Topographically selective motor inhibition under threat of pain.

ABSTRACT: Pain-related motor adaptations may be enacted predictively at the mere threat of pain, before pain occurrence. Yet, in humans, the neurophysiological mechanisms underlying motor adaptations in anticipation of pain remain poorly understood. We tracked the evolution of changes in corticospinal excitability (CSE) as healthy adults learned to anticipate the occurrence of lateralized, muscle-specific pain to the upper limb. Using a Pavlovian threat conditioning task, different visual stimuli predicted pain to the right or left forearm (experiment 1) or hand (experiment 2). During stimuli presentation before pain occurrence, single-pulse transcranial magnetic stimulation was applied over the left primary motor cortex to probe CSE and elicit motor evoked potentials from target right forearm and hand muscles. The correlation between participants' trait anxiety and CSE was also assessed. Results showed that threat of pain triggered corticospinal inhibition specifically in the limb where pain was expected. In addition, corticospinal inhibition was modulated relative to the threatened muscle, with threat of pain to the forearm inhibiting the forearm and hand muscles, whereas threat of pain to the hand inhibited the hand muscle only. Finally, stronger corticospinal inhibition correlated with greater trait anxiety. These results advance the mechanistic understanding of pain processes showing that pain-related motor adaptations are enacted at the mere threat of pain, as sets of anticipatory, topographically organized motor changes that are associated with the expected pain and are shaped by individual anxiety levels. Including such anticipatory motor changes into models of pain may lead to new treatments for pain-related disorders.

The Spatiotemporal Dynamics of Facial Movements Reveals the Left Side of a Posed Smile.

Humans can recombine thousands of different facial expressions. This variability is due to the ability to voluntarily or involuntarily modulate emotional expressions, which, in turn, depends on the existence of two anatomically separate pathways. The Voluntary (VP) and Involuntary (IP) pathways mediate the production of posed and spontaneous facial expressions, respectively, and might also affect the left and right sides of the face differently. This is a neglected aspect in the literature on emotion, where posed expressions instead of genuine expressions are often used as stimuli. Two experiments with different induction methods were specifically designed to investigate the unfolding of spontaneous and posed facial expressions of happiness along the facial vertical axis (left, right) with a high-definition 3-D optoelectronic system. The results showed that spontaneous expressions were distinguished from posed facial movements as revealed by reliable spatial and speed key kinematic patterns in both experiments. Moreover, VP activation produced a lateralization effect: compared with the felt smile, the posed smile involved an initial acceleration of the left corner of the mouth, while an early deceleration of the right corner occurred in the second phase of the movement, after the velocity peak.

When Corticospinal Inhibition Favors an Efficient Motor Response.

Many daily activities involve responding to the actions of other people. However, the functional relationship between the motor preparation and execution phases still needs to be clarified. With the combination of different and complementary experimental techniques (i.e., motor excitability measures, reaction times, electromyography, and dyadic 3-D kinematics), we investigated the behavioral and neurophysiological signatures characterizing different stages of a motor response in contexts calling for an interactive action. Participants were requested to perform an action (i.e., stirring coffee or lifting a coffee cup) following a co-experimenter's request gesture. Another condition, in which a non-interactive gesture was used, was also included. Greater corticospinal inhibition was found when participants prepared their motor response after observing an interactive request, compared to a non-interactive gesture. This, in turn, was associated with faster and more efficient action execution in kinematic terms (i.e., a social motor priming effect). Our results provide new insights on the inhibitory and facilitatory drives guiding social motor response generation. Altogether, the integration of behavioral and neurophysiological indexes allowed us to demonstrate that a more efficient action execution followed a greater corticospinal inhibition. These indexes provide a full picture of motor activity at both planning and execution stages.

Corticospinal excitability and conductivity are related to the anatomy of the corticospinal tract.

Probing the brain structure-function relationship is at the heart of modern neuroscientific explorations, enabled by recent advances in brain mapping techniques. This study aimed to explore the anatomical blueprint of corticospinal excitability and shed light on the structure-function relationship within the human motor system. Using diffusion magnetic resonance imaging tractography, based on the spherical deconvolution approach, and transcranial magnetic stimulation (TMS), we show that anatomical inter-individual variability of the corticospinal tract (CST) modulates the corticospinal excitability and conductivity. Our findings show for the first time the relationship between increased corticospinal excitability and conductivity in individuals with a bigger CST (i.e., number of streamlines), as well as increased corticospinal microstructural organization (i.e., fractional anisotropy). These findings can have important implications for the understanding of the neuroanatomical basis of TMS as well as the study of the human motor system in both health and disease.

Contextual Priors Guide Perception and Motor Responses to Observed Actions.

In everyday-life scenarios, prior expectations provided by the context in which actions are embedded support action prediction. However, it is still unclear how newly learned action-context associations can drive our perception and motor responses. To fill this gap, we measured behavioral (Experiment 1) and motor responses (Experiment 2) during two tasks requiring the prediction of occluded actions or geometrical shapes. Each task consisted of an implicit probabilistic learning and a test phase. During learning, we exposed participants to videos showing specific associations between a contextual cue and a particular action or shape. During the test phase, videos were earlier occluded to reduce the amount of sensorial information and induce participants to use the implicitly learned action/shape-context associations for disambiguation. Results showed that reliable contextual cues made participants more accurate in identifying the unfolding action or shape. Importantly, motor responses were modulated by contextual probability during action, but not shape prediction. Particularly, in conditions of perceptual uncertainty the motor system coded for the most probable action based on contextual informativeness, regardless of action kinematics. These findings suggest that contextual priors can shape motor responses to action observation beyond mere kinematics mapping.

Reach-to-Grasp: A Multisensory Experience.

The reach-to-grasp movement is ordinarily performed in everyday living activities and it represents a key behavior that allows humans to interact with their environment. Remarkably, it serves as an experimental test case for probing the multisensory architecture of goal-oriented actions. This review focuses on experimental evidence that enhances or modifies how we might conceptualize the "multisensory" substrates of prehension. We will review evidence suggesting that how reach-to-grasp movements are planned and executed is influenced by information coming from different sensory modalities such as vision, proprioception, audition, taste, and olfaction. The review closes with some considerations about the predominant role of the multisensory constituents in shaping prehensile behavior and how this might be important for future research developments, especially in the rehabilitative domain.

Autistic Traits Differently Account for Context-Based Predictions of Physical and Social Events.

Autism is associated with difficulties in making predictions based on contextual cues. Here, we investigated whether the distribution of autistic traits in the general population, as measured through the Autistic Quotient (AQ), is associated with alterations of context-based predictions of social and non-social stimuli. Seventy-eight healthy participants performed a social task, requiring the prediction of the unfolding of an action as interpersonal (e.g., to give) or individual (e.g., to eat), and a non-social task, requiring the prediction of the appearance of a moving shape as a short (e.g., square) or a long (e.g., rectangle) figure. Both tasks consisted of (i) a familiarization phase, in which the association between each stimulus type and a contextual cue was manipulated with different probabilities of co-occurrence, and (ii) a testing phase, in which visual information was impoverished by early occlusion of video display, thus forcing participants to rely on previously learned context-based associations. Findings showed that the prediction of both social and non-social stimuli was facilitated when embedded in high-probability contexts. However, only the contextual modulation of non-social predictions was reduced in individuals with lower 'Attention switching' abilities. The results provide evidence for an association between weaker context-based expectations of non-social events and higher autistic traits.

Social Motor Priming: when offline interference facilitates motor execution.

Many daily activities involve synchronizing with other people's actions. Previous literature has revealed that a slowdown of performance occurs whenever the action to be carried out is different to the one observed (i.e., visuomotor interference). However, action execution can be facilitated by observing a different action if it calls for an interactive gesture (i.e., social motor priming). The aim of this study is to investigate the costs and benefits of spontaneously processing a social response and then executing the same or a different action. Participants performed two different types of grips, which could be either congruent or not with the socially appropriate response and with the observed action. In particular, participants performed a precision grip (PG; thumb-index fingers opposition) or a whole-hand grasp (WHG; fingers-palm opposition) after observing videos showing an actor performing a PG and addressing them (interactive condition) or not (non-interactive condition). Crucially, in the interactive condition, the most appropriate response was a WHG, but in 50 percent of trials participants were asked to perform a PG. This procedure allowed us to measure both the facilitator effect of performing an action appropriate to the social context (WHG)-but different with respect to the observed one (PG)-and the cost of inhibiting it. These effects were measured by means of 3-D kinematical analysis of movement. Results show that, in terms of reaction time and movement time, the interactive request facilitated (i.e., speeded) the socially appropriate action (WHG), whereas interfered with (i.e., delayed) a different action (PG), although observed actions were always PGs. This interference also manifested with an increase of maximum grip aperture, which seemingly reflects the concurrent representation of the socially appropriate response. Overall, these findings extend previous research by revealing that physically incongruent action representations can be integrated into a single action plan even during an offline task and without any training.

Gaze and body cues interplay during interactive requests.

Although observing other's gaze and body movements provides a crucial source of information to successfully interact with other people, it remains unclear whether observers weigh differently these cues and whether the convergence of gaze and body's directions determines facilitation effects. Here we aim to shed more light on this issue by testing the reliance upon these cues from both a behavioral and a neurophysiological perspective in a social interactive context. In Experiment 1, we manipulated the convergence between the direction of an actor's upper limb movement and gaze direction while he attempts to socially interact with the participants observing the scene. We determined the direction of gaze as well as the duration of participants' ocular fixations during the observation of the scene. In Experiment 2, we measured and correlated the effect of the body/gaze manipulation on corticospinal excitability and on the readiness to interact-a disposition to engage in social situations. Eye-tracking data revealed that participants fixated chiefly the actor's head when his hand and gaze directions were divergent. Possibly a strategy to disambiguate the scene. Whereas participants mainly fixated the actor's hand when he performed an interactive request toward the participants. From a neurophysiological point of view, the more participants felt involved in the interaction, the lower was motor preparation in the muscle potentially needed to fulfill the actor's request. We contend that social contexts are more likely to elicit motor preparation compared to non-social ones, and that muscular inhibition is a necessary mechanism in order to prevent unwanted overt reactions during action observation tasks.

Changes in corticospinal excitability associated with post-error slowing.

According to available evidence, after making an erroneous decision people tend to slow down on the next decision. This empirical regularity, known as "post error slowing" (PES), has been traditionally interpreted as the result of a conservative response criterion adopted to avoid future errors and it is supposed to be driven by changes in the excitability of the motor system. However, the consequences of errors have been almost exclusively investigated by means of button-press tasks, which have been criticized because of their limited ecological validity and it is still unclear to what extent errors bias the motor system activity during the planning and the on-line control of complex and realistic goal-directed actions. To overcome these potential limitations, in the present study, we investigated the effect of errors on the preparation and execution of the reach-to-grasp movement, one of the most significant daily life actions. In addition to reaction times (RTs), we measured motor-evoked potential (MEP) to explore the influence of errors on corticospinal (CS) excitability, and we applied kinematical analysis to examine the underlying reorganization of the movement following an error. The results of the present study showed that MEPs tend to be reduced after the failure to reach and grasp an object, supporting the traditional interpretation of PES. Furthermore, in addition to RTs, we found that error-reactivity strategically influences the grasping component of the action, whereas the reaching component appears to be impermeable to PES. These findings demonstrate that the error-reactivity is a strong empirical phenomenon, which spreads into the motor system at the level of both movement preparation and execution, even when more realistic and ecologically valid tasks are used.

Action Observation and Effector Independency.

The finding of reasonably consistent spatial and temporal productions of actions across different body parts has been used to argue in favor of the existence of a high-order representation of motor programs. In these terms, a generalized motor program consists of an abstract memory structure apt to specify a class of non-specific instructions used to guide a broad range of movements (e.g., "grasp," "bite"). Although a number of studies, using a variety of tasks, have assessed the issue of effector independence in terms of action execution, little is known regarding the issue of effector independence within an action observation context. Here corticospinal excitability (CSE) of the right hand's first dorsal interosseous (FDI) and abductor digiti minimi (ADM) muscles was assessed by means of single-pulse transcranial magnetic stimulation (spTMS) during observation of a grasping action performed by the hand, the foot, the mouth, the elbow, or the knee. The results indicate that observing a grasping action performed with different body parts activates the effector typically adopted to execute that action, i.e., the hand. We contend that, as far as grasping is concerned, motor activations by action observation are evident in the muscles typically used to perform the observed action, even when the action is executed with another effector. Nevertheless, some exceptions call for a deeper analysis of motor coding.

Look at Me: Early Gaze Engagement Enhances Corticospinal Excitability During Action Observation.

Direct gaze is a powerful social cue able to capture the onlooker's attention. Beside gaze, head and limb movements as well can provide relevant sources of information for social interaction. This study investigated the joint role of direct gaze and hand gestures on onlookers corticospinal excitability (CE). In two experiments we manipulated the temporal and spatial aspects of observed gaze and hand behavior to assess their role in affecting motor preparation. To do this, transcranial magnetic stimulation (TMS) on the primary motor cortex (M1) coupled with electromyography (EMG) recording was used in two experiments. In the crucial manipulation, we showed to participants four video clips of an actor who initially displayed eye contact while starting a social request gesture, and then completed the action while directing his gaze toward a salient object for the interaction. This way, the observed gaze potentially expressed the intention to interact. Eye tracking data confirmed that gaze manipulation was effective in drawing observers' attention to the actor's hand gesture. In the attempt to reveal possible time-locked modulations, we tracked CE at the onset and offset of the request gesture. Neurophysiological results showed an early CE modulation when the actor was about to start the request gesture looking straight to the participants, compared to when his gaze was averted from the gesture. This effect was time-locked to the kinematics of the actor's arm movement. Overall, data from the two experiments seem to indicate that the joint contribution of direct gaze and precocious kinematic information, gained while a request gesture is on the verge of beginning, increases the subjective experience of involvement and allows observers to prepare for an appropriate social interaction. On the contrary, the separation of gaze cues and body kinematics can have adverse effects on social motor preparation. CE is highly susceptible to biological cues, such as averted gaze, which is able to automatically capture and divert observer's attention. This point to the existence of heuristics based on early action and gaze cues that would allow observers to interact appropriately.

Reach-To-Grasp Movements: A Multimodal Techniques Study.

The aim of the present study was to investigate the correlation between corticospinal activity, kinematics, and electromyography (EMG) associated with the execution of precision and whole-hand grasps (WHGs). To this end, motor-evoked potentials (MEPs) induced by transcranial magnetic stimulation (TMS), EMG, and 3-D motion capture data have been simultaneously recorded during the planning and the execution of prehensile actions toward either a small or a large object. Differences in the considered measures were expected to distinguish between the two types of grasping actions both in terms of action preparation and execution. The results indicate that the index finger (FDI) and the little finger (ADM) muscles showed different activation patterns during grasping execution, but only the FDI appeared to distinguish between the two types of actions during motor preparation. Kinematics analysis showed that precision grips differed from WHGs in terms of displayed fingers distance when shaping before object's contact, and in terms of timing and velocity patterns. Moreover, significant correlations suggest a relationship between the muscular activation and the temporal aspects concerned with the index finger's extension during whole-hand actions. Overall, the present data seem to suggest a crucial role played by index finger as an early "marker" of differential motor preparation for different types of grasps and as a "navigator" in guiding whole-hand prehensile actions. Aside from the novelty of the methodological approach characterizing the present study, the data provide new insights regarding the level of crosstalk among different levels concerned with the neuro-behavioral organization of reach-to-grasp movements.

Testing rTMS-Induced Neuroplasticity: A Single Case Study of Focal Hand Dystonia.

Focal hand dystonia in musicians is a neurological motor disorder in which aberrant plasticity is caused by excessive repetitive use. This work's purposes were to induce plasticity changes in a dystonic musician through five daily thirty-minute sessions of 1 Hz repetitive transcranial magnetic stimulation (rTMS) applied to the left M1 by using neuronavigated stimulation and to reliably measure the effect of these changes. To this aim, the relationship between neuroplasticity changes and motor recovery was investigated using fine-grained kinematic analysis. Our results suggest a statistically significant improvement in motor coordination both in a task resembling the dystonic-inducing symptoms and in a reach-to-grasp task. This single case study supports the safe and effective use of noninvasive brain stimulation in neurologic patients and highlights the importance of evaluating outcomes in measurable ways. This issue is a key aspect to focus on to classify the clinical expression of dystonia. These preliminary results promote the adoption of kinematic analysis as a valuable diagnostic tool.

Numerical Affordance Influences Action Execution: A Kinematic Study of Finger Movement.

Humans represent symbolic numbers as oriented from left to right: the mental number line (MNL). Up to now, scientific studies have mainly investigated the MNL by means of response times. However, the existing knowledge on the MNL can be advantaged by studies on motor patterns while responding to a number. Cognitive representations, in fact, cannot be fully understood without considering their impact on actions. Here we investigated whether a motor response can be influenced by number processing. Participants seated in front of a little soccer goal. On each trial they were visually presented with a numerical (2, 5, 8) or a non-numerical ($) stimulus. They were instructed to kick a small ball with their right index toward a frontal soccer goal as soon as a stimulus appeared on a screen. However, they had to refrain from kicking when number five was presented (no-go signal). Our main finding is that performing a kicking action after observation of the larger digit proved to be more efficient: the trajectory path was shorter and lower on the surface, velocity peak was anticipated. The smaller number, instead, specifically altered the temporal and spatial aspects of trajectories, leading to more prolonged left deviations. This is the first experimental demonstration that the reaching component of a movement is influenced by number magnitude. Since this paradigm does not require any verbal skill and non-symbolic stimuli (array of dots) can be used, it could be fruitfully adopted to evaluate number abilities in children and even preschoolers. Notably, this is a self-motivating and engaging task, which might help children to get involved and to reduce potential arousal connected to institutional paper-and-pencil examinations.

Act on Numbers: Numerical Magnitude Influences Selection and Kinematics of Finger Movement.

In the past decade hand kinematics has been reliably adopted for investigating cognitive processes and disentangling debated topics. One of the most controversial issues in numerical cognition literature regards the origin - cultural vs. genetically driven - of the mental number line (MNL), oriented from left (small numbers) to right (large numbers). To date, the majority of studies have investigated this effect by means of response times, whereas studies considering more culturally unbiased measures such as kinematic parameters are rare. Here, we present a new paradigm that combines a "free response" task with the kinematic analysis of movement. Participants were seated in front of two little soccer goals placed on a table, one on the left and one on the right side. They were presented with left- or right-directed arrows and they were instructed to kick a small ball with their right index toward the goal indicated by the arrow. In a few test trials participants were presented also with a small (2) or a large (8) number, and they were allowed to choose the kicking direction. Participants performed more left responses with the small number and more right responses with the large number. The whole kicking movement was segmented in two temporal phases in order to make a hand kinematics' fine-grained analysis. The Kick Preparation and Kick Finalization phases were selected on the basis of peak trajectory deviation from the virtual midline between the two goals. Results show an effect of both small and large numbers on action execution timing. Participants were faster to finalize the action when responding to small numbers toward the left and to large number toward the right. Here, we provide the first experimental demonstration which highlights how numerical processing affects action execution in a new and not-overlearned context. The employment of this innovative and unbiased paradigm will permit to disentangle the role of nature and culture in shaping the direction of MNL and the role of finger in the acquisition of numerical skills. Last but not least, similar paradigms will allow to determine how cognition can influence action execution.

Overt orienting of spatial attention and corticospinal excitability during action observation are unrelated.

Observing moving body parts can automatically activate topographically corresponding motor representations in the primary motor cortex (M1), the so-called direct matching. Novel neurophysiological findings from social contexts are nonetheless proving that this process is not automatic as previously thought. The motor system can flexibly shift from imitative to incongruent motor preparation, when requested by a social gesture. In the present study we aim to bring an increase in the literature by assessing whether and how diverting overt spatial attention might affect motor preparation in contexts requiring interactive responses from the onlooker. Experiment 1 shows that overt attention-although anchored to an observed biological movement-can be captured by a target object as soon as a social request for it becomes evident. Experiment 2 reveals that the appearance of a short-lasting red dot in the contralateral space can divert attention from the target, but not from the biological movement. Nevertheless, transcranial magnetic stimulation (TMS) over M1 combined with electromyography (EMG) recordings (Experiment 3) indicates that attentional interference reduces corticospinal excitability related to the observed movement, but not motor preparation for a complementary action on the target. This work provides evidence that social motor preparation is impermeable to attentional interference and that a double dissociation is present between overt orienting of spatial attention and neurophysiological markers of action observation.

Kick with the finger: symbolic actions shape motor cortex excitability.

A large body of research indicates that observing actions made by others is associated with corresponding motor facilitation of the observer's corticospinal system. However, it is still controversial whether this matching mechanism strictly reflects the kinematics of the observed action or its meaning. To test this issue, motor evoked potentials induced by single-pulse transcranial magnetic stimulation were recorded from hand and leg muscles while participants observed a symbolic action carried out with the index finger, but classically performed with the leg (i.e., a soccer penalty kick). A control condition in which participants observed a similar (but not symbolic) hand movement was also included. Results showed that motor facilitation occurs both in the observer's hand (first dorsal interosseous) and leg (quadriceps femoris) muscles. The present study provides evidence that both the kinematics and the symbolic value of an observed action are able to modulate motor cortex excitability. The human motor system is thus not only involved in mirroring observed actions but is also finely tuned to their symbolic value.

Congruent and Incongruent Corticospinal Activations at the Level of Multiple Effectors.

Motor resonance is defined as the subliminal activation of the motor system while observing actions performed by others. However, resonating with another person's actions is not always an appropriate response: In real life, people do not just imitate but rather respond in a suitable fashion. A growing body of neurophysiologic studies has demonstrated that motor resonance can be overridden by complementary motor responses (such as preparing a precision grip on a small object when seeing an open hand in sign of request). In this study, we investigated the relationship between congruent and incongruent corticospinal activations at the level of multiple effectors. The modulation of motor evoked potentials evoked by single-pulse TMS over the motor cortex was assessed in upper and lower limb muscles of participants observing a soccer player performing a penalty kick straight in their direction. Study results revealed a double dissociation: Seeing the soccer player kicking the ball triggered a motor resonance in the observer's lower limb, whereas the upper limb response afforded by the object was overridden. On the other hand, seeing the ball approaching the observers elicited a complementary motor activation in upper limbs while motor resonance in lower limbs disappeared. Control conditions showing lateral kicks, mimicked kicks, and a ball in penalty area were also included to test the motor coding of object affordances. Results point to a modulation of motor responses in different limbs over the course of action and in function of their relevance in different contexts. We contend that ecologically valid paradigms are now needed to shed light on the motor system functioning in complex forms of interaction.

Complementary actions.

Complementary colors are color pairs which, when combined in the right proportions, produce white or black. Complementary actions refer here to forms of social interaction wherein individuals adapt their joint actions according to a common aim. Notably, complementary actions are incongruent actions. But being incongruent is not sufficient to be complementary (i.e., to complete the action of another person). Successful complementary interactions are founded on the abilities: (i) to simulate another person's movements, (ii) to predict another person's future action/s, (iii) to produce an appropriate incongruent response which differ, while interacting, with observed ones, and (iv) to complete the social interaction by integrating the predicted effects of one's own action with those of another person. This definition clearly alludes to the functional importance of complementary actions in the perception-action cycle and prompts us to scrutinize what is taking place behind the scenes. Preliminary data on this topic have been provided by recent cutting-edge studies utilizing different research methods. This mini-review aims to provide an up-to-date overview of the processes and the specific activations underlying complementary actions.