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

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 MEPs 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 nowadays needed to shed light on the motor system functioning in complex forms of interaction

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

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\u2009Hz 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

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\u2019s 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\u2019s extension during whole-hand actions. Overall, the present data seem to suggest a crucial role played by index finger as an early \u201cmarker\u201d of differential motor preparation for different types of grasps and as a \u201cnavigator\u201d 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

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

Complementary actions: exploring the flexibility of the Action Observation System

Social interaction is an essential part of the human experience and actions are the primary means by which humans interact with the surrounding world. The ability to recognize and understand other people’s actions is necessary for an efficient interaction with other agents. Our motor system can promptly and accurately coordinate these forms of interactions in our daily activity. However, how the brain is able to produce such appropriate output has yet to be fully understood. The present work aims at unveiling the processes taking place in the motor system while observing actions of interactive agents and action calling for an (interactive) involvement of the observer. The core argument is to explore the flexibility of the motor system when preparing identical and non-identical responses in complex realistic situations, and to test the automaticity of these processes by directly investigating the role played by visuospatial attention during action observation. The introductory section of this thesis will first provide an overview of the state of the art regarding the mechanism that could be at the basis of the comprehension of other’s actions, that is the ‘mirror mechanism’ (Chapter 1). Mirror neurons are neural cells which activate both during the execution of an action and during the observation of the same action performed by another individual. From their first discovery in the premotor cortex of the macaque brain in the early nineties (Di Pellegrino, Fadiga, Fogassi, Gallese and Rizzolatti, 1992), these visuomotor neurons have been extensively studied both in primates and in humans. Chapter 1 will review evidence on the existence of such mirror mechanism and on its basic properties and anatomy, with a particular focus on the human literature concerned with the Action Observation System (AOS). Convergent evidence suggests that actions are coded in the observer’s brain in such a way that resembles the actual execution of the action. As a result, an embodied simulation (i.e., from the inside) would allow to understand the observed action through the onlooker’s own motor experience. However, to simulate the actions of other people is not always the best strategy to interact with them. Indeed, we are often required to perform actions which differ from those observed. Chapter 2 will summarize recent neurophysiological findings suggesting that the human brain is able to overcome the imitative bias in favor of non-identical responses which are appropriate to the context requirements. A particular focus will be given to the literature on complementary actions, namely a type of social interactions in which the involved agents have to perform incongruent responses to reach a common goal. Put simply, it seems that while the human motor system is prone to simulate other’s action, this imitative tendency can be modulated according to the context. However, whether top-down factors might play a role in determining the embodied simulation is still controversial. In Chapter 3 a review of the literature in which the automaticity of the visuo-motor transformation has been questioned will be presented. Overall, it emerges that top-down factors, such as visuospatial attention, may influence the motor simulation of observed actions. The second part of the present thesis concerns the experimental work I undertook. Chapter 4 provides a description of the general methodology common to the experimental studies conducted with transcranial magnetic stimulation (TMS) coupled with electromyographic (EMG) registration to measure corticospinal excitability modulations during action observation. In the first experiment (Chapter 5) a novel paradigm to study complementary actions at the level of multiple effectors will be described. Participants were presented with a soccer player kicking a ball toward them, thus implicitly requiring their response as to parry the approaching ball. Control conditions showing lateral kicks, mimicked kicks, and the ball still in penalty area were also included. This paradigm was adopted to investigate the time-course of imitative and complementary responses in lower and upper limbs. In a subsequent experiment presented in Chapter 6, a similar paradigm was adopted, but crucially it included a condition in which the imitative and the complementary responses were simultaneously elicited in the observers’ motor system. This allowed to disentangle the contribution of different levels of motor coding – namely, kinematic, predictive and response coding – during action observation. Chapters 7 and 8 will report on two experiments aimed at clarifying the influence of spatial attention allocation during observation of actions eliciting (or not) a complementary response. In particular, in Chapter 7 participants were presented with action sequences evoking a complementary gesture, such as picking up a mug placed in the video foreground, when an individual was inviting them to do so. Notably, the observed and required actions were mismatched in order to investigate the observers’ spontaneous unfolding of different motor activations. Crucially, spatial attention allocation toward specific parts of the visual scene was manipulated by means of the sudden appearance of a red dot, and responses were recorded both at a behavioral (eye-tracking) and at a neurophysiological level. In a further experiment (Chapter 8), the allocation of attention toward parts of the visual scene was modulated by means of the actor’s gaze direction, which represents a more ecologically-valid manipulation. This experimental work shows the role of spatial attention in simulation and reciprocity, thus promoting a more complete and integrated understanding on the role of top-down factors in action observation. A general discussion (Chapter 9), contextualizing the results obtained by the studies presented in the present thesis will follow. Taken together, these studies will help to better define how the motor system flexibly and dynamically modulates its activity during the course of action observation. Moreover, the present work could broadening our view on action observation processes in social contexts, towards the definition of a more complete account

Contextual Priors Guide Perception and Motor Responses to Observed Actions

Published: 23 July 2021In 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.Italian Ministry of University and Research (PRIN 2017, Prot. 2017N7WCLP; to C.U.); the Italian Ministry of Health (Ricerca Corrente 2021, Scientific Institute, IRCCS E. Medea; to A.F.); and by the Department of Languages and Literatures, Communication, Education and Society, University of Udine (PRID 2017; to C.U.)

Social Motor Priming: when offline interference facilitates motor execution

Many daily activities involve synchronizing with other people\u2019s 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)\u2014but different with respect to the observed one (PG)\u2014and 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\u2019s 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\u2019s 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\u2019s 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\u2019 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\u2014a disposition to engage in social situations. Eye-tracking data revealed that participants fixated chiefly the actor\u2019s head when his hand and gaze directions were divergent. Possibly a strategy to disambiguate the scene. Whereas participants mainly fixated the actor\u2019s 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\u2019s 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