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

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