Motor facilitation during action observation: topographic mapping of the target muscle and influence of the onlooker's posture

Transcranial magnetic stimulation (TMS) studies report that viewing a given action performed by a model activates the neural representation of the onlooker's muscles that are activated during the actual execution of the observed action. Here we sought to determine whether this mirror observation-execution facilitation reflects only muscular specificity or whether it is also influenced by postural congruency between onlooker/model body parts. We recorded motor potentials evoked by single-pulse TMS from the first dorsal interosseous (FDI) and abductor digiti minimi (ADM) muscles during observation of the right index and little finger abduction/adduction movements of models who kept their hands in a palm-down or palm-up position. Moreover, in different experiments observers kept their right hand palm down or palm up. Selective motor facilitation was observed during observation of movements that map the motor function of the targeted muscles, regardless of the posture of the observed hand. Modulation of FDI, however, was obtained only when participants kept their hand palm down; by contrast, modulation of ADM was obtained only when participants kept their hand palm up. Interestingly, electromyographic recordings showed that FDI is mostly active when index abduction/adduction movements are performed in the palm-down position, whereas ADM is mostly active when little finger abduction/adduction movements are performed in the palm-up position. Results show that the influence of the onlooker's hand posture is comparable in action execution and observation, thus indicating a fine-grain functional correspondence between these two processes.     

Early and late motor responses to action observation

Is a short visuomotor associative training sufficient to reverse the visuomotor tuning of mirror neurons in adult humans? We tested the effects of associative training on corticospinal modulation during action observation in the 100–320 ms interval after action onset. In two separate experiments, the acceleration of transcranial magnetic stimulation (TMS)-induced movements was recorded before and after training participants to respond to observed acts with an opposite or similar behavior. Before training, TMS-induced accelerations mirrored the observed action at 250 and 320 ms. After training, responses at 250 ms were unchanged and still mirrored the stimuli, without any effect of training direction. Only at 320 ms, we observed training-dependent changes in evoked responses. A control experiment with non-biological rotational movements as visual stimuli indicated that spatial stimulus–response compatibility is not sufficient to account for the results of the two main experiments. We show that the effects of a short visuomotor associative training are not pervasive on the automatic mirror responses. ‘Early’ (250 ms) responses were not influenced by training. Conversely only ‘late’ (320 ms) responses changed according to the training direction. This biphasic time course indicates that two distinct mechanisms produce the automatic mirror responses and the newly learned visuomotor associations.     

Dynamical entrainment of corticospinal excitability during rhythmic movement observation: a Transcranial Magnetic Stimulation study

Spontaneous modulations of corticospinal excitability during action observation have been interpreted as evidence for the activation of internal motor representations equivalent to the observed action. Alternatively or complementary to this perspective, growing evidence shows that motor activity during observation of rhythmic movements can be modulated by direct visuomotor couplings and dynamical entrainment. In‐phase and anti‐phase entrainment spontaneously occur, characterized by cyclic movements proceeding simultaneously in the same (in‐phase) or opposite (anti‐phase) direction. Here we investigate corticospinal excitability during the observation of vertical oscillations of an index finger using Transcranial Magnetic Stimulation (TMS). Motor‐evoked potentials (MEPs) were recorded from participants’ flexor and extensor muscles of the right index finger, placed in either a maximal steady flexion or extension position, with stimulations delivered at maximal flexion, maximal extension or mid‐trajectory of the observed finger oscillations. Consistent with the occurrence of dynamical motor entrainment, increased and decreased MEP responses – suggesting the facilitation of stable in‐phase and anti‐phase relations but not an unstable 90° phase relation – were found in participants’ flexors. Anti‐phase motor facilitation contrasts with the activation of internal motor representation as it involves activity in the motor system opposite from activity required for the execution of the observed movement. These findings demonstrate the relevance of dynamical entrainment theories and methods for understanding spontaneous motor activity in the brain during action observation and the mechanisms underpinning coordinated movements during social interaction.     

EEG evidence for the presence of an action observation-execution matching system in children

In the adult human brain, passive observation of actions performed by others activates some of the same cortical areas that are involved in the execution of actions, thereby contributing to action recognition. This mechanism appears to occur through activation of a population of action-coding cells known as mirror neurons (MN). In the adult motor cortex, performing actions and observing human movement reduces the magnitude of the mu (8-13 Hz) rhythm, possibly reflecting MN system activity. Despite the wealth of information available regarding the adult MN system, little is known about its existence in children. Here, we used EEG to probe mu rhythm modulation in 15 children during observation and execution of hand actions. Our data show that mu rhythm attenuation occurs in children under 11 years old during observation of hand movements. Similarly to what has been reported in adults, observation of goal/object-orientated movement produces greater modulation of the mu rhythm than intransitive movement. These data confirm the existence of an observation-execution matching system in the immature human brain and may be of clinical value in the understanding of neurodevelopmental disorders associated with a faulty MN system, such as autism spectrum disorder.     

Differential modulation of corticospinal excitability during observation, mental imagery and imitation of hand actions

In this study, we attempted to better delineate the changes in corticospinal excitability that accompany perceptual to motor transformations when people are asked to observe, image or imitate actions. Motor evoked potentials (MEP) from transcranial magnetic stimulation were recorded in the first dorsal interosseous (FDI) muscle of the dominant hand (15 right, 4 left) in five different conditions: (1) passive observation; (2) observation to imitate; (3) imagery; (4) imitation; and (5) counting backwards mentally. MEPs were also recorded at rest at the beginning and at the end of the session to establish baseline (BL) values. For the observation conditions, participants (n=19, 18-38 years) watched video sequences (5s) of hand actions performed by a model with the right arm (passive observation: scissors; observation to imitate: OK sign). Active imitation produced the greatest MEP facilitation compared to baseline, followed by the two observation conditions and the imagery conditions, which all produced similar levels of facilitation (post hoc comparisons). Mental counting produced some facilitation, but this effect was inconsistent. Baseline MEPs remained stable at the end of the session. A further comparison between right-handers (n=15) and left-handers (n=4) revealed no difference in the pattern of modulation across conditions. The similarity found between observation and imagery of hand actions in terms of corticospinal facilitation is interpreted in the light of the motor-simulation theory of Jeannerod [Neuroimage 14 (2001)], which proposes that perceiving actions involves neural simulation of the same action by the observer, thereby explaining the parallel between actions observed and actions imaged at the representational level.     

Transcranial magnetic stimulation reveals modulation of corticospinal excitability when observing actions with the intention to imitate

Studies using transcranial magnetic stimulation have demonstrated that action observation can modulate the activity of the corticospinal system. This has been attributed to the activity of an 'action observation network', whereby premotor cortex activity influences corticospinal excitability. Neuroimaging studies have demonstrated that the context in which participants observe actions (i.e. whether they simply attend to an action, or observe it with the intention to imitate) modulates action observation network activity. The study presented here examined whether the context in which actions were observed revealed similar modulatory effects on corticospinal excitability. Eight human participants observed a baseline stimulus (a fixation cross), observed actions in order to attend to them, or observed the same actions with the intention to imitate them. Whereas motor evoked potentials elicited from the first dorsal interosseus muscle of the hand were facilitated by attending to actions, observing the same actions in an imitative capacity led to no facilitation effect. Furthermore, no motor facilitation effects occurred in a control muscle. Electromyographic data collected when participants physically imitated the observed actions revealed that the activity of the first dorsal interosseus muscle increased significantly during action execution compared with rest. These data suggest that an inhibitory mechanism acts on the corticospinal system to prevent the immediate overt imitation of observed actions. These data provide novel insight into the properties of the human action observation network, demonstrating for the first time that observing actions with the intention to imitate them can modulate the effects of action observation on corticospinal excitability.     

Neurons in primary motor cortex engaged during action observation

Neurons in higher cortical areas appear to become active during action observation, either by mirroring observed actions (termed mirror neurons) or by eliciting mental rehearsal of observed motor acts. We report the existence of neurons in the primary motor cortex (M1), an area that is generally considered to initiate and guide movement performance, responding to viewed actions. Multielectrode recordings in monkeys performing or observing a well‐learned step‐tracking task showed that approximately half of the M1 neurons that were active when monkeys performed the task were also active when they observed the action being performed by a human. These ‘view’ neurons were spatially intermingled with ‘do’ neurons, which are active only during movement performance. Simultaneously recorded ‘view’ neurons comprised two groups: approximately 38% retained the same preferred direction (PD) and timing during performance and viewing, and the remainder (62%) changed their PDs and time lag during viewing as compared with performance. Nevertheless, population activity during viewing was sufficient to predict the direction and trajectory of viewed movements as action unfolded, although less accurately than during performance. ‘View’ neurons became less active and contained poorer representations of action when only subcomponents of the task were being viewed. M1 ‘view’ neurons thus appear to reflect aspects of a learned movement when observed in others, and form part of a broadly engaged set of cortical areas routinely responding to learned behaviors. These findings suggest that viewing a learned action elicits replay of aspects of M1 activity needed to perform the observed action, and could additionally reflect processing related to understanding, learning or mentally rehearsing action.     

Left hemisphere motor facilitation in response to manual action sounds

Previous studies indicate that the motor areas of both hemispheres are active when observing actions. Here we explored how the motor areas of each hemisphere respond to the sounds associated with actions. We used transcranial magnetic stimulation (TMS) to measure motor corticospinal excitability of hand muscles while listening to sounds. Sounds associated with bimanual actions produced greater motor corticospinal excitability than sounds associated with leg movements or control sounds. This facilitation was exclusively lateralized to the left hemisphere, the dominant hemisphere for language. These results are consistent with the hypothesis that action coding may be a precursor of language.     

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.     

Prediction of human actions: Expertise and task‐related effects on neural activation of the action observation network

The action observation network (AON) is supposed to play a crucial role when athletes anticipate the effect of others' actions in sports such as tennis. We used functional magnetic resonance imaging to explore whether motor expertise leads to a differential activation pattern within the AON during effect anticipation and whether spatial and motor anticipation tasks are associated with a differential activation pattern within the AON depending on participant expertise level. Expert (N = 16) and novice (N = 16) tennis players observed video clips depicting forehand strokes with the instruction to either indicate the predicted direction of ball flight (spatial anticipation) or to decide on an appropriate response to the observed action (motor anticipation). The experts performed better than novices on both tennis anticipation tasks, with the experts showing stronger neural activation in areas of the AON, namely, the superior parietal lobe, the intraparietal sulcus, the inferior frontal gyrus, and the cerebellum. When novices were contrasted with experts, motor anticipation resulted in stronger activation of the ventral premotor cortex, the supplementary motor area, and the superior parietal lobe than spatial anticipation task did. In experts, the comparison of motor and spatial anticipation revealed no increased activation. We suggest that the stronger activation of areas in the AON during the anticipation of action effects in experts reflects their use of the more fine‐tuned motor representations they have acquired and improved during years of training. Furthermore, results suggest that the neural processing of different anticipation tasks depends on the expertise level. Hum Brain Mapp 35:4016–4034, 2014. © 2014 Wiley Periodicals, Inc .     

The influence of intrapersonal sensorimotor experiences on the corticospinal responses during action–observation

The coupling of perception and action has been strongly indicated by evidence that the observation of an action primes a response in the observer. It has been proposed that these primed responses may be inhibited when the observer is able to more closely distinguish between self- and other-generated actions – the greater the distinction, then the greater the inhibition of the primed response. This self–other distinction is shown to be enhanced following a period of visual feedback of self-generated action. The present study was designed to examine how sensorimotor experiences pertaining to self-generated action affect primed responses from observed actions. Single-pulse transcranial magnetic stimulation was used to investigate corticospinal activity elicited during the observation of index- and little-finger actions before and after training (self-generated action). For sensorimotor training, participants executed finger movements with or without visual feedback of their own movement. Results showed that the increases in muscle-specific corticospinal activity elicited from action–observation persisted after training without visual feedback, but did not emerge following training with visual feedback. This inhibition in corticospinal activity during action–observation following training with vision could have resulted from the refining of internal models of self-generated action, which then led to a greater distinction between “self” and “other” actions.     

Reputation in an economic game modulates premotor cortex activity during action observation

Our interactions with other people – and our processing of their actions – are shaped by their reputation. Research has identified an Action Observation Network (AON) which is engaged when observing other people's actions. Yet, little is known about how the processing of others’ actions is influenced by another's reputation. Is the response of the AON modulated by the reputation of the actor? We developed a variant of the ultimatum game in which participants watched either the visible or occluded actions of two ‘proposers’. These actions were tied to decisions of how to split a pot of money although the proposers’ decisions on each trial were not known to participants when observing the actions. One proposer made fair offers on the majority of trials, establishing a positive reputation, whereas the other made predominantly, unfair offers resulting in a negative reputation. We found significant activations in two regions of the left dorsal premotor cortex (dPMC). The first of these showed a main effect of reputation with greater activation for the negative reputation proposer than the positive reputation proposer. Furthermore individual differences in trust ratings of the two proposers covaried with activation in the right primary motor cortex (M1). The second showed an interaction between visibility and reputation driven by a greater effect of reputation when participants were observing an occluded action. Our findings show that the processing of others’ actions in the AON is modulated by an actor's reputation, and suggest a predictive role for the PMC during action observation.     

Excitability changes in human corticospinal projections to muscles moving hand and fingers while viewing a reaching and grasping action

Excitability of the H-reflex in the relaxed flexor digitorum superficialis (FDS) muscle was tested in five subjects observing a reaching and grasping action. The amplitude of the FDS H-reflex was modulated with a peak occurring during the hand-opening phase of the observed movement. When the H-reflex was facilitated by subliminal transcranial magnetic stimulation (TMS), the modulation was larger than for an unconditioned reflex of similar size. This suggests that the primary motor cortex excitability is modulated by action viewing and reasonably causes the motoneuronal excitability changes. Moreover, motor evoked potentials (MEPs) were elicited by supraliminal TMS in FDS, flexor carpi radialis (FCR) and first dorsal interosseus (FDI) when observing the same movement. MEP amplitude was modulated in FDS with the same time-course as the H-reflex, the peak excitability occurring during hand opening. In FDI, however, the maximal excitability occurred during finger closing while in FCR no correlation was found with the movement phases. Finally the EMG activity of FCR, FDS and FDI was recorded while the subjects were actually performing a grasping movement similar to the one observed. In all subjects and for each muscle there was a clear-cut correspondence between the time-course of the excitability modulation of MEPs and the temporal pattern of EMG recruitment. In conclusion, the present study suggests that 'motor resonance' subliminally activates the same motor pathways that would be overtly recruited in each observer when actually performing the observed movement, reproducing the personal strategy adopted in the same task.     

Functional specificity of human premotor-motor cortical interactions during action selection

Functional connections between dorsal premotor cortex (PMd) and primary motor cortex (M1) have been revealed by paired-pulse transcranial magnetic stimulation (TMS). We tested if such connections would be modulated during a cognitive process (response selection) known to rely on those circuits. PMd-M1 TMS applied 75 ms after a cue to select a manual response facilitated motor-evoked potentials (MEPs). MEPs were facilitated at 50 ms in a control task of response execution, suggesting that PMd-M1 interactions at 75 ms are functionally specific to the process of response selection. At 100 ms, PMd-M1 TMS delayed choice reaction time (RT). Importantly, the MEP (at 75 ms) and the RT (at 100 ms) effects were correlated in a way that was hand-specific. When the response was made with the M1-contralateral hand, MEPs correlated with slower RTs. When the response was made with the M1-ipsilateral hand, MEPs correlated with faster RTs. Paired-pulse TMS confined to M1 did not produce these effects, confirming the causal influence of PMd inputs. This study shows that a response selection signal evolves in PMd early during the reaction period (75-100 ms), impacts on M1 and affects behaviour. Such interactions are temporally, anatomically and functionally specific, and have a causal role in choosing which movement to make.     

The essential role of Broca's area in imitation

The posterior sector of Broca's area (Brodmann area 44), a brain region critical for language, may have evolved from neurons active during observation and execution of manual movements. Imaging studies showing increased Broca's activity during execution, imagination, imitation and observation of hand movements support this hypothesis. Increased Broca's activity in motor task, however, may simply be due to inner speech. To test whether Broca's area is essential to imitation, we used repetitive transcranial magnetic stimulation (rTMS), which is known to transiently disrupt functions in stimulated areas. Subjects imitated finger key presses (imitation) or executed finger key presses in response to spatial cues (control task). While performing the tasks, subjects received rTMS over the left and right pars opercularis of the inferior frontal gyrus (where Brodmann area 44 is probabilistically located) and over the occipital cortex. There was significant impairment in imitation, but not in the control task, during rTMS over left and right pars opercularis compared to rTMS over the occipital cortex. This suggests that Broca's area is a premotor region essential to finger movement imitation.     

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.     

Lateralization of motor excitability during observation of bimanual signs

Viewing another person's hand actions enhances excitability in an observer's left and right primary motor (M1) cortex. We aimed to determine whether viewing communicative hand actions alters this bilateral sensorimotor resonance. Using single-pulse transcranial magnetic stimulation (TMS), we measured excitability in the left and right M1 while right-handed non-signing participants observed bimanual communicative hand actions, i.e., meaningful signs in British Sign Language. TMS-induced motor evoked potentials were recorded from hand muscles during sign observation before and after teaching the participants to associate meanings with half of the signs. Before this teaching, when participants did not know that the presented hand actions were signs, excitability of left and right M1 was modulated equally. After learning the meanings of half the signs, excitability of the left, but not right, M1 was significantly enhanced. This left-lateralized enhancement of M1 excitability occurred during observation of signs with known and unknown meanings. The findings suggest that awareness of the communicative nature of another person's hand actions strengthens sensorimotor resonance in the left M1 cortex and alters hemispheric balance during action observation.     

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.     

Modulation of spinal excitability during observation of hand actions in humans

There is growing evidence that observation of actions performed by other individuals activates observer's cortical motor areas. This matching of observed actions on the observer's motor repertoire could be at the basis of action recognition. Here we investigated if action observation, in addition to cortical motor areas, involves also low level motor structures mimicking the observed actions as if they were performed by the observer. Spinal cord excitability was tested by eliciting the H-reflex in a finger flexor muscle (flexor digitorum superficialis) in humans looking at goal-directed hand actions presented on a TV screen. We found that, in the absence of any detectable muscle activity, there was in the observers a significant modulation of the monosynaptic reflex size, specifically related to the different phases of the observed movement. The recorded H-reflex rapidly increased in size during hand opening, it was depressed during hand closing and quickly recovered during object lifting. This modulation pattern is, however, opposite to that occurring when the recorded muscles are actually executing the observed action [Lemon et al. (1995) J. Neurosci., 15, 6145-56]. Considering that, when investigated at cortical level the modulation pattern of corticospinal excitability replicates the observed movements [Fadiga et al. (1995) J. Neurophysiol., 73, 2608-2611], this spinal 'inverted mirror' behaviour might be finalised to prevent the overt replica of the seen action.