Mirror neuron system: basic findings and clinical applications

In primates, ventral premotor and rostral inferior parietal neurons fire during the execution of hand and mouth actions. Some cells (called mirror neurons) also fire when hand and mouth actions are just observed. Mirror neurons provide a simple neural mechanism for understanding the actions of others. In humans, posterior inferior frontal and rostral inferior parietal areas have mirror properties. These human areas are relevant to imitative learning and social behavior. Indeed, the socially isolating condition of autism is associated with a deficit in mirror neuron areas. Strategies inspired by mirror neuron research recently have been used in the treatment of autism and in motor rehabilitation after stroke.     

Mirror neurons responding to observation of actions made with tools in monkey ventral premotor cortex

In the present study, we describe a new type of visuomotor neurons, named tool-responding mirror neurons, which are found in the lateral sector of monkey ventral premotor area F5. Tool-responding mirror neurons discharge when the monkey observes actions performed by an experimenter with a tool (a stick or a pair of pliers). This response is stronger than that obtained when the monkey observes a similar action made with a biological effector (the hand or the mouth). These neurons respond also when the monkey executes actions with both the hand and the mouth. The visual and the motor responses of each neuron are congruent in that they share the same general goal, that is, taking possession of an object and modifying its state. It is hypothesized that after a relatively long visual exposure to tool actions, a visual association between the hand and the tool is created, so that the tool becomes as a kind of prolongation of the hand. We propose that tool-responding mirror neurons enable the observing monkey to extend action-understanding capacity to actions that do not strictly correspond to its motor representations. Our findings support the notion that the motor cortex plays a crucial role in understanding action goals.     

Potential role of monkey inferior parietal neurons coding action semantic equivalences as precursors of parts of speech

Abstract

The anterior portion of the inferior parietal cortex possesses comprehensive representations of actions embedded in behavioural contexts. Mirror neurons, which respond to both self-executed and observed actions, exist in this brain region in addition to those originally found in the premotor cortex. We found that parietal mirror neurons responded differentially to identical actions embedded in different contexts. Another type of parietal mirror neuron represents an inverse and complementary property of responding equally to dissimilar actions made by itself and others for an identical purpose. Here, we propose a hypothesis that these sets of inferior parietal neurons constitute a neural basis for encoding the semantic equivalence of various actions across different agents and contexts. The neurons have mirror neuron properties, and they encoded generalization of agents, differentiation of outcomes, and categorization of actions that led to common functions. By integrating the activities of these mirror neurons with various codings, we further suggest that in the ancestral primates’ brains, these various representations of meaningful action led to the gradual establishment of equivalence relations among the different types of actions, by sharing common action semantics. Such differential codings of the components of actions might represent precursors to the parts of protolanguage, such as gestural communication, which are shared among various members of a society. Finally, we suggest that the inferior parietal cortex serves as an interface between this action semantics system and other higher semantic systems, through common structures of action representation that mimic language syntax.     

Fronto‐parietal coding of goal‐directed actions performed by artificial agents

With advances in technology, artificial agents such as humanoid robots will soon become a part of our daily lives. For safe and intuitive collaboration, it is important to understand the goals behind their motor actions. In humans, this process is mediated by changes in activity in fronto‐parietal brain areas. The extent to which these areas are activated when observing artificial agents indicates the naturalness and easiness of interaction. Previous studies indicated that fronto‐parietal activity does not depend on whether the agent is human or artificial. However, it is unknown whether this activity is modulated by observing grasping (self‐related action) and pointing actions (other‐related action) performed by an artificial agent depending on the action goal. Therefore, we designed an experiment in which subjects observed human and artificial agents perform pointing and grasping actions aimed at two different object categories suggesting different goals. We found a signal increase in the bilateral inferior parietal lobule and the premotor cortex when tool versus food items were pointed to or grasped by both agents, probably reflecting the association of hand actions with the functional use of tools. Our results show that goal attribution engages the fronto‐parietal network not only for observing a human but also a robotic agent for both self‐related and social actions. The debriefing after the experiment has shown that actions of human‐like artificial agents can be perceived as being goal‐directed. Therefore, humans will be able to interact with service robots intuitively in various domains such as education, healthcare, public service, and entertainment.     

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.     

Recognition of point-light biological motion: mu rhythms and mirror neuron activity

Changes in power in the mu frequency band (8-13Hz) of the electroencephalogram (EEG) is thought to indirectly reflect the activity of mirror neurons in premotor cortex. Activation of these neurons by self-performed, observed or imagined motor actions is assumed to produce asynchronous firing and a reduction in mu rhythm oscillation (referred to as mu suppression) in sensorimotor cortex. A recent fMRI study by Saygin et al. [Saygin AP, Wilson SM, Hagler Jr DJ, Bates E, Sereno MI. Point-light biological motion perception activates human premotor cortex. J Neurosci 2004;24:6181-8] revealed that the premotor brain regions containing mirror-neurons are also activated in response to point-light human motion. The perceived movement of these light cues are integrated into one percept of a complete human action (e.g. jumping jacks), rather than seen as individual moving lights. The present study examined whether recruitment of the mirror neuron system, as reflected in mu rhythm suppression, mediates recognition of point-light biological motion. Changes in mu power were recorded while subjects viewed point-light biological motion videos, matched scrambled versions of these animations, and visual white-noise (baseline). The results revealed that point-light biological animations produced mu suppression relative to baseline, while scrambled versions of these animations did not. This supports the hypothesis that the mirror neuron system is involved in inferring human actions by recovering object information from sparse input.     

Making mirrors: premotor cortex stimulation enhances mirror and counter-mirror motor facilitation

Mirror neurons fire during both the performance of an action and the observation of the same action being performed by another. These neurons have been recorded in ventral premotor and inferior parietal cortex in the macaque, but human brain imaging studies suggest that areas responding to the observation and performance of actions are more widespread. We used paired-pulse TMS to test whether dorsal as well as ventral premotor cortex is involved in producing mirror motor facilitation effects. Stimulation of premotor cortex enhanced mirror motor facilitation and also enhanced the effects of counter-mirror training. No differences were found between the two premotor areas. These results support an associative account of mirror neuron properties, whereby multiple regions that process both sensory and motor information have the potential to contribute to mirror effects.     

Resonance of cortico-cortical connections of the motor system with the observation of goal directed grasping movements

Goal directed movements require the activation of parietal, premotor and primary motor areas. In monkeys, neurons of these areas become active also during the observation of movements performed by others, especially for coding the goal of the action (mirror system). Using bifocal transcranial magnetic stimulation (TMS) in healthy subjects, we tested whether the observation of goal directed reach to grasp actions may lead to specific changes in the short-latency connections linking key areas of the mirror system, such as the anterior intraparietal cortex (AIP) and the ventral premotor cortex (PMv), with the primary motor cortex (M1). We found that AIP-M1 and PMv-M1 cortico-cortical interactions were specifically activated when observing successful reaching to grasp goal directed actions, in which the hand posture was congruent with the goal of the action performed by the actor. On the other hand they were not modified when the same goal directed actions were performed wrongly with an inappropriate grasping posture. A similar profile of excitability was observed when testing specific intracortical facilitatory circuits in M1 (I₂-waves), known to reflect the activity in cortico-cortical pathways transmitting information from PMv. We conclude that the simple observation of others’ goal directed actions is able to induce specific neurophysiological changes in some cortico-cortical circuits of the human motor system.     

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.     

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.     

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.     

Mirror neurons responding to the observation of ingestive and communicative mouth actions in the monkey ventral premotor cortex

In the ventral premotor cortex (area F5) of the monkey there are neurons that discharge both when the monkey performs specific motor actions and when it observes another individual performing a similar action (mirror neurons). Previous studies on mirror neurons concerned hand actions. Here, we describe the mirror responses of F5 neurons that motorically code mouth actions. The results showed that about one-third of mouth motor neurons also discharge when the monkey observes another individual performing mouth actions. The majority of these 'mouth mirror neurons' become active during the execution and observation of mouth actions related to ingestive functions such as grasping, sucking or breaking food. Another population of mouth mirror neurons also discharges during the execution of ingestive actions, but the most effective visual stimuli in triggering them are communicative mouth gestures (e.g. lip smacking). Some also fire when the monkey makes communicative gestures. These findings extend the notion of mirror system from hand to mouth action and suggest that area F5, the area considered to be the homologue of human Broca's area, is also involved in communicative functions.     

Neurones miroirs,substrat neuronal de la compréhension de l’action?

In 1992, the Laboratory of Human Physiology at the University of Parma (Italy) publish a study describing “mirror” neurons in the macaque that activate both when the monkey performs an action and when it observes an experimenter performing the same action. The research team behind this discovery postulates that the mirror neurons system is the neural basis of our ability to understand the actions of others, through the motor mapping of the observed action on the observer's motor repertory (direct-matching hypothesis). Nevertheless, this conception met serious criticism. These critics attempt to relativize their function by placing them within a network of neurocognitive and sensory interdependencies. In short, the essential characteristic of these neurons is to combine the processing of sensory information, especially visual, with that of motor information. Their elementary function would be to provide a motor simulation of the observed action, based on visual information from it. They can contribute, with other non-mirror areas, to the identification/prediction of the action goal and to the interpretation of the intention of the actor performing it. Studying the connectivity and high frequency synchronizations of the different brain areas involved in action observation would likely provide important information about the dynamic contribution of mirror neurons to “action understanding”. The aim of this review is to provide an up-to-date analysis of the scientific evidence related to mirror neurons and their elementary functions, as well as to shed light on the contribution of these neurons to our ability to interpret and understand others’ actions.     

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.     

Les neurones miroirs

The neurophysiological studies of the last two decades have provided evidence that the motor cortex is not simply involved in movement programming and execution, but plays a main role in coding the goal of motor acts. The presence of dedicated anatomical circuits linking single premotor areas with specific areas of the posterior parietal cortex allows motor representations to be matched with several types of sensory inputs, thus allowing several types of sensorimotor integrations. An example of this matching mechanism is represented by mirror neurons, found in both the ventral premotor and the inferior parietal cortex of the monkey, responding during both observation and execution of hand and mouth motor acts. This capacity would allow individuals to understand the meaning of motor acts done by others. More recent studies on the response of these neurons during observation of motor acts performed at different distances suggested that they could play a role also in triggering different types of behavioral reactions. Furthermore, other recent studies indicate that mirror neurons may also have an important role in decoding the motor intention of others. A bulk of studies showed the presence of a parieto-premotor mirror system also in humans. Interestingly, some human studies demonstrated that this system could be modified by motor experience. This plasticity has been exploited in motor rehabilitation, to assess whether stroke patients can improve their motor function after an observation therapy. The results are positive and it seems that this therapy can be employed successfully also in children with cerebral palsy.     

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.     

Distinct cortical networks support the planning and online control of reaching-to-grasp in humans

A number of brain imaging studies have identified regions involved in the planning and control of complex actions. Here we attempt to contrast activity related to planning and online control in the human brain during simple reaching and grasping movements. In four conditions, participants did one of the following: passively observed a grasp target; planned a grasping movement without executing; planned and then executed a grasp; or immediately executed a grasp. Neural activity was measured using functional magnetic resonance imaging and activity in the various conditions compared. Two large, independent networks of brain activity were identified: (i) a planning network including the premotor cortex, basal ganglia, anterior cingulate, posterior medial parietal area, superior parietal occipital cortex and middle intraparietal sulcus; and (ii) a control network including sensorimotor cortex, the cerebellum, the supramarginal gyrus and the superior parietal lobule. These findings provide evidence that the planning and control of even simple reaching and grasping actions use different brain regions, including different parts of the frontal and parietal lobes.     

Connecting mirror neurons and forward models

Two recent developments in motor neuroscience are promising the extension of theoretical concepts from motor control towards cognitive processes, including human social interactions and understanding the intentions of others. The first of these is the discovery of what are now called mirror neurons, which code for both observed and executed actions. The second is the concept of internal models, and in particular recent proposals that forward and inverse models operate in paired modules. These two ideas will be briefly introduced, and a recent suggestion linking between the two processes of mirroring and modelling will be described which may underlie our abilities for imitating actions, for cooperation between two actors, and possibly for communication via gesture and language.     

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.     

Central thalamic inactivation impairs the expression of action‐ and outcome‐related responses of medial prefrontal cortex neurons in the rat

The mediodorsal (MD) and adjacent intralaminar (IL) and midline nuclei provide the main thalamic input to the medial prefrontal cortex (mPFC) and are critical for associative learning and decision‐making. MD neurons exhibit activity related to actions and outcomes that mirror responses of mPFC neurons in rats during dynamic delayed non‐match to position (dDNMTP), a variation of DNMTP where start location is varied randomly within an open octagonal arena to avoid confounding behavioral events with spatial location. To test whether the thalamus affects the expression of these responses in mPFC, we inhibited the central thalamus unilaterally by microinjecting muscimol at doses and sites found to affect decision‐making when applied bilaterally. Unilateral inactivation reduced normalized task‐related responses in the ipsilateral mPFC without disrupting behavior needed to characterize event‐related neuronal activity. Our results extend earlier findings that focused on delay‐related activity by showing that central thalamic inactivation interferes with responses related to actions and outcomes that occur outside the period of memory delay. These findings are consistent with the broad effects of central thalamic lesions on behavioral measures of reinforcement‐guided responding. Most (7/8) of the prefrontal response types affected by thalamic inactivation have also been observed in MD during dDNMTP. These results support the hypothesis that MD and IL act as transthalamic gates: monitoring prefrontal activity through corticothalamic inputs; integrating this information with signals from motivational and sensorimotor systems that converge in thalamus; and acting through thalamocortical projections to enhance expression of neuronal responses in the PFC that support adaptive goal‐directed behavior.