Mirror neuron function, psychosis, and empathy in schizophrenia

Processing of social and emotional information has been shown to be disturbed in schizophrenia. The biological underpinnings of these abnormalities may be explained by an abnormally functioning mirror neuron system. Yet the relationship between mirror neuron system activity in schizophrenia, as measured using an electroencephalography (EEG) paradigm, and socio-emotional functioning has not been assessed. The present research measured empathy and mirror neuron activity using an established EEG paradigm assessing the integrity of the Mu rhythm (8-13Hz) suppression over the sensorimotor cortex during observed and actual hand movement in 16 schizophrenia-spectrum disorder (SSD) participants (n=8 actively psychotic and n=8 in residual illness phase) and 16 age- and gender-matched healthy comparison participants. Actively psychotic SSD participants showed significantly greater mu suppression over the sensorimotor cortex of the left hemisphere than residual phase SSD and healthy comparison individuals. The latter two groups showed similar levels of mu suppression. Greater left-sided mu suppression was positively correlated with psychotic symptoms (i.e., greater mu suppression/mirror neuron activity was highest among subjects with the greater severity of psychotic symptoms). SSD subjects tended to have significantly higher levels of Personal Distress (as measured by the Interpersonal Reactivity Index) than healthy participants. The present study suggests that abnormal mirror neuron activity may exist among patients with schizophrenia during the active (psychotic) phase of the illness, and correlates with severity of psychosis.     

Electroencephalogram evidence for the activation of human mirror neuron system during the observation of intransitive shadow and line drawing actions

Previous studies have demonstrated that hand shadows may activate the motor cortex associated with the mirror neuron system in human brain. However, there is no evidence of activity of the human mirror neuron system during the observation of intransitive movements by shadows and line drawings of hands. This study examined the suppression of electroencephalography mu waves (8-13 Hz) induced by observation of stimuli in 18 healthy students. Three stimuli were used: real hand actions, hand shadow actions and actions made by line drawings of hands. The results showed significant desynchronization of the mu rhythm ("mu suppression") across the sensorimotor cortex (recorded at C3, Cz and C4), the frontal cortex (recorded at F3, Fz and F4) and the central and right posterior parietal cortex (recorded at Pz and P4) under all three conditions. Our experimental findings suggest that the observation of "impoverished hand actions", such as intransitive movements of shadows and line drawings of hands, is able to activate widespread cortical areas related to the putative human mirror neuron system.     

Effects of brief imitative experience on EEG desynchronization during action observation

There is a good deal of evidence that observing the actions of other people is associated with activation of the observer's motor system, which may reflect involvement of the mirror neuron system (MNS) in certain aspects of action processing in humans. Furthermore, variation in the extent of this activation appears to be partly dependent on individuals’ experience with performing the observed actions. However, very little work has examined the processes through which the observation of unfamiliar actions - which are not in an observer's motor repertoire - might become associated with MNS activation. In the current study we examined differences in EEG desynchronization in alpha-range bands during action observation following very brief imitative experience with the observed actions, which were novel drawing movements. Compared to carrying out unrelated actions, brief imitative experience was specifically associated with a significantly larger desynchronization in the 11-13 Hz band at mid-frontal sites (F3 and F4) when a previously imitated action was viewed again. In addition, higher fidelity of imitation was significantly correlated with greater bilateral desynchronization of the lower mu band (8-10 Hz) at central sites (C3 and C4) during subsequent observation of the previously imitated action. Our findings point to the involvement of frontal cortical processing and the MNS in the early stages of imitative learning.     

Neural correlates related to action observation in expert archers

A growing body of evidence suggests that activity of the mirror neuron system is dependent on the observer's motor experience of a given action. It remains unclear, however, whether activity of the mirror neuron system is also associated with the observer's motor experience in sports game. Therefore, the aim of the present study is to investigate differences in activation of the mirror neuron system during action observation between experts and non-archer control subjects. We used video of Western-style archery in which participants were asked to watch the archery movements. Hyperactivation of the premotor and inferior parietal cortex in expert archers relative to non-archer control subjects suggests that the human mirror neuron system could contain and expand representations of the motor repertoire. The fact that dorsomedial prefrontal cortex was more active in expert archers than in non-archer control subjects indicates a spontaneous engagement of theory of mind in experts when watching video of Western-style archery. Compared with the non-archer control subjects, expert archers showed greater activation in the neural system in regions associated with episodic recall from familiar and meaningful information, including the cingulate cortex, retrosplenial cortex, and parahippocampal gyrus. The results demonstrate that expertise effects stimulate brain activity not only in the mirror neuron system but also in the neural networks related to theory of mind and episodic memory.     

Understanding mirror neurons: Evidence for enhanced corticospinal excitability during the observation of transitive but not intransitive hand gestures

Putative measures of mirror neuron activity suggest that mirror neurons respond preferentially to biological motion, but it remains unclear whether enhanced cortical activity occurs during the observation of any behaviour, or whether that behaviour needs to be associated with a particular object or goal. Forty-three healthy adults completed a transcranial magnetic stimulation (TMS) experiment that assessed corticospinal excitability while viewing intransitive and transitive hand gestures (compared with the presentation of a static hand). Visual presentations were designed to control for motoric and stimulus properties. A significant increase in corticospinal excitability (putatively reflecting mirror neuron activation) was seen only during the observation of transitive behaviour. These findings are consistent with the notion that human hand-related mirror neurons are sensitive to object- and goal-directed behaviour, rather than biological motion per se.     

Sensorimotor mu rhythm during action observation changes across the lifespan independently from social cognitive processes

The observation of actions performed by another person activates parts of the brain as if the observer were performing that action, referred to as the ‘mirror system’. Very little is currently known about the developmental trajectory of the mirror system and related social cognitive processes. This experimental study sought to explore the modulation of the sensorimotor mu rhythm during action observation using EEG measures, and how these may relate to social cognitive abilities across the lifespan, from late childhood through to old age. Three-hundred and one participants aged 10- to 86-years-old completed an action observation EEG task and three additional explicit measures of social cognition. As predicted, findings show enhanced sensorimotor alpha and beta desynchronization during hand action observation as compared to static hand observation. Overall, our findings indicate that the reactivity of the sensorimotor mu rhythm to the observation of others’ actions increases throughout the lifespan, independently from social cognitive processes.     

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.     

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.     

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.     

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.     

Mu rhythm modulation during observation of an object-directed grasp

Recent electrophysiological studies have shown that the human electroencephalographic mu rhythm is suppressed during the observation of actions performed by other persons, an effect that may be functionally related to the behaviour of so-called "mirror neurons" observed in area F5 of nonhuman primates. Because mirror neuron activity has been reported to be functionally specific to object-oriented actions, the present study was designed to determine if the human mu rhythm also exhibits this property. EEG measurements were obtained from 12 normal subjects while they observed either a precision grip of a manipulandum or an empty grip using the same hand position. Our results showed that the magnitude of the mu rhythm was significantly lower for the object grip condition than for the empty grip condition. These data support the notion that the human mu rhythm indexes a brain system that is functionally comparable to the monkey mirror neuron system. We propose that nonobject-directed actions may result in representational schemas that are either different or less salient than motorically equivalent actions that are directed toward objects.     

Gender differences in the human mirror system: a magnetoencephalography study

The present study investigated whether the human mirror-neuron system exhibits gender differences. Neuromagenetic mu (approximately 20 Hz) oscillations were recorded over the right primary motor cortex, which reflect the mirror neuron activity, in 10 female and 10 male participants while they observed the videotaped hand actions and moving dot. In accordance with previous studies, all participants had mu suppression during the observation of hand action, indicating activation of primary motor cortex. Interestingly, the female participants displayed apparently stronger (P < 0.05) suppression for the hand action than for the moving dot whereas the men showed the opposite (P < 0.05). These findings have implications for the extreme male brain theory of autism and support the hypothesis of a dysfunctional mirror-neuron system in autism.     

物理训练外的活动依赖性神经康复：镜像机制

The present study observed the effects of the non-invasive, mirror neuron system application on neurorehabilitation. In primate studies, mirror neurons have been shown to fire when the subject observes or performs a specific action, thereby allowing for observation of motor cortex activation. This activation of the mirror neuron system could serve as a treatment for stroke patients. In the present study, the combination of a mirror neuron system-based therapy was introduced for the treatment of patients with motor-deficits, who could not perform rehabilitation exercises. The results also indicate that this therapeutic method plays a positive role in emotional regulation in the same patients.     

Reduced Mirror Neuron Activity in Schizophrenia and Its Association With Theory of Mind Deficits: Evidence From a Transcranial Magnetic Stimulation Study

Background: The “mirror-neuron system” has been proposed to be a neurophysiological substrate for social cognition (SC) ability. We used transcranial magnetic stimulation (TMS) paradigms to compare putative mirror neuron activity (MNA) in 3 groups: antipsychotic-naive, medicated schizophrenia patients, and healthy comparison subjects. We also explored the association between MNA and SC ability in patients. Methods: Fifty-four consenting right-handed schizophrenia patients (33 antipsychotic naive) and 45 matched healthy comparison subjects completed a TMS experiment to assess putative premotor MNA. We used 4 TMS paradigms of eliciting motor-evoked potentials (MEP) in the right first dorsal interosseous (FDI) muscle. These were applied while the subjects observed a goal-directed action involving the FDI (actual action and its video) and a static image. The difference in the amplitude of the MEP while they observed the static image and the action provided a measure of MNA. Subjects also underwent SC assessments (theory of mind [ToM], emotion processing, and social perception). Results: Two-way repeated measures ANOVA revealed significant group × occasion interaction effect in 3 TMS paradigms, indicating deficient motor facilitation during action observation relative to rest state in antipsychotic-naive schizophrenia patients as compared with the other two groups. Among patients, there were significant direct correlations between measures of MNA and ToM performance. Conclusions: Antipsychotic-naive schizophrenia patients have poorer MNA than medicated patients and healthy controls. Measures of putative MNA had significant and consistent associations with ToM abilities. These findings suggest a possibility of deficient mirror neuron system underlying SC deficits in schizophrenia.Key words: mirror neurons, social cognition, mental state attribution, psychosis, antipsychotic-naive, embodied simulation     

An fMRI study of action observation and action execution in childhood

Although many studies have examined the location and function of the mirror neuron system (MNS) in human adults, we know relatively little about its development. The current study fills this gap by using fMRI to examine for the first time the development of the brain regions implicated in action execution, action observation, and their overlap. We examined age-related differences in brain activation by contrasting a group of children (n = 21) and adults (n = 18). Surfaced-based analyses of action execution and action observation revealed that brain activity for action observation and execution in children is similar to adults, though adults displayed greater activity than children within the right superior parietal lobe during action execution and the occipital lobe during action observation compared to control. Further, within-individual measures of overlapping activation between action observation and execution revealed age-related differences, such that adults, compared to children, displayed more spatial overlap. Moreover, the extent of the overlap in activation across conditions was related to better motor skills and action representation abilities in children. These data indicate that the MNS changes between middle childhood and adulthood. The data also demonstrate the functional significance of the putative MNS to motor skills and action representation during development.     

Effects of different viewing perspectives on somatosensory activations during observation of touch

Previous studies showed that neurons in the monkey premotor cortex became active when performing a particular action and also when observing the same action performed by others. These findings suggest a mirror system for action observation. Recently, bimodal neurons, sensitive both to visual and tactile stimulation, were reported in the parietal cortex, suggesting a potential mirror neuron system for observing and experiencing tactile stimulation. Subsequently, a mirror neuron system for observed touch has been suggested. The current study was designed to determine whether the activation of a sensory mirror system during touch observation is affected by possible attributions of the observed touch to oneself (subjective view) or to somebody else (objective view). In the study, healthy volunteers observed video clips of a touched or nontouched hand either in an egocentric or in an allocentric perspective during functional magnetic resonance imaging. Results showed activation of somatosensory cortices when observing the hand being touched in egocentric as well as in the allocentric perspectives. Moreover, somatosensory responses differed depending on the perspective of the observed touch. We discuss the results in terms of a possible mirror neuron system for observed and experienced touch. Hum Brain Mapp 2009. © 2009 Wiley‐Liss, Inc.     

Mirror neuron activation as a function of explicit learning: changes in mu‐event‐related power after learning novel responses to ideomotor compatible,partially compatible,and non‐compatible stimuli

Questions regarding the malleability of the mirror neuron system (MNS) continue to be debated. MNS activation has been reported when people observe another person performing biological goal‐directed behaviors, such as grasping a cup. These findings support the importance of mapping goal‐directed biological behavior onto one's motor repertoire as a means of understanding the actions of others. Still, other evidence supports the Associative Sequence Learning (ASL) model which predicts that the MNS responds to a variety of stimuli after sensorimotor learning, not simply biological behavior. MNS activity develops as a consequence of developing stimulus‐response associations between a stimulus and its motor outcome. Findings from the ideomotor literature indicate that stimuli that are more ideomotor compatible with a response are accompanied by an increase in response activation compared to less compatible stimuli; however, non‐compatible stimuli robustly activate a constituent response after sensorimotor learning. Here, we measured changes in the mu‐rhythm, an EEG marker thought to index MNS activity, predicting that stimuli that differ along dimensions of ideomotor compatibility should show changes in mirror neuron activation as participants learn the respective stimulus‐response associations. We observed robust mu‐suppression for ideomotor‐compatible hand actions and partially compatible dot animations prior to learning; however, compatible stimuli showed greater mu‐suppression than partially or non‐compatible stimuli after explicit learning. Additionally, non‐compatible abstract stimuli exceeded baseline only after participants explicitly learned the motor responses associated with the stimuli. We conclude that the empirical differences between the biological and ASL accounts of the MNS can be explained by Ideomotor Theory.     

Reduced motor facilitation during action observation in schizophrenia: a mirror neuron deficit?

Impairments in social cognitive functioning are well documented in schizophrenia, however the neural basis of these deficits is unclear. A recent explanatory model of social cognition centers upon the activity of mirror neurons, which are cortical brain cells that become active during both the performance and observation of behavior. Here, we test for the first time whether mirror neuron functioning is reduced in schizophrenia. Fifteen individuals with schizophrenia or schizoaffective disorder and fifteen healthy controls completed a transcranial magnetic stimulation (TMS) experiment designed to assess mirror neuron activation. While patients demonstrated no abnormalities in cortical excitability, motor facilitation during action observation, putatively reflecting mirror neuron activity, was reduced in schizophrenia. Dysfunction within the mirror neuron system may contribute to the pathophysiology of schizophrenia.     

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.     

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.