Modulation of motor cortex excitability by physical similarity with an observed hand action

The passive observation of hand actions is associated with increased motor cortex excitability, presumably reflecting activity within the human mirror neuron system (MNS). Recent data show that in-group ethnic membership increases motor cortex excitability during observation of culturally relevant hand gestures, suggesting that physical similarity with an observed body part may modulate MNS responses. Here, we ask whether the MNS is preferentially activated by passive observation of hand actions that are similar or dissimilar to self in terms of sex and skin color. Transcranial magnetic stimulation-induced motor evoked potentials were recorded from the first dorsal interosseus muscle while participants viewed videos depicting index finger movements made by female or male participants with black or white skin color. Forty-eight participants equally distributed in terms of sex and skin color participated in the study. Results show an interaction between self-attributes and physical attributes of the observed hand in the right motor cortex of female participants, where corticospinal excitability is increased during observation of hand actions in a different skin color than that of the observer. Our data show that specific physical properties of an observed action modulate motor cortex excitability and we hypothesize that in-group/out-group membership and self-related processes underlie these effects.     

Empathy and the somatotopic auditory mirror system in humans

How do we understand the actions of other individuals if we can only hear them? Auditory mirror neurons respond both while monkeys perform hand or mouth actions and while they listen to sounds of similar actions . This system might be critical for auditory action understanding and language evolution . Preliminary evidence suggests that a similar system may exist in humans . Using fMRI, we searched for brain areas that respond both during motor execution and when individuals listened to the sound of an action made by the same effector. We show that a left hemispheric temporo-parieto-premotor circuit is activated in both cases, providing evidence for a human auditory mirror system. In the left premotor cortex, a somatotopic pattern of activation was also observed: A dorsal cluster was more involved during listening and execution of hand actions, and a ventral cluster was more involved during listening and execution of mouth actions. Most of this system appears to be multimodal because it also responds to the sight of similar actions. Finally, individuals who scored higher on an empathy scale activated this system more strongly, adding evidence for a possible link between the motor mirror system and empathy.     

Testing simulation theory with cross-modal multivariate classification of fMRI data

The discovery of mirror neurons has suggested a potential neural basis for simulation and common coding theories of action perception, theories which propose that we understand other people's actions because perceiving their actions activates some of our neurons in much the same way as when we perform the actions. We propose testing this model directly in humans with functional magnetic resonance imaging (fMRI) by means of cross-modal classification. Cross-modal classification evaluates whether a classifier that has learned to separate stimuli in the sensory domain can also separate the stimuli in the motor domain. Successful classification provides support for simulation theories because it means that the fMRI signal, and presumably brain activity, is similar when perceiving and performing actions. In this paper we demonstrate the feasibility of the technique by showing that classifiers which have learned to discriminate whether a participant heard a hand or a mouth action, based on the activity patterns in the premotor cortex, can also determine, without additional training, whether the participant executed a hand or mouth action. This provides direct evidence that, while perceiving others' actions, (1) the pattern of activity in premotor voxels with sensory properties is a significant source of information regarding the nature of these actions, and (2) that this information shares a common code with motor execution.     

Grasping the Intentions of Others with One's Own Mirror Neuron System

Understanding the intentions of others while watching their actions is a fundamental building block of social behavior. The neural and functional mechanisms underlying this ability are still poorly understood. To investigate these mechanisms we used functional magnetic resonance imaging. Twenty-three subjects watched three kinds of stimuli: grasping hand actions without a context, context only (scenes containing objects), and grasping hand actions performed in two different contexts. In the latter condition the context suggested the intention associated with the grasping action (either drinking or cleaning). Actions embedded in contexts, compared with the other two conditions, yielded a significant signal increase in the posterior part of the inferior frontal gyrus and the adjacent sector of the ventral premotor cortex where hand actions are represented. Thus, premotor mirror neuron areas—areas active during the execution and the observation of an action—previously thought to be involved only in action recognition are actually also involved in understanding the intentions of others. To ascribe an intention is to infer a forthcoming new goal, and this is an operation that the motor system does automatically.     

Grasping the intentions of others with one's own mirror neuron system

Understanding the intentions of others while watching their actions is a fundamental building block of social behavior. The neural and functional mechanisms underlying this ability are still poorly understood. To investigate these mechanisms we used functional magnetic resonance imaging. Twenty-three subjects watched three kinds of stimuli: grasping hand actions without a context, context only (scenes containing objects), and grasping hand actions performed in two different contexts. In the latter condition the context suggested the intention associated with the grasping action (either drinking or cleaning). Actions embedded in contexts, compared with the other two conditions, yielded a significant signal increase in the posterior part of the inferior frontal gyrus and the adjacent sector of the ventral premotor cortex where hand actions are represented. Thus, premotor mirror neuron areas—areas active during the execution and the observation of an action—previously thought to be involved only in action recognition are actually also involved in understanding the intentions of others. To ascribe an intention is to infer a forthcoming new goal, and this is an operation that the motor system does automatically.     

Impaired motor facilitation during action observation in individuals with autism spectrum disorder

It has been suggested that social impairments observed in individuals with autism spectrum disorder (ASD) can be partly explained by an abnormal mirror neuron system (MNS) 1., 2.. Studies on monkeys have shown that mirror neurons are cells in premotor area F5 that discharge when a monkey executes or sees a specific action or when it hears the corresponding action-related sound 3., 4., 5.. Evidence for the presence of a MNS in humans comes in part from studies using transcranial magnetic stimulation (TMS), where a change in the amplitude of the TMS-induced motor-evoked potentials (MEPs) during action observation has been demonstrated 6., 7., 8., 9.. These data suggest that actions are understood when the representation of that action is mapped onto the observer's own motor structures [10]. To determine if the neural mechanism matching action observation and execution is anomalous in individuals with ASD, TMS was applied over the primary motor cortex (M1) during observation of intransitive, meaningless finger movements. We show that overall modulation of M1 excitability during action observation is significantly lower in individuals with ASD compared with matched controls. In addition, we find that basic motor cortex abnormalities do not underlie this impairment.     

Action Processing and Mirror Neuron Function in Patients with Amyotrophic Lateral Sclerosis: An fMRI Study

Amyotrophic lateral sclerosis (ALS) is a highly debilitating and rapidly fatal neurodegenerative disease. It has been suggested that social cognition may be affected, such as impairment in theory of mind (ToM) ability. Despite these findings, research in this area is scarce and the investigation of neural mechanisms behind such impairment is absent. Nineteen patients with ALS and eighteen healthy controls participated in this study. Because the mirror neuron system (MNS) is thought to be involved in theory of mind, we first implemented a straightforward action-execution and observation task to assess basic MNS function. Second, we examined the social-cognitive ability to understand actions of others, which is a component of ToM. We used fMRI to assess BOLD activity differences between groups during both experiments. Theory of mind was also measured behaviorally using the Reading the Mind in the Eyes test (RME). ALS patients displayed greater BOLD activity during the action-execution and observation task, especially throughout right anterior cortical regions. These areas included the right inferior operculum, premotor and primary motor regions, and left inferior parietal lobe. A conjunction analysis showed significantly more co-activated voxels during both the observation and action-execution conditions in the patient group throughout MNS regions. These results support a compensatory response in the MNS during action processing. In the action understanding experiment, healthy controls performed better behaviorally and subsequently recruited greater regions of activity throughout the prefrontal cortex and middle temporal gyrus. Lastly, action understanding performance was able to cluster patients with ALS into high and lower performing groups, which then differentiated RME performance. Collectively, these data suggest that social cognition, particularly theory of mind, may be affected in a subset of patients with ALS. This impairment may be related to functioning of the MNS and other regions related to action processing and understanding. Implications for future research are discussed.     

Attention Narrows Position Tuning of Population Responses in V1

When attention is directed to a region of space, visual resolution at that location flexibly adapts, becoming sharper to resolve fine-scale details or coarser to reflect large-scale texture and surface properties [1]. By what mechanism does attention improve spatial resolution? An improved signal-to-noise ratio (SNR) at the attended location contributes [2], because of retinotopically specific signal gain [3], [4], [5], [6], [7], [8], [9] and [10]. Additionally, attention could sharpen position tuning at the neural population level, so that adjacent objects activate more distinct regions of the visual cortex. A dual mechanism involving both signal gain and sharpened position tuning would be highly efficient at improving visual resolution, but there is no direct evidence that attention can narrow the position tuning of population responses. Here, we compared the spatial spread of the fMRI BOLD response for attended versus ignored stimuli. The activity produced by adjacent stimuli overlapped less when subjects were attending at their locations versus attending elsewhere, despite a stronger peak response with attention. Our results show that even as early as primary visual cortex (V1), spatially directed attention narrows the tuning of population-coded position representations.     

Extending the mirror neuron system model, II: what did I just do? A new role for mirror neurons

A mirror system is active both when an animal executes a class of actions (self-actions) and when it sees another execute an action of that class. Much attention has been given to the possible roles of mirror systems in responding to the actions of others but there has been little attention paid to their role in self-actions. In the companion article (Bonaiuto et al. Biol Cybern 96:9–38, 2007) we presented MNS2, an extension of the Mirror Neuron System model of the monkey mirror system trained to recognize the external appearance of its own actions as a basis for recognizing the actions of other animals when they perform similar actions. Here we further extend the study of the mirror system by introducing the novel hypotheses that a mirror system may additionally help in monitoring the success of a self-action and may also be activated by recognition of one’s own apparent actions as well as efference copy from one’s intended actions. The framework for this computational demonstration is a model of action sequencing, called augmented competitive queuing, in which action choice is based on the desirability of executable actions. We show how this “what did I just do?” function of mirror neurons can contribute to the learning of both executability and desirability which in certain cases supports rapid reorganization of motor programs in the face of disruptions.     

Young children with autism spectrum disorder use predictive eye movements in action observation

Does a dysfunction in the mirror neuron system (MNS) underlie the social symptoms defining autism spectrum disorder (ASD)? Research suggests that the MNS matches observed actions to motor plans for similar actions, and that these motor plans include directions for predictive eye movements when observing goal-directed actions. Thus, one important question is whether children with ASD use predictive eye movements in action observation. Young children with ASD as well as typically developing children and adults were shown videos in which an actor performed object-directed actions (human agent condition). Children with ASD were also shown control videos showing objects moving by themselves (self-propelled condition). Gaze was measured using a corneal reflection technique. Children with ASD and typically developing individuals used strikingly similar goal-directed eye movements when observing others’ actions in the human agent condition. Gaze was reactive in the self-propelled condition, suggesting that prediction is linked to seeing a hand–object interaction. This study does not support the view that ASD is characterized by a global dysfunction in the MNS.     

Granger causality mapping during joint actions reveals evidence for forward models that could overcome sensory-motor delays

Studies investigating joint actions have suggested a central role for the putative mirror neuron system (pMNS) because of the close link between perception and action provided by these brain regions [1], [2], [3]. In contrast, our previous functional magnetic resonance imaging (fMRI) experiment demonstrated that the BOLD response of the pMNS does not suggest that it directly integrates observed and executed actions during joint actions [4]. To test whether the pMNS might contribute indirectly to the integration process by sending information to brain areas responsible for this integration (integration network), here we used Granger causality mapping (GCM) [5]. We explored the directional information flow between the anterior sites of the pMNS and previously identified integrative brain regions. We found that the left BA44 sent more information than it received to both the integration network (left thalamus, right middle occipital gyrus and cerebellum) and more posterior nodes of the pMNS (BA2). Thus, during joint actions, two anatomically separate networks therefore seem effectively connected and the information flow is predominantly from anterior to posterior areas of the brain. These findings suggest that the pMNS is involved indirectly in joint actions by transforming observed and executed actions into a common code and is part of a generative model that could predict the future somatosensory and visual consequences of observed and executed actions in order to overcome otherwise inevitable neural delays.     

Selective imitation in domestic dogs

The transmission of cultural knowledge requires learners to identify what relevant information to retain and selectively imitate when observing others' skills. Young human infants--without relying on language or theory of mind--already show evidence of this ability. If, for example, in a communicative context, a model demonstrates a head action instead of a more efficient hand action, infants imitate the head action only if the demonstrator had no good reason to do so, suggesting that their imitation is a selective, interpretative process [1]. Early sensitivity to ostensive-communicative cues and to the efficiency of goal-directed actions is thought to be a crucial prerequisite for such relevance-guided selective imitation [2]. Although this competence is thought to be human specific [2], here we show an analog capacity in the dog. In our experiment, subjects watched a demonstrator dog pulling a rod with the paw instead of the preferred mouth action. In the first group, using the "inefficient" action was justified by the model's carrying of a ball in her mouth, whereas in the second group, no constraints could explain the demonstrator's choice. In the first trial after observation, dogs imitated the nonpreferred action only in the second group. Consequently, dogs, like children, demonstrated inferential selective imitation.     

Neural Activation in Humans during a Simple Motor Task Differs between BDNF Polymorphisms

The BDNF Val66Met polymorphism has been linked to decreased synaptic plasticity involved in motor learning tasks. We investigated whether individual differences in this polymorphism may promote differences in neural activity during a two-alternative forced-choice motor performance. In two separate sessions, the BOLD signal from 22 right-handed healthy men was measured during button presses with the left and right index finger upon visual presentation of an arrow. 11 men were Val66Val carriers (ValVal group), the other 11 men carried either the Val66Met or the Met66Met polymorphism (Non-ValVal group). Reaction times, resting and active motor thresholds did not differ between ValVal and Non-ValVal groups. Compared to the ValVal group the Non-ValVal group showed significantly higher BOLD signals in the right SMA and motor cingulate cortex during motor performance. This difference was highly consistent for both hands and across all four sessions. Our finding suggests that this BDNF polymorphism may not only influence complex performance during motor learning but is already associated with activation differences during rather simple motor tasks. The higher BOLD signal observed in Non-ValVal subjects suggests the presence of cumulative effects of the polymorphism on the motor system, and may reflect compensatory functional activation mediating equal behavioral performance between groups.     

Schema design and implementation of the grasp-related mirror neuron system

 Mirror neurons within a monkey's premotor area F5 fire not only when the monkey performs a certain class of actions but also when the monkey observes another monkey (or the experimenter) perform a similar action. It has thus been argued that these neurons are crucial for understanding of actions by others. We offer the hand-state hypothesis as a new explanation of the evolution of this capability: the basic functionality of the F5 mirror system is to elaborate the appropriate feedback – what we call the hand state– for opposition-space based control of manual grasping of an object. Given this functionality, the social role of the F5 mirror system in understanding the actions of others may be seen as an exaptation gained by generalizing from one's own hand to an other's hand. In other words, mirror neurons first evolved to augment the “canonical” F5 neurons (active during self-movement based on observation of an object) by providing visual feedback on “hand state,” relating the shape of the hand to the shape of the object. We then introduce the MNS1 (mirror neuron system 1) model of F5 and related brain regions. The existing Fagg–Arbib–Rizzolatti–Sakata model represents circuitry for visually guided grasping of objects, linking the anterior intraparietal area (AIP) with F5 canonical neurons. The MNS1 model extends the AIP visual pathway by also modeling pathways, directed toward F5 mirror neurons, which match arm–hand trajectories to the affordances and location of a potential target object. We present the basic schemas for the MNS1 model, then aggregate them into three “grand schemas”– visual analysis of hand state, reach and grasp, and the core mirror circuit – for each of which we present a useful implementation (a non-neural visual processing system, a multijoint 3-D kinematics simulator, and a learning neural network, respectively). With this implementation we show how the mirror system may learnto recognize actions already in the repertoire of the F5 canonical neurons. We show that the connectivity pattern of mirror neuron circuitry can be established through training, and that the resultant network can exhibit a range of novel, physiologically interesting behaviors during the process of action recognition. We train the system on the basis of final grasp but then observe the whole time course of mirror neuron activity, yielding predictions for neurophysiological experiments under conditions of spatial perturbation, altered kinematics, and ambiguous grasp execution which highlight the importance of the timingof mirror neuron activity. Received: 6 August 2001 / Accepted in revised form: 5 February 2002     

The role of ventral premotor cortex in action execution and action understanding

The human ventral premotor cortex overlaps, at least in part, with Broca's region in the dominant cerebral hemisphere, that is known to mediate the production of language and contributes to language comprehension. This region is constituted of Brodmann's areas 44 and 45 in the inferior frontal gyrus. We summarize the evidence that the motor related part of Broca's region is localized in the opercular portion of the inferior frontal cortex, mainly in area 44 of Brodmann. According to our own data, there seems to be a homology between Brodmann area 44 in humans and the monkey area F5. The non-language related motor functions of Broca's region comprise complex hand movements, associative sensorimotor learning and sensorimotor integration. Brodmann's area 44 is also a part of a specialized parieto-premotor network and interacts significantly with the neighbouring premotor areas. In the ventral premotor area F5 of monkeys, the so called mirror neurons have been found which discharge both when the animal performs a goal-directed hand action and when it observes another individual performing the same or a similar action. More recently, in the same area mirror neurons responding not only to the observation of mouth actions, but also to sounds characteristic to actions have been found. In humans, through an fMRI study, it has been shown that the observation of actions performed with the hand, the mouth and the foot leads to the activation of different sectors of Broca's area and premotor cortex, according to the effector involved in the observed action, following a somatotopic pattern which resembles the classical motor cortex homunculus. On the other hand the evidence is growing that human ventral premotor cortex, especially Brodmann's area 44, is involved in polymodal action processing. These results strongly support the existence of an execution-observation matching system (mirror neuron system). It has been proposed that this system is involved in polymodal action recognition and might represent a precursor of language processing. Experimental evidence in favour of this hypothesis both in the monkey and humans is shortly reviewed.     

Complementary Hand Responses Occur in Both Peri- and Extrapersonal Space

Human beings have a strong tendency to imitate. Evidence from motor priming paradigms suggests that people automatically tend to imitate observed actions such as hand gestures by performing mirror-congruent movements (e.g., lifting one’s right finger upon observing a left finger movement; from a mirror perspective). Many observed actions however, do not require mirror-congruent responses but afford complementary (fitting) responses instead (e.g., handing over a cup; shaking hands). Crucially, whereas mirror-congruent responses don''t require physical interaction with another person, complementary actions often do. Given that most experiments studying motor priming have used stimuli devoid of contextual information, this space or interaction-dependency of complementary responses has not yet been assessed. To address this issue, we let participants perform a task in which they had to mirror or complement a hand gesture (fist or open hand) performed by an actor depicted either within or outside of reach. In three studies, we observed faster reaction times and less response errors for complementary relative to mirrored hand movements in response to open hand gestures (i.e., ‘hand-shaking’) irrespective of the perceived interpersonal distance of the actor. This complementary effect could not be accounted for by a low-level spatial cueing effect. These results demonstrate that humans have a strong and automatic tendency to respond by performing complementary actions. In addition, our findings underline the limitations of manipulations of space in modulating effects of motor priming and the perception of affordances.     

Frequency and topography in monkey electroencephalogram during action observation: possible neural correlates of the mirror neuron system

The observation of actions executed by others results in desynchronization of electroencephalogram (EEG) in the alpha and beta frequency bands recorded from the central regions in humans. On the other hand, mirror neurons, which are thought to be responsible for this effect, have been studied only in macaque monkeys, using single-cell recordings. Here, as a first step in a research programme aimed at understanding the parallels between human and monkey mirror neuron systems (MNS), we recorded EEG from the scalp of two monkeys during action observation. The monkeys were trained to fixate on the face of a human agent and subsequently to fixate on a target upon which the agent performed a grasping action. We found that action observation produced desynchronization in the 19–25 Hz band that was strongest over anterior and central electrodes. These results are in line with human data showing that specific frequency bands within the power spectrum of the ongoing EEG may be modulated by observation of actions and therefore might be a specific marker of MNS activity.     

An interference effect of observed biological movement on action

It has been proposed that actions are intrinsically linked to perception and that imagining, observing, preparing, or in any way representing an action excites the motor programs used to execute that same action. There is neurophysiological evidence that certain brain regions involved in executing actions are activated by the mere observation of action (the so-called "mirror system;" ). However, it is unknown whether this mirror system causes interference between observed and simultaneously executed movements. In this study we test the hypothesis that, because of the overlap between action observation and execution, observed actions should interfere with incongruous executed actions. Subjects made arm movements while observing either a robot or another human making the same or qualitatively different arm movements. Variance in the executed movement was measured as an index of interference to the movement. The results demonstrate that observing another human making incongruent movements has a significant interference effect on executed movements. However, we found no evidence that this interference effect occurred when subjects observed a robotic arm making incongruent movements. These results suggest that the simultaneous activation of the overlapping neural networks that process movement observation and execution infers a measurable cost to motor control.     

Optimal task-dependent changes of bimanual feedback control and adaptation

The control and adaptation of bimanual movements is often considered to be a function of a fixed set of mechanisms [1, 2]. Here, I show that both feedback control and adaptation change optimally with task goals. Participants reached with two hands to two separate spatial targets (two-cursor condition) or used the same bimanual movements to move a cursor presented at the spatial average location of the two hands to a single target (one-cursor condition). A force field was randomly applied to one of the hands. In the two-cursor condition, online corrections occurred only on the perturbed hand, whereas the other movement was controlled independently. In the one-cursor condition, online correction could be detected on both hands as early as 190 ms after the start. These changes can be shown to be optimal in respect to a simple task-dependent cost function [3]. Adaptation, the influence of a perturbation onto the next movement, also depended on task goals. In the two-cursor condition, only the perturbed hand adapted to a force perturbation [2], whereas in the one-cursor condition, both hands adapted. These findings demonstrate that the central nervous system changes bimanual feedback control and adaptation optimally according to the current task requirements.     

Motor simulation without motor expertise: enhanced corticospinal excitability in visually experienced dance spectators

The human "mirror-system" is suggested to play a crucial role in action observation and execution, and is characterized by activity in the premotor and parietal cortices during the passive observation of movements. The previous motor experience of the observer has been shown to enhance the activity in this network. Yet visual experience could also have a determinant influence when watching more complex actions, as in dance performances. Here we tested the impact visual experience has on motor simulation when watching dance, by measuring changes in corticospinal excitability. We also tested the effects of empathic abilities. To fully match the participants' long-term visual experience with the present experimental setting, we used three live solo dance performances: ballet, Indian dance, and non-dance. Participants were either frequent dance spectators of ballet or Indian dance, or "novices" who never watched dance. None of the spectators had been physically trained in these dance styles. Transcranial magnetic stimulation was used to measure corticospinal excitability by means of motor-evoked potentials (MEPs) in both the hand and the arm, because the hand is specifically used in Indian dance and the arm is frequently engaged in ballet dance movements. We observed that frequent ballet spectators showed larger MEP amplitudes in the arm muscles when watching ballet compared to when they watched other performances. We also found that the higher Indian dance spectators scored on the fantasy subscale of the Interpersonal Reactivity Index, the larger their MEPs were in the arms when watching Indian dance. Our results show that even without physical training, corticospinal excitability can be enhanced as a function of either visual experience or the tendency to imaginatively transpose oneself into fictional characters. We suggest that spectators covertly simulate the movements for which they have acquired visual experience, and that empathic abilities heighten motor resonance during dance observation.