Action processing in the motor system: Transcranial Magnetic Stimulation (TMS) evidence of shared mechanisms in the visual and linguistic modalities.

In two experiments, we compared the dynamics of corticospinal excitability when processing visually or linguistically presented tool-oriented hand actions in native speakers and sequential bilinguals. In a third experiment we used the same procedure to test non-motor, low-level stimuli, i.e. scrambled images and pseudo-words. Stimuli were presented in sequence: pictures (tool + tool-oriented hand action or their scrambled counterpart) and words (tool noun + tool-action verb or pseudo-words). Experiment 1 presented German linguistic stimuli to native speakers, while Experiment 2 presented English stimuli to non-natives. Experiment 3 tested Italian native speakers. Single-pulse trascranial magnetic stimulation (spTMS) was applied to the left motor cortex at five different timings: baseline, 200 ms after tool/noun onset, 150, 350 and 500 ms after hand/verb onset with motor-evoked potentials (MEPs) recorded from the first dorsal interosseous (FDI) and abductor digiti minimi (ADM) muscles. We report strong similarities in the dynamics of corticospinal excitability across the visual and linguistic modalities. MEPs' suppression started as early as 150 ms and lasted for the duration of stimulus presentation (500 ms). Moreover, we show that this modulation is absent for stimuli with no motor content. Overall, our study supports the notion of a core, overarching system of action semantics shared by different modalities.

The embodiment of language in tremor-dominant Parkinson's disease patients.

According to embodied cognition, processing language with motor content involves a simulation of this content by the brain motor system. Patients with brain lesions involving the motor system are characterized by deficits in action verbs processing in the absence of dementia. We sought to assess whether action verbs interfere with the motor behavior of patients with Parkinson's disease (PD) having tremor dominant symptoms. PD tremor is considered to result from dysfunction of cortical-subcortical motor circuits driven by dopamine depletion. In addition, PD tremor is reduced during active movement execution. Therefore, likewise movement execution, the motor simulation of bodily actions predicted by the embodiment may show to be effective in modifying tremor by interfering with a dysfunctional motor system. Here, we asked to simply read and repeat words expressing a hand-related bodily action. Abstract verbs served as control. Changes in tremor kinematics were evaluated using a monoaxial accelerometer. Seventeen PD patients with rest tremor of the upper limbs were enrolled. Tremor amplitude was significantly smaller when reading action verbs as compared to abstract verbs. We provide empirical evidence supporting the embodied cognition theory by showing that circuits mediating tremor of PD patients are distinctively affected by processing action language.

To me or to you? When the self is advantaged.

The present study aimed at verifying whether and why sequences of actions directed to oneself are facilitated when compared to action sequences directed to conspecifics. In experiment 1, participants reached to grasp and brought a piece of food either to their own mouth for self-feeding or to the mouth of a conspecific for feeding. In control conditions, they executed the same sequence to place the piece of food into a mouth-like aperture in a flat container placed upon either their own mouth or the mouth of a conspecific. Kinematic analysis showed that the actions of reaching and bringing were faster when directed to the participant's own body, especially for self-feeding. The data support the hypothesis that reaching to grasp and bringing to one's own body and, in particular, one's own mouth for self-feeding, form an automatic sequence, because this is the result of more frequent execution and coordination between different effectors of one's own body, such as arm and mouth. In contrast, the same sequence directed toward a conspecific is not automatic and requires more accuracy probably because it is guided by social intentions. This hypothesis was supported by the results of control experiment 2 in which we compared the kinematics of reaching to grasp and placing the piece of food into the mouth of a conspecific (i.e. feeding) with those of reaching to grasp and placing the same piece of food into a mouth-like aperture in a human body shape (i.e. placing). Indeed, the entire sequence was slowed down during feeding when compared to placing.

Action word understanding and overt motor behavior.

Is the motor system involved in language processing? In order to clarify this issue, we carried out three behavioral experiments, using go-no-go and choice paradigms. In all the experiments, we used a semantic decision task with an early delivery of the go signal (during processing language material). Italian verbs expressing hand actions, foot actions or an abstract content served as stimuli. Participants executed intransitive (Experiment 1) or transitive (Experiment 2) actions with their right hand in response to the acoustic presentation of action-related verbs and refrained from responding to abstract verbs. The kinematics of the actions was slowed down by hand action-related verbs when compared with foot action-related verbs. In Experiment 3, hand-related and foot-related verbs were presented. Participants responded to hand-related and foot-related verbs with their hand and their foot (compatible condition) and in another block of trials they responded to hand-related and foot-related verbs with their foot and their hand (incompatible condition), respectively. In the compatible condition, the beginning of the action was faster, whereas the kinematics of the action was slower. The present findings suggest complete activation of verb-related motor programs during language processing. The data are discussed in support of the hypothesis that this complete activation is necessary requisite to understand the exact meaning of action words because goal and consequence of the actions are represented.

When the hands speak.

In the present review we will summarize evidence that the control of spoken language shares the same system involved in the control of arm gestures. Studies of primate premotor cortex discovered the existence of the so-called mirror system as well as of a system of double commands to hand and mouth. These systems may have evolved initially in the context of ingestion, and later formed a platform for combined manual and vocal communication. In humans, manual gestures are integrated with speech production, when they accompany speech. Lip kinematics and parameters of voice spectra during speech production are influenced by executing or observing transitive actions (i.e. guided by an object). Manual actions also play an important role in language acquisition in children, from the babbling stage onwards. Behavioural data reported here even show a reciprocal influence between words and symbolic gestures and studies employing neuroimaging and repetitive transcranial magnetic stimulation (rTMS) techniques suggest that the system governing both speech and gesture is located in Broca's area.

Automatic grasp imitation following action observation affects estimation of intrinsic object properties.

The present study aimed to determine whether the observation of different grasps of the same object elicits automatic imitation of the kinematics of those grasps and this process influences the estimation of intrinsic target properties. In experiments 1 and 2, participants reached and grasped differently sized spheres after observation of the same objects grasped using two different types of grasp (power and precision grasp) and hand kinematics. The observed grasp kinematics were imitated especially when the vision of the target and the acting hand were precluded. In experiments 3, 4 and 5 participants matched the diameter of the spheres, either perceived or imagined, by opening their thumb and index finger (i.e. the fingers used to grasp the objects) after observation of the two types of grasp. Finger opening was larger after observation of power grasp than precision grasp, consistently with the notion that power grasp and precision grasp are preferentially used to grasp large and small objects, respectively. However, the effect was poorly observed for the small object, this depending on the fact that the participants imitated also the final position of the thumb and index finger, which were closer to each other in the power grasp. Finally, those participants, for whom the effect was stronger, reported to have perceived more differently sized objects than those really presented. The results suggest that imitation evoked by a mirror system is involved in planning how to interact with an object and in the estimation of the properties extracted for sensory-motor integration.

From meaning to categorization: The hierarchical recruitment of brain circuits selective for action verbs.

Sensorimotor and affective brain systems are known to be involved in language processing. However, to date it is still debated whether this involvement is a crucial step of semantic processing or, on the contrary, it is dependent on the specific context or strategy adopted to solve a task at hand. The present electroencephalographic (EEG) study is aimed at investigating which brain circuits are engaged when processing written verbs. By aligning event-related potentials (ERPs) both to the verb onset and to the motor response indexing the accomplishment of a semantic task of categorization, we were able to dissociate the relative stimulus-related and response-related cognitive components at play, respectively. EEG signal source reconstruction showed that while the recruitment of sensorimotor fronto-parietal circuits was time-locked with action verb onset, a left temporal-parietal circuit was time-locked to the task accomplishment. Crucially, by comparing the time course of both these bottom-up and top-down cognitive components, it appears that the frontal motor involvement precedes the task-related temporal-parietal activity. The present findings suggest that the recruitment of fronto-parietal sensorimotor circuits is independent of the specific strategy adopted to solve a semantic task and, given its temporal hierarchy, it may provide crucial information to brain circuits involved in the categorization task. Eventually, a discussion on how the present results may contribute to the clinical literature on patients affected by disorders specifically impairing the motor system is provided.

Processing graspable object images and their nouns is impaired in Parkinson's disease patients.

According to embodiment, the recruitment of the motor system is necessary to process language material expressing a motor content. Coherently, an impairment of the motor system should affect the capacity to process language items with a motor content. The aim of the present study was to assess the capacity to process graspable objects and their nouns in Parkinson's disease (PD) patients and healthy controls. Participants saw photos and nouns depicting graspable and non-graspable objects. Scrambled images and pseudo-words served as control stimuli. At 150 msec after stimulus presentation, they had to respond when the stimulus referred to a real object, and refrain from responding when it was meaningless (go-no go paradigm). In the control group, participants gave slower motor responses for stimuli (both photos and nouns) related to graspable objects as compared to non-graspable ones. This in keeping with data obtained in a previous study with young healthy participants. In the PD group, motor responses were similar for both graspable and non-graspable items. Moreover, error number was significantly greater than in controls. These findings support the notion that when the motor circuits are lesioned, like in PD, patients do not show the typical modulation of motor responses and have troubles in processing graspable objects and their nouns.

Walking indoors, walking outdoors: an fMRI study.

An observation/execution matching system for walking has not been assessed yet. The present fMRI study was aimed at assessing whether, as for object-directed actions, an observation/execution matching system is active for walking and whether the spatial context of walking (open or narrow space) recruits different neural correlates. Two experimental conditions were employed. In the execution condition, while being scanned, participants performed walking on a rolling cylinder located just outside the scanner. The same action was performed also while observing a video presenting either an open space (a country field) or a narrow space (a corridor). In the observation condition, participants observed a video presenting an individual walking on the same cylinder on which the actual action was executed, the open space video and the narrow space video, respectively. Results showed common bilateral activations in the dorsal premotor/supplementary motor areas and in the posterior parietal lobe for both execution and observation of walking, thus supporting a matching system for this action. Moreover, specific sectors of the occipital-temporal cortex and the middle temporal gyrus were consistently active when processing a narrow space versus an open one, thus suggesting their involvement in the visuo-motor transformation required when walking in a narrow space. We forward that the present findings may have implications for rehabilitation of gait and sport training.

Does listening to action-related sentences modulate the activity of the motor system? Replication of a combined TMS and behavioral study.

The neurophysiological and behavioral correlates of action-related language processing have been debated for long time. A precursor in this field was the study by Buccino et al. (2005) combining transcranial magnetic stimulation (TMS) and behavioral measures (reaction times, RTs) to study the effect of listening to hand- and foot-related sentences. In the TMS experiment, the authors showed a decrease of motor evoked potentials (MEPs) recorded from hand muscles when processing hand-related verbs as compared to foot-related verbs. Similarly, MEPs recorded from leg muscles decreased when participants processed foot-related as compared to hand-related verbs. In the behavioral experiment, using the same stimuli and a semantic decision task the authors found slower RTs when the participants used the body effector (hand or foot) involved in the actual execution of the action expressed by the presented verb to give their motor responses. These findings were interpreted as an interference effect due to a simultaneous involvement of the motor system in both a language and a motor task. Our replication aimed to enlarge the sample size and replicate the findings with higher statistical power. The TMS experiment showed a significant modulation of hand MEPs, but in the sense of a motor facilitation when processing hand-related verbs. On the contrary, the behavioral experiment did not show significant results. The results are discussed within the general debate on the time-course of the modulation of motor cortex during implicit and explicit language processing and in relation to the studies on action observation/understanding.

Spatiotemporal dynamics during processing of abstract and concrete verbs: an ERP study.

Different accounts have been proposed to explain the nature of concept representations. Embodied accounts claim a key involvement of sensory-motor systems during semantic processing while more traditional accounts posit that concepts are abstract mental entities independent of perceptual and motor brain systems. While the involvement of sensory-motor areas in concrete language processing is supported by a large number of studies, this involvement is far from being established when considering abstract language. The present study addressed abstract and concrete verb processing, by investigating the spatiotemporal dynamics of evoked responses by means of high density EEG while participants performed a semantic decision task. In addition, RTs to the same set of stimuli were collected. In both early and late time intervals, ERP scalp topography significantly differed according to word categories. Concrete verbs showed involvement of parieto-frontal networks for action, according to the implied body effector. In contrast, abstract verbs recruited mostly frontal regions outside the motor system, suggesting a non-motor semantic processing for this category. In addition, differently from what has been reported during action observation, the parietal recruitment related to concrete verbs presentation followed the frontal one. The present findings suggest that action word semantic is grounded in sensory-motor systems, provided a bodily effector is specified, while abstract concepts׳ representation cannot be easily explained by a motor embodiment.

The dynamics of sensorimotor cortical oscillations during the observation of hand movements: an EEG study.

BACKGROUND: The observation of action done by others determines a desynchronization of the rhythms recorded from cortical central regions. Here, we examined whether the observation of different types of hand movements (target directed, non-target directed, cyclic and non-cyclic) elicits different EEG cortical temporal patterns. METHODOLOGY: Video-clips of four types of hand movements were shown to right-handed healthy participants. Two were target directed (grasping and pointing) motor acts; two were non-target directed (supinating and clenching) movements. Grasping and supinating were performed once, while pointing and clenching twice (cyclic movements). High-density EEG was recorded and analyzed by means of wavelet transform, subdividing the time course in time bins of 200 ms. The observation of all presented movements produced a desynchronization of alpha and beta rhythms in central and parietal regions. The rhythms desynchronized as soon as the hand movement started, the nadir being reached around 700 ms after movement onset. At the end of the movement, a large power rebound occurred for all bands. Target and non-target directed movements produced an alpha band desynchronization in the central electrodes at the same time, but with a stronger desynchronization and a prolonged rebound for target directed motor acts. Most interestingly, there was a clear correlation between the velocity profile of the observed movements and beta band modulation. SIGNIFICANCE: Our data show that the observation of motor acts determines a modulation of cortical rhythm analogous to that occurring during motor act execution. In particular, the cortical motor system closely follows the velocity of the observed movements. This finding provides strong evidence for the presence in humans of a mechanism (mirror mechanism) mapping action observation on action execution motor programs.

Social requests and social affordances: how they affect the kinematics of motor sequences during interactions between conspecifics.

The present study aimed at determining whether and what factors affect the control of motor sequences related to interactions between conspecifics. Experiment 1 demonstrated that during interactions between conspecifics guided by the social intention of feeding, a social affordance was activated, which modified the kinematics of sequences constituted by reaching-grasping and placing. This was relative to the same sequence directed to an inanimate target. Experiments 2 and 4 suggested that the related-to-feeding social request emitted by the receiver (i.e. the request gesture of mouth opening) is prerequisite in order to activate a social affordance. Specifically, the two experiments showed that the social request to be fed activated a social affordance even when the sequences directed towards a conspecific were not finalized to feed. Experiment 3 showed that moving inside the peripersonal space of a conspecific, who did not produce any social request, marginally affected the sequence. Finally, experiments 5 and 6 indicated that the gaze of a conspecific is necessary to make a social request effective at activating a social affordance. Summing up, the results of the present study suggest that the control of motor sequences can be changed by the interaction between giver and receiver: the interaction is characterized by a social affordance that the giver activates on the basis of social requests produced by the receiver. The gaze of the receiver is a prerequisite to make a social request effective.

The observation of manual grasp actions affects the control of speech: a combined behavioral and Transcranial Magnetic Stimulation study.

Does the mirror system affect the control of speech? This issue was addressed in behavioral and Transcranial Magnetic Stimulation (TMS) experiments. In behavioral experiment 1, participants pronounced the syllable /da/ while observing (1) a hand grasping large and small objects with power and precision grasps, respectively, (2) a foot interacting with large and small objects and (3) differently sized objects presented alone. Voice formant 1 was higher when observing power as compared to precision grasp, whereas it remained unaffected by observation of the different types of foot interaction and objects alone. In TMS experiment 2, we stimulated hand motor cortex, while participants observed the two types of grasp. Motor Evoked Potentials (MEPs) of hand muscles active during the two types of grasp were greater when observing power than precision grasp. In experiments 3-5, TMS was applied to tongue motor cortex of participants silently pronouncing the syllable /da/ and simultaneously observing power and precision grasps, pantomimes of the two types of grasps, and differently sized objects presented alone. Tongue MEPs were greater when observing power than precision grasp either executed or pantomimed. Finally, in TMS experiment 6, the observation of foot interaction with large and small objects did not modulate tongue MEPs. We hypothesized that grasp observation activated motor commands to the mouth as well as to the hand that were congruent with the hand kinematics implemented in the observed type of grasp. The commands to the mouth selectively affected postures of phonation organs and consequently basic features of phonological units.

Spoken language and arm gestures are controlled by the same motor control system.

Arm movements can influence language comprehension much as semantics can influence arm movement planning. Arm movement itself can be used as a linguistic signal. We reviewed neurophysiological and behavioural evidence that manual gestures and vocal language share the same control system. Studies of primate premotor cortex and, in particular, of the so-called "mirror system", including humans, suggest the existence of a dual hand/mouth motor command system involved in ingestion activities. This may be the platform on which a combined manual and vocal communication system was constructed. In humans, speech is typically accompanied by manual gesture, speech production itself is influenced by executing or observing transitive hand actions, and manual actions play an important role in the development of speech, from the babbling stage onwards. Behavioural data also show reciprocal influence between word and symbolic gestures. Neuroimaging and repetitive transcranial magnetic stimulation (rTMS) data suggest that the system governing both speech and gesture is located in Broca's area. In general, the presented data support the hypothesis that the hand motor-control system is involved in higher order cognition.

Repetitive transcranial magnetic stimulation of Broca's area affects verbal responses to gesture observation.

The aim of the present study was to determine whether Broca's area is involved in translating some aspects of arm gesture representations into mouth articulation gestures. In Experiment 1, we applied low-frequency repetitive transcranial magnetic stimulation over Broca's area and over the symmetrical loci of the right hemisphere of participants responding verbally to communicative spoken words, to gestures, or to the simultaneous presentation of the two signals. We performed also sham stimulation over the left stimulation loci. In Experiment 2, we performed the same stimulations as in Experiment 1 to participants responding with words congruent and incongruent with gestures. After sham stimulation voicing parameters were enhanced when responding to communicative spoken words or to gestures as compared to a control condition of word reading. This effect increased when participants responded to the simultaneous presentation of both communicative signals. In contrast, voicing was interfered when the verbal responses were incongruent with gestures. The left stimulation neither induced enhancement on voicing parameters of words congruent with gestures nor interference on words incongruent with gestures. We interpreted the enhancement of the verbal response to gesturing in terms of intention to interact directly. Consequently, we proposed that Broca's area is involved in the process of translating into speech aspects concerning the social intention coded by the gesture. Moreover, we discussed the results in terms of evolution to support the theory [Corballis, M. C. (2002). From hand to mouth: The origins of language. Princeton, NJ: Princeton University Press] proposing spoken language as evolved from an ancient communication system using arm gestures.