way as one's own in the absence of perceptual evidence. In two experiments a joint spatial numerical association of response codes (SNARC) effect is demonstrated, providing further evidence that individuals form functionally equivalent representations of their own and others' potential actions. It is shown that numerical (symbolic) stimuli that are mapped onto a spatially arranged internal representation (a mental number line) can activate a co-represented action in the same way as spatial stimuli. This generalizes previous results on co-representation.We discuss the role of the mirror system in co-representation as a basis for shared intentionality and communication.     

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.     

More than an imitation game: Top-down modulation of the human mirror system

All interpersonal interactions are underpinned by action: perceiving and understanding the actions of others, and responding by planning and performing self-made actions. Perception of action, both self-made and observed, informs ongoing motor responses by iterative feedback within a perception-action loop. This fundamental phenomenon occurs within single-cells of the macaque brain which demonstrate sensory and motor response properties. These ‘mirror’ neurons have led to a swathe of research leading to the broadly accepted idea of a human mirror system. The current review examines the putative human mirror system literature to highlight several inconsistencies in comparison to the seminal macaque data, and ongoing controversies within human focused research (including mirror neuron origin and function). In particular, we will address the often-neglected other side to the ‘mirror’: complementary and opposing actions. We propose that engagement of the mirror system in meeting changing task-demands is dynamically modulated via frontal control networks.     

Linking differences in action perception with differences in action execution

Successful human social interactions depend upon the transmission of verbal and non-verbal signals from one individual to another. Non-verbal social communication is realized through our ability to read and understand information present in other people’s actions. It has been proposed that employing the same motor programs, we use to execute an action when observing the same action underlies this action understanding. The main prediction of this framework is that action perception should be strongly correlated with parameters of action execution. Here, we demonstrate that subjects’ sensitivity to observed movement speeds is dependent upon how quickly they themselves executed the observed action. This result is consistent with the motor theory of social cognition and suggests that failures in non-verbal social interactions between individuals may in part result from differences in how those individuals move.     

Modeling the Development of Goal-Specificity in Mirror Neurons

Neurophysiological studies have shown that parietal mirror neurons encode not only actions but also the goal of these actions. Although some mirror neurons will fire whenever a certain action is perceived (goal-independently), most will only fire if the motion is perceived as part of an action with a specific goal. This result is important for the action-understanding hypothesis as it provides a potential neurological basis for such a cognitive ability. It is also relevant for the design of artificial cognitive systems, in particular robotic systems that rely on computational models of the mirror system in their interaction with other agents. Yet, to date, no computational model has explicitly addressed the mechanisms that give rise to both goal-specific and goal-independent parietal mirror neurons. In the present paper, we present a computational model based on a self-organizing map, which receives artificial inputs representing information about both the observed or executed actions and the context in which they were executed. We show that the map develops a biologically plausible organization in which goal-specific mirror neurons emerge. We further show that the fundamental cause for both the appearance and the number of goal-specific neurons can be found in geometric relationships between the different inputs to the map. The results are important to the action-understanding hypothesis as they provide a mechanism for the emergence of goal-specific parietal mirror neurons and lead to a number of predictions: (1) Learning of new goals may mostly reassign existing goal-specific neurons rather than recruit new ones; (2) input differences between executed and observed actions can explain observed corresponding differences in the number of goal-specific neurons; and (3) the percentage of goal-specific neurons may differ between motion primitives.     

"She" is not like "I": the tie between language and action is in our imagination

Embodied theories hold that understanding what another person is doing requires the observer to map that action directly onto his or her own motor representation and simulate it internally. The human motor system may, thus, be endowed with a "mirror matching" device through which the same motor representation is activated, when the subject is either the performer or the observer of another's action ("self-other shared representation"). It is suggested that understanding action verbs relies upon the same mechanism; this implies that motor responses to these words are automatic and independent of the subject of the verb. In the current study, participants were requested to read silently and decide on the syntactic subject of action and nonaction verbs, presented in first (1P) or third (3P) person, while TMS was applied to the left hand primary motor cortex (M1). TMS-induced motor-evoked potentials were recorded from hand muscles as a measure of cortico-spinal excitability. Motor-evoked potentials increased for 1P, but not for 3P, action verbs or 1P and 3P nonaction verbs. We provide novel demonstration that the motor simulation is triggered only when the conceptual representation of a word integrates the action with the self as the agent of that action. This questions the core principle of "mirror matching" and opens to alternative interpretations of the relationship between conceptual and sensorimotor processes.     

μ-suppression during action observation and execution correlates with BOLD in dorsal premotor, inferior parietal, and SI cortices

The discovery of mirror neurons in the monkey, that fire during both the execution and the observation of the same action, sparked great interest in studying the human equivalent. For over a decade, both functional magnetic resonance imaging (fMRI) and electroencephalography (EEG) have been used to quantify activity in the human mirror neuron system (MNS)-yet, little is still known about how fMRI and EEG measures of the MNS relate to each other. To test the frequent assumption that regions of the MNS as evidenced by fMRI are the origin of the suppression of the EEG μ-rhythm during both action execution and observation, we recorded EEG and BOLD-fMRI signals simultaneously while participants observed and executed actions. We found that the suppression of the μ-rhythm in EEG covaried with BOLD activity in typical MNS regions, inferior parietal lobe (IPL), dorsal premotor (dPM) and primary somatosensory cortex (BA2), during both action observation and execution. In contrast, in BA44, only nonoverlapping voxels correlated with μ-suppression during observation and execution. These findings provide direct support for the notion that μ-suppression is a valid indicator of MNS activity in BA2, IPL, and dPM, but argues against the idea that mirror neurons in BA44 are the prime source of μ-suppression. These results shed light on the neural basis of μ-suppression and provide a basis for integrating more closely the flourishing but often separate literatures on the MNS using fMRI and EEG.