Motor Resonance Research Articles

First and Second Language at Hand: A Chronometric Transcranial-Magnetic Stimulation Study on Semantic and Motor Resonance

According to embodied theories, motor and language processing bidirectionally interact: Motor activation modulates behavior in lexico-semantic tasks (semantic resonance), and understanding motor-related words entails activation of the corresponding motor brain areas (motor resonance). Whereas many studies investigated such interaction in the first language (L1), only few did so in a second language (L2), focusing on motor resonance. Here, we directly compared L1 and a late L2, for the first time both in terms of semantic and motor resonance and both in terms of magnitude and timing, by taking advantage of single-pulse TMS. Twenty-five bilinguals judged, in each language, whether hand motor-related ("grasp") and non-motor-related verbs ("believe"), were physical or mental. Meanwhile, we applied TMS on the hand motor cortex at 125, 275, 350, and 500 msec post verb onset, and recorded behavioral responses and TMS-induced motor evoked potentials. TMS induced faster responses for L1 versus L2 motor and nonmotor verbs at 125 msec (three-way interaction β = -0.0442, 95% CI [0.0814, -0.0070]), showing a semantic resonance effect at an early stage of word processing in L1 but not in L2. Concerning motor resonance, TMS-induced motor evoked potentials at 275 msec revealed higher motor cortex excitability for L2 versus L1 processing (two-way interaction β = 0.095, 95% CI [0.017, 0.173]). These findings confirm action-language interaction at early stages of word recognition, provide further evidence that L1 and L2 are differently embodied, and call for an update of existing models of bilingualism and embodiment, concerning both language representations and processing.

Visual Attention and Motion Visibility Modulate Motor Resonance during Observation of Human Walking in Different Manners.

To advance our knowledge on the motor system during cyclic gait observation, we aimed to explore the effects of gaze fixation on corticospinal excitability evaluated by single-pulse transcranial magnetic stimulation (TMS). Fourteen healthy adult volunteers watched a video of a demonstrator walking on a treadmill under three different conditions: (1) observing the right lower limb, (2) observing the right ankle joint, and (3) observing the right lower limb on a video focused on the area below the knee. In each condition, motor-evoked potentials elicited by TMS in the tibialis anterior (TA) muscle were measured synchronously with the demonstrator’s initial contact and toe-off points. Directing visual attention to the ankle joint and focusing on its movements caused corticospinal facilitation in the TA muscle compared with watching the video without any visual fixation. In addition, phase-dependent differences in corticospinal excitability between the initial contact and toe-off points were only detected when the visibility range was restricted to below the knee. Our findings indicated that motor resonance during cyclic gait observation is modulated by visual attention and motion visibility in different activation manners.

Does agency matter? Neural processing of robotic movements in 4- and 8-year olds

Despite the increase in interactions between children and robots, our understanding of children's neural processing of robotic movements is limited. The current study theorized that motor resonance hinges on the agency of an actor: its ability to perform actions volitionally. As one of the first studies with a cross-sectional sample of preschoolers and older children and with a specific focus on robotic action (rather than abstract non-human action), the current study investigated whether the perceived agency of a robot moderated children's motor resonance for robotic movements, and whether this changed with age. Motor resonance was measured using electroencephalography (EEG) by assessing mu power while 4 and 8-year-olds observed actions performed by agentic versus non-agentic robots and humans. Results show that older children resonated more strongly with non-agentic than agentic robotic or human movement, while no such differences were found for preschoolers. This outcome is discussed in terms of a predictive coding account of motor resonance. Importantly, these findings contribute to the existing set of studies on this topic by showing that, while keeping all kinematic information constant, there is a clear developmental difference in how children process robotic movement depending on the level of agency of a robot.

Motor resonance is modulated by an object's weight distribution

Transcranial magnetic stimulation (TMS) studies showed that corticospinal excitability (CSE) is modulated during observation of object lifting, an effect termed ‘motor resonance’. Specifically, motor resonance is driven by movement features indicating object weight, such as object size or observed movement kinematics. We investigated in 16 humans (8 females) whether motor resonance is also modulated by an object's weight distribution. Participants were asked to lift an inverted T-shaped manipulandum with interchangeable center of mass after first observing an actor lift the same manipulandum. Participants and actor were instructed to minimize object roll and rely on constrained digit positioning during lifting. Constrained positioning was either collinear (i.e., fingertips on the same height) or noncollinear (i.e., fingertip on the heavy side higher than the one on the light side). The center of mass changed unpredictably before the actor's lifts and participants were explained that their weight distribution always matched the actor's one. Last, TMS was applied during both lift observation and planning of lift actions. Our results showed that CSE was similarly modulated during lift observation and planning: when participants observed or planned lifts in which the weight distribution was asymmetrically right-sided, CSE recorded from the thumb muscles was significantly increased compared to when the weight distribution was left-sided. During both lift observation and planning, this increase seemed to be primarily driven by the weight distribution and not specifically by the (observed) digit positioning or muscle contraction. In conclusion, our results indicate that complex intrinsic object properties such as weight distributions can modulate activation of the motor system during both observation and planning of lifting actions.

Interplay of self-other distinction and cognitive control mechanisms in a social automatic imitation task: An ERP study.

The regulation of motor resonance processes in daily life is indispensable. The automatic imitation task is an experimental model of those daily-life motor resonance processes. Recent research suggests that both self-other distinction and cognitive control processes may be involved in interference control during automatic imitation. Yet, we lack a clear understanding of the chronological sequence of interacting processes. To this end, this study used event-related potentials (ERPs) to investigate the time course underlying interference control during automatic imitation. We moreover aimed to extend previous results by investigating its modulation by social context. Cognitive conflict/action monitoring was assessed with the N2, in an exploratory manner the N450, and the CRN components. The Pre-Motor Positivity (PMP), associated with movement initiation, was suggested as a possible correlate of the successful resolution of self-other distinction. The cognitive control/action monitoring ERP components were influenced by the social context manipulation and partly by congruency, while PMP amplitudes were only sensitive to congruency. In addition, the exploratorily investigated N450 component predicted response times on incongruent relative to congruent trials in the different social contexts. This suggested that cognitive control/action monitoring processes, reflected in the N450, are guiding behavioral outcomes. Overall, interference control may primarily be guided by processes of cognitive control/action monitoring, whilst being modulated by social context demands.

A Review of The Rise of the Australian Neurohumanities

A Review of <i>The Rise of the Australian Neurohumanities</i>

Modulation of Response Times During Processing of Emotional Body Language.

The investigation of how humans perceive and respond to emotional signals conveyed by the human body has been for a long time secondary compared with the investigation of facial expressions and emotional scenes recognition. The aims of this behavioral study were to assess the ability to process emotional body postures and to test whether motor response is mainly driven by the emotional content of the picture or if it is influenced by motor resonance. Emotional body postures and scenes (IAPS) divided into three clusters (fear, happiness, and neutral) were shown to 25 healthy subjects (13 males, mean age ± SD: 22.3 ± 1.8 years) in a three-alternative forced choice task. Subjects were asked to recognize the emotional content of the pictures by pressing one of three keys as fast as possible in order to estimate response times (RTs). The rating of valence and arousal was also performed. We found shorter RTs for fearful body postures as compared with happy and neutral postures. In contrast, no differences across emotional categories were found for the IAPS stimuli. Analysis on valence and arousal and the subsequent item analysis showed an excellent reliability of the two sets of images used in the experiment. Our results show that fearful body postures are rapidly recognized and processed, probably thanks to the automatic activation of a series of central nervous system structures orchestrating the defensive threat reactions, strengthening and supporting previous neurophysiological and behavioral findings in body language processing.

Social Cognitive Networks and Social Cognitive Performance Across Individuals With Schizophrenia Spectrum Disorders and Healthy Control Participants

BackgroundSchizophrenia spectrum disorders (SSDs) feature social cognitive deficits, although their neural basis remains unclear. Social cognitive performance may relate to neural circuit activation patterns more than to diagnosis, which would have important prognostic and therapeutic implications. The current study aimed to determine how functional connectivity within and between social cognitive networks relates to social cognitive performance across individuals with SSDs and healthy control participants. MethodsParticipants with SSDs (n = 164) and healthy control participants (n = 117) completed the Empathic Accuracy task during functional magnetic resonance imaging as well as lower-level (e.g., emotion recognition) and higher-level (e.g., theory of mind) social cognitive measures outside the scanner. Functional connectivity during the Empathic Accuracy task was analyzed using background connectivity and graph theory. Data-driven social cognitive networks were identified across participants. Regression analyses were used to examine network connectivity–performance relationships across individuals. Positive and negative within- and between-network connectivity strengths were also compared in poor versus good social cognitive performers and in SSD versus control groups. ResultsThree social cognitive networks were identified: motor resonance, affect sharing, and mentalizing. Regression and group-based analyses demonstrated reduced between-network negative connectivity, or segregation, and greater within- and between-network positive connectivity in worse social cognitive performers. There were no significant effects of diagnostic group on within- or between-network connectivity. ConclusionsThese findings suggest that the neural circuitry of social cognitive performance may exist dimensionally. Across participants, better social cognitive performance was associated with greater segregation between social cognitive networks, whereas poor versus good performers may compensate via hyperconnectivity within and between social cognitive networks.

Implicit visual sensitivity towards slim versus overweight bodies modulates motor resonance in the primary motor cortex: A tDCS study

Motor resonance (MR) can be influenced by individual differences and similarity in the physical appearance between the actor and observer. Recently, we reported that action simulation is modulated by an implicit visual sensitivity towards normal-weight compared with overweight bodies. Furthermore, recent research has suggested the existence of an action observation network responsible for MR, with limited evidence whether the primary motor cortex (M1) is part of this. We expanded our previous findings with regards to the role of an implicit normal-weight-body preference in the MR mechanism. At the same time, we tested the functional relevance of M1 to MR, by using a transcranial direct current stimulation (tDCS) protocol. Seventeen normal-weight and 17 overweight participants were asked to observe normal-weight or overweight actors reaching and grasping a light or heavy cube, and then, at the end of each video-clip to indicate the correct cube weight. Before the task, all participants received 15 min of sham or cathodal tDCS over the left M1. Measures of anti-fat attitudes were also collected. During sham tDCS, all participants were better in simulating the actions performed by normal-weight compared with overweight models. Surprisingly, cathodal tDCS selectively improved the ability in the overweight group to simulate actions performed by the overweight models. This effect was not associated with scores of fat phobic attitudes or implicit anti-fat bias. Our findings are discussed in the context of relevance of M1 to MR and its social modulation by anti-fat attitudes.

Modulation of corticospinal excitability during paintings viewing: A TMS study

It has been hypothesized that embodied mechanisms encompassing the simulation of actions, emotions and corporeal sensations contribute to aesthetic appreciation of art. In line with this, in this study we assessed whether there is a relationship between the extent to which an artwork triggers motor resonance mechanisms and liking for the artwork. To this aim, we measured motor evoked potentials (MEPs) induced by TMS over M1 whilst participants viewed a series of paintings depicting either humans in static postures or performing dynamic actions, and paintings depicting static or dynamic non-human scenes. Following recording of MEPs, participants indicated how much they liked each painting and found the painting to be dynamic. Viewing of paintings depicting dynamic human actions was associated with a significant increase in MEPs size compared to baseline and to viewing of the other paintings. The more the painting conveyed the impression of a dynamic human action, the higher the MEPs amplitude and the more the artwork was liked. However, liking per se was not related to MEPs size. In fact, the positive relationship between MEPs size and preference for paintings depicting humans was entirely mediated by the perceived dynamism of the portrayed actions, and no positive relationship was observed between subjective preference for paintings depicting landscapes/objects and MEPs size. Overall, our data contribute to shed light on the possible role of embodied resonance mechanisms in aesthetic appreciation of visual art, and show that characterization of motor cortical excitability may serve as a promising approach in neuroaesthetics.

Proactive gaze is present during biological and non-biological motion observation

Others' action observation activates in the observer a coordinated hand-eye motor program, covert for the hand (i.e. motor resonance), and overt for the eye (i.e. proactive gaze), similar to that of the observed agent. The biological motion hypothesis of action anticipation claims that proactive gaze occurs only in the presence of biological motion, and that kinematic information is sufficient to determine the anticipation process. The results of the present study did not support the biological motion hypothesis of action anticipation. Specifically, proactive gaze was present during observation of both a biological accelerated-decelerated motion and a non-biological constant velocity motion (Experiment 1), in the presence of a barrier able to restrict differences between the two kinematics to the motion profile of individual markers prior to contact (Experiment 2), but only if an object was present at the end point of the movement trajectory (Experiment 3). Furthermore, proactive gaze was found independently of the presence of end effects temporally congruent with the instant in which the movement stopped (Experiments 4, and 5). We propose that the involvement of the observer's motor system is not restricted to when the agent moves with natural kinematics, and it is mandatory whenever the presence of an agent or a goal is evident, regardless of physical appearance, natural kinematics, and the possibility to identify the action behind the stimulus.

Motor resonance in monkey parietal and premotor cortex during action observation: Influence of viewing perspective and effector identity

Observing others performing motor acts like grasping has been shown to elicit neural responses in the observer`s parieto-frontal motor network, which typically becomes active when the observer would perform these actions him/herself. While some human studies suggested strongest motor resonance during observation of first person or egocentric perspectives compared to third person or allocentric perspectives, other research either report the opposite or did not find any viewpoint-related preferences in parieto-premotor cortices. Furthermore, it has been suggested that these motor resonance effects are lateralized in the parietal cortex depending on the viewpoint and identity of the observed effector (left vs right hand). Other studies, however, do not find such straightforward hand identity dependent motor resonance effects. In addition to these conflicting findings in human studies, to date, little is known about the modulatory role of viewing perspective and effector identity (left or right hand) on motor resonance effects in monkey parieto-premotor cortices. Here, we investigated the extent to which different viewpoints of observed conspecific hand actions yield motor resonance in rhesus monkeys using fMRI. Observing first person, lateral and third person viewpoints of conspecific hand actions yielded significant activations throughout the so-called action observation network, including STS, parietal and frontal cortices. Although region-of-interest analysis of parietal and premotor motor/mirror neuron regions AIP, PFG and F5, showed robust responses in these regions during action observation in general, a clear preference for egocentric or allocentric perspectives was not evident. Moreover, except for lateralized effects due to visual field biases, motor resonance in the monkey brain during grasping observation did not reflect hand identity dependent coding.

Do gaze behaviours during action observation predict interpersonal motor resonance?

Interpersonal motor resonance (IMR) is a common putative index of the mirror neuron system (MNS), a network containing specialised cells that fire during both action execution and observation. Visual content inputs to the MNS, however, it is unclear whether visual behaviours mediate the putative MNS response. We aimed to examine gaze effects on IMR during action observation. Neurotypical adults (N = 99; 60 female) underwent transcranial magnetic stimulation, electromyography, and eye-tracking during the observation of videos of actors performing grasping actions. IMR was measured as a percentage change in motor evoked potentials (MEPs) of the first dorsal interosseous muscle during action observation relative to baseline. MEP facilitation was observed during action observation, indicating IMR (65.43%, SE = 11.26%, P < 0.001). Fixations occurring in biologically relevant areas (face/hand/arm) yielded significantly stronger IMR (81.03%, SE = 14.15%) than non-biological areas (63.92%, SE = 14.60, P = 0.012). This effect, however, was only evident in the first of four experimental blocks. Our results suggest that gaze fixation can modulate IMR, but this may be affected by the salience and novelty of the observed action. These findings have important methodological implications for future studies in both clinical and healthy populations.

Reconceptualizing mirroring: Sound imitation and rapport in naturally occurring interaction

This study interrogates the frequently made claim that mirroring behavior is directly linked to interpersonal rapport. The paper proposes a more nuanced conceptualization of the positive effect of mirroring, showing it to be underpinning not affiliation as such but instead speakers' joint commitment to a common interactional cause. The analysis of naturally occurring talk shows that sound imitation is primarily an affiliation-neutral resource that facilitates the progression of interaction. The paper argues that socially embedded mirroring behavior is more than a behavioral manifestation of the motor resonance described in social neuroscience. Mirroring as part of jointly achieved talk is one of several mechanisms for conversational participants to establish progressivity, that is, trajectories of social action, sequence and stance. The data also show that sound mirroring, when it is part of naturally occurring interaction, is not automatic, but that participants choose to mirror, or not. It is proposed that socially situated imitation is reconceptualized as facilitating social collaboration and the joint achievement of interaction more broadly, rather than empathy or rapport in a narrow sense. Such a reconceptualization of mirroring allows us to describe more accurately how humans build sociality.

Sensorimotor Expectations Bias Motor Resonance during Observation of Object Lifting: The Causal Role of pSTS.

Transcranial magnetic stimulation studies have highlighted that corticospinal excitability is increased during observation of object lifting, an effect termed "motor resonance." This facilitation is driven by movement features indicative of object weight, such as object size or observed movement kinematics. Here, we investigated in 35 humans (23 females) how motor resonance is altered when the observer's weight expectations, based on visual information, do not match the actual object weight as revealed by the observed movement kinematics. Our results highlight that motor resonance is not robustly driven by object weight but easily masked by a suppressive mechanism reflecting the correctness of weight expectations. Subsequently, we investigated in 24 humans (14 females) whether this suppressive mechanism was driven by higher-order cortical areas. For this, we induced "virtual lesions" to either the posterior superior temporal sulcus (pSTS) or dorsolateral prefrontal cortex (DLPFC) before having participants perform the task. Importantly, virtual lesion of pSTS eradicated this suppressive mechanism and restored object weight-driven motor resonance. In addition, DLPFC virtual lesion eradicated any modulation of motor resonance. This indicates that motor resonance is heavily mediated by top-down inputs from both pSTS and DLPFC. Together, these findings shed new light on the theorized cortical network driving motor resonance. That is, our findings highlight that motor resonance is not only driven by the putative human mirror neuron network consisting of the primary motor and premotor cortices as well as the anterior intraparietal sulcus, but also by top-down input from pSTS and DLPFC.SIGNIFICANCE STATEMENT Observation of object lifting activates the observer's motor system in a weight-specific fashion: Corticospinal excitability is larger when observing lifts of heavy objects compared with light ones. Interestingly, here we demonstrate that this weight-driven modulation of corticospinal excitability is easily suppressed by the observer's expectations about object weight and that this suppression is mediated by the posterior superior temporal sulcus. Thus, our findings show that modulation of corticospinal excitability during observed object lifting is not robust but easily altered by top-down cognitive processes. Finally, our results also indicate how cortical inputs, originating remotely from motor pathways and processing action observation, overlap with bottom-up motor resonance effects.

Observer-Agent Kinematic Similarity Facilitates Action Intention Decoding

It is well known that the kinematics of an action is modulated by the underlying motor intention. In turn, kinematics serves as a cue also during action observation, providing hints about the intention of the observed action. However, an open question is whether decoding others’ intentions on the basis of their kinematics depends solely on how much the kinematics varies across different actions, or rather it is also influenced by its similarity with the observer motor repertoire. The execution of reach-to-grasp and place actions, differing for target size and context, was recorded in terms of upper-limb kinematics in 21 volunteers and in an actor. Volunteers had later to observe the sole reach-to-grasp phase of the actor’s actions, and predict the underlying intention. The potential benefit of the kinematic actor-participant similarity for recognition accuracy was evaluated. In execution, both target size and context modulated specific kinematic parameters. More importantly, although participants performed above chance in intention recognition, the similarity of motor patterns positively correlated with recognition accuracy. Overall, these data indicate that kinematic similarity exerts a facilitative role in intention recognition, providing further support to the view of action intention recognition as a visuo-motor process grounded in motor resonance.

Paired Associative Stimulation drives the emergence of motor resonance

BackgroundAssociative plasticity, the neurophysiological bases of Hebbian learning, has been implied in the formation of the association between sensory and motor representations of actions in the Mirror Neuron System; however, such inductor role still needs empirical support. Objective/hypothesisWe have assessed whether Paired Associative Stimulation (PAS), known to activate Hebbian associative plasticity, can induce the formation of atypical (absent in normal conditions), visuo-motor associations, reshaping motor resonance. MethodsHealthy participants underwent a novel PAS protocol (mirror-PAS, m-PAS), during which they were exposed to repeated pairings of transcranial magnetic stimulation (TMS) applied over the right primary motor cortex (M1), time-locked with the view of index-finger movements of the right (ipsilateral) hand. In a first experiment, the inter-stimulus interval (ISI) between visual-action stimuli and TMS pulses was varied. Before and after each m-PAS session, motor resonance was assessed by recording Motor Evoked Potentials induced by single-pulse TMS applied to the right M1, during the observation of both contralateral (left) and ipsilateral (right) index-finger movements. In the second experiment, the specificity of the m-PAS was assessed by presenting a visual stimulus depicting a non-biological movement. ResultsBefore m-PAS, the facilitation of corticospinal excitability occurred only during the view of contralateral (with respect to the TMS side) index-finger movements. The m-PAS induced new ipsilateral motor resonance responses, indexed by atypical facilitation of corticospinal excitability by the view of ipsilateral hand movements. This effect occurred only if the associative stimulation followed the chronometry of motor control (ISI of 25 ms) and if the visual stimulus of the m-PAS depicts a biological movement (human hand action). ConclusionsThe present findings provide the first empirical evidence that Hebbian learning induced by a PAS protocol shapes the visual-motor matching properties of the human Mirror Neuron System.

Neural multimodal integration underlying synchronization with a co-performer in music: Influences of motor expertise and visual information

Sensorimotor synchronization is a general skill that musicians have developed to the highest levels of performance, including synchronization in timing and articulation. This study investigated neurocognitive processes that enable such high levels of performance, specifically testing the relevance of 1) motor resonance and sharing high levels of motor expertise with the co-performer, and 2) the role of visual information in addition to auditory information. Musicians with varying levels of piano expertise (including non-pianists) performed on a single piano key with their right hand along with recordings of a pianist who performed simple melodies with the left hand, synchronizing timing and articulation. The prerecorded performances were presented as audio-only, audio-video, or audio-animation stimuli. Double pulse Transcranial Magnetic Stimulation (dTMS) was applied to test the contribution of the right dorsal premotor cortex (dPMC), an area implicated in motor resonance with observed (left-hand) actions, and the contribution of the right intraparietal sulcus (IPS), an area known for multisensory binding. Results showed effects of dTMS in the conditions that included visual information. IPS stimulation improved synchronization, although this effect was found to reverse in the video condition with higher levels of piano expertise. dPMC stimulation improved or worsened synchronization ability. Level of piano expertise was found to influence this direction in the video condition. These results indicate that high levels of relevant motor expertise are required to beneficially employ visual and motor information of a co-performer for sensorimotor synchronization, which may qualify the effects of dPMC and IPS involvement.

The last chance to pass the ball: investigating the role of temporal expectation and motor resonance in processing temporal errors in motor actions.

Humans can acquire information on others’ motor outputs (action prediction) and intentions (action understanding) according to their individual motor repertoire and to the detected gesture’s features (e.g. temporal patterns). We aimed at dissociating between action prediction and action understanding abilities in soccer players and novices observing soccer action videos including correct timing pass (CTP) or delayed pass (DP). First, we used an occluding paradigm to evaluate participants’ ability to predict the correct time to pass the ball. Although soccer players showed reduced reaction times, all subjects showed a similar pattern of performance: during DP observation, responses appeared delayed with respect to the other conditions but anticipated with respect to the observed DP. In a separate experiment, we investigated the ability to recognize CTP vs DP and the modulation of primary motor cortex (M1) excitability associated to video observation. Only soccer players showed selective modulation of M1 according to the plausibility of the observed action, with increased excitability during the observation of the CTP and in a phase preceding the DP. In conclusion, action prediction ability seems to be independent from the individual motor repertoire. By contrast, only subjects with previously acquired sensorimotor skills are able to infer the observed action’s long-term intention.

Social perceptions of warmth and competence influence behavioral intentions and neural processing.

Perceptions of the primary social dimensions, warmth and competence, determine how we view and relate to social targets. To discern how warmth and competence might affect neural processing and its downstream behavioral consequences, we manipulated impressions of targets' warmth and competence and then measured intentions toward the target and motor resonance, a neural process previously linked to social processing. While EEG was recorded, 66 participants watched videos of people performing a simple motor activity and completed a measure of hypothetical intentions to help or harm. Both perceptions of warmth and competence predicted an increase in helping intentions. Moreover, participants showed the least motor resonance with high competence-medium warmth targets, suggesting the importance of both social dimensions in driving neural simulation of targets' actions. Perceptions of a person's warmth and competence can affect not only how others might intend to treat them, but also how they might process their basic experiences on a neural level.