Motor Properties of Peripersonal Space in Humans

Background: A stimulus approaching the body requires fast processing and appropriate motor reactions. In monkeys, fronto-parietal networks are involved both in integrating multisensory information within a limited space surrounding the body (i.e. peripersonal space, PPS) and in action planning and execution, suggesting an overlap between sensory representations of space and motor representations of action. In the present study we investigate whether these overlapping representations also exist in the human brain. Methodology/Principal Findings: We recorded from hand muscles motor-evoked potentials (MEPs) induced by single-pulse of transcranial magnetic stimulation (TMS) after presenting an auditory stimulus either near the hand or in far space. MEPs recorded 50 ms after the near-sound onset were enhanced compared to MEPs evoked after far sounds. This near-far modulation faded at longer inter-stimulus intervals, and reversed completely for MEPs recorded 300 ms after the sound onset. At that time point, higher motor excitability was associated with far sounds. Such auditory modulation of hand motor representation was specific to a hand-centred, and not a body-centred reference frame. Conclusions/Significance: This pattern of corticospinal modulation highlights the relation between space and time in the PPS representation: an early facilitation for near stimuli may reflect immediate motor preparation, whereas, at later time intervals, motor preparation relates to distant stimuli potentially approaching the body

The future in action: neurophysiological and behavioral evidence of anticipatory motor simulation.

The motor system can no longer be considered as a mere passive executive system of motor commands generated elsewhere in the brain. On the contrary, it is deeply involved in perceptual and cognitive functions and acts as an “anticipation device”. The present thesis investigates the anticipatory motor mechanisms occurring in two particular instances: i) when processing sensory events occurring within the peripersonal space (PPS); and ii) when perceiving and predicting others’actions. The first study provides evidence that PPS representation in humans modulates neural activity within the motor system, while the second demonstrates that the motor mapping of sensory events occurring within the PPS critically relies on the activity of the premotor cortex. The third study provides direct evidence that the anticipatory motor simulation of others’ actions critically relies on the activity of the anterior node of the action observation network (AON), namely the inferior frontal cortex (IFC). The fourth study, sheds light on the pivotal role of the left IFC in predicting the future end state of observed right-hand actions. Finally, the fifth study examines how the ability to predict others’ actions could be influenced by a reduction of sensorimotor experience due to the traumatic or congenital loss of a limb. Overall, the present work provides new insights on: i) the anticipatory mechanisms of the basic reactivity of the motor system when processing sensory events occurring within the PPS, and the same anticipatory motor mechanisms when perceiving others’ implied actions; ii) the functional connectivity and plasticity of premotor-motor circuits both during the motor mapping of sensory events occurring within the PPS and when perceiving others’ actions; and iii) the anticipatory mechanisms related to others’ actions prediction

Raw MEPs amplitudes recorded from the FDI (top) and the ADM muscle (bottom) in one representative subject from Experiment 1 (only 120% rMT blocks are shown).

<p>Raw MEPs amplitudes recorded from the FDI (top) and the ADM muscle (bottom) in one representative subject from Experiment 1 (only 120% rMT blocks are shown).</p

Boosting and decreasing action prediction abilities through excitatory and inhibitory tDCS of inferior frontal cortex

Influential theories suggest that humans predict others’ upcoming actions by using their own motor system as an internal forward model. However, evidence that the motor system is causally essential for predicting others’ actions is meager. Using transcranial direct current stimulation (tDCS), we tested the role of the inferior frontal cortex (IFC), in action prediction (AP). We devised a novel AP task where participants observed the initial phases of right-hand reaching-to-grasp actions and had to predict their outcome (i.e., the goal/object to be grasped). We found that suppression by cathodal (inhibitory) tDCS of the left IFC, but not the left superior temporal sulcus or the right IFC, selectively impaired performance on the AP task, but not on a difficulty-matched control task. Remarkably, anodal (excitatory) tDCS of the left IFC brought about a selective improvement in the AP task. These findings indicate that the left IFC is necessary for predicting the outcomes of observed human right-hand actions. Crucially, our study shows for the first time that down- and up-regulating excitability within the motor system can hinder and enhance AP abilities, respectively. These findings support predictive coding theories of action perception and have implications for enhancement of AP abilities

Experimental set up.

<p>The main panel represents the experimental set up and a typical subject during Experiment 1. The small upper panel represents the sequence of events in each trial. The small lower panel represents a typical subject during Experiment 2, when participants placed their right arm to the side, with the hand pointing backwards (far from the source of near sounds).</p

Suppression of left ventral premotor cortex impairs action prediction: transcranial direct current stimulation studies

Influential theoretical models suggest that the human motor system is designed to act as an anticipation device and that humans predict others\u2019 forthcoming actions by using their own motor system as an internal forward model. However to date evidence for a causative role of the motor system in predicting the outcome of observed actions is lacking. Here we used transcranial direct current stimulation (tDCS) to test the role of ventral premotor cortex (vPMc) in predicting the end-state of an observed action. In the Action-Prediction (AP) task, participants observed the initial phase of a right-hand reaching-grasping action. The final phase of the action was masked and subjects had to guess which of two objects were going to be grasped by the hand. In a difficulty-matched control task, subjects observed similarly interrupted movements of a non-biological (NB) stimulus approaching one of two targets. Participants performed both tasks in two separate sessions (1 week interval) that were carried out after 15 minutes of inhibitory (cathodal) real- or sham-tDCS over the left-vPMc (experiment 1) or the right-vPMc (experiment 2). Relative to sham stimulation, suppression of left-vPMc but not of right-vPMc brought about a selective reduction of accuracy in the AP-task, but not in the NB-task. These findings indicate that left-vPMc is necessary for extracting the future end-state of human actions based on the observation of the initial phases of the movement and suggest a left frontal lateralization in the predictive coding of others\u2019 right-hand actions

Mean MEP amplitude with respect to baseline (MEPi) recorded when sounds were presented NEAR (red lines) and FAR (blue lines) from the subjects' body (Experiment 2).

<p>(A) MEPi recorded with lower (120% rMT) TMS pulse intensity. (B) MEPi recorded with higher (140% rMT) TMS pulse intensity. Error bars denote s.e.m.</p