Alessio Avenanti

Somatic and Motor Components of Action Simulation

Seminal studies in monkeys report that the viewing of actions performed by other individuals activates frontal and parietal cortical areas typically involved in action planning and execution. That mirroring actions might rely on both motor and somatosensory components is suggested by reports that action observation and execution increase neural activity in motor and in somatosensory areas. This occurs not only during observation of naturalistic movements but also during the viewing of biomechanically impossible movements that tap the afferent component of action, possibly by eliciting strong somatic feelings in the onlooker. Although somatosensory feedback is inherently linked to action execution, information on the possible causative role of frontal and parietal cortices in simulating motor and sensory action components is lacking. By combining low-frequency repetitive and single-pulse transcranial magnetic stimulation, we found that virtual lesions of ventral premotor cortex (vPMc) and primary somatosensory cortex (S1) suppressed mirror motor facilitation contingent upon observation of possible and impossible movements, respectively. In contrast, virtual lesions of primary motor cortex did not influence mirror motor facilitation. The reported double dissociation suggests that vPMc and S1 play an active, differential role in simulating efferent and afferent components of observed actions.

Low-frequency rTMS promotes use-dependent motor plasticity in chronic stroke A randomized trial

Objective: To investigate the long-term behavioral and neurophysiologic effects of combined time-locked repetitive transcranial magnetic stimulation (rTMS) and physical therapy (PT) intervention in chronic stroke patients with mild motor disabilities. Methods: Thirty patients were enrolled in a double-blind, randomized, single-center clinical trial. Patients received 10 daily sessions of 1 Hz rTMS over the intact motor cortex. In different groups, stimulation was either real (rTMSR) or sham (rTMSS) and was administered either immediately before or after PT. Outcome measures included dexterity, force, interhemispheric inhibition, and corticospinal excitability and were assessed for 3 months after the end of treatment. Results: Treatment induced cumulative rebalance of excitability in the 2 hemispheres and a reduction of interhemispheric inhibition in the rTMSR groups. Use-dependent improvements were detected in all groups. Improvements in trained abilities were small and transitory in rTMSS patients. Greater behavioral and neurophysiologic outcomes were found after rTMSR, with the group receiving rTMSR before PT (rTMSR-PT) showing robust and stable improvements and the other group (PT-rTMSR) showing a slight improvement decline over time. Conclusion: Our findings indicate that priming PT with inhibitory rTMS is optimal to boost use-dependent plasticity and rebalance motor excitability and suggest that time-locked rTMS is a valid and promising approach for chronic stroke patients with mild motor impairment. Classification of evidence: This interventional study provides Class I evidence that time-locked rTMS before or after physical therapy improves measures of dexterity and force in the affected limb in patients with chronic deficits more than 6 months poststroke. Neurology® 2012;78:256–264

Compensatory Plasticity in the Action Observation Network: Virtual Lesions of STS Enhance Anticipatory Simulation of Seen Actions

Observation of snapshots depicting ongoing motor acts increases corticospinal motor excitability. Such motor facilitation indexes the anticipatory simulation of observed (implied) actions and likely reflects computations occurring in the parietofrontal nodes of a cortical network subserving action perception (action observation network, AON). However, direct evidence for the active role of AON in simulating the future of seen actions is lacking. Using a perturb-and-measure transcranial magnetic stimulation (TMS) approach, we show that off-line TMS disruption of regions within (inferior frontal cortex, IFC) and upstream (superior temporal sulcus, STS) the parietofrontal AON transiently abolishes and enhances the motor facilitation to observed implied actions, respectively. Our findings highlight the critical role of IFC in anticipatory motor simulation. More importantly, they show that disruption of STS calls into play compensatory motor simulation activity, fundamental for counteracting the noisy visual processing induced by TMS. Thus, short-term plastic changes in the AON allow motor simulation to deal with any gap or ambiguity of ever-changing perceptual worlds. These findings support the active, compensatory, and predictive role of frontoparietal nodes of the AON in the perception and anticipatory simulation of implied actions.

Kinesthetic Imagery and Tool-Specific Modulation of Corticospinal Representations in Expert Tennis Players

Specific physical or mental practice may induce short- and long-term neuroplastic changes in the motor system and cause tools to become part of ones own body representation. Athletes who use tools as part of their practice may be an excellent model for assessing the neural correlates of possible bodily representation changes that are specific to extensive practice. We used single-pulse transcranial magnetic stimulation to measure corticospinal excitability in forearm and hand muscles of expert tennis players and novices while they mentally practiced a tennis forehand, table tennis forehand, and a golf drive. The muscles of expert tennis players showed increased corticospinal facilitation during motor imagery of tennis but not golf or table tennis. Novices, although athletes, were not modulated across sports. Subjective reports indicated that only in the tennis imagery condition did experts differ from novices in the ability to form proprioceptive images and to consider the tool as an extension of the hand. Neurophysiological and subjective data converge to suggest a key role of long-term experience in modulating sensorimotor body representations during mental simulation of sports.

Corticospinal facilitation during first and third person imagery

Motor imagery can be defined as the covert rehearsal of movement. Previous research with transcranial magnetic stimulation (TMS) has demonstrated that motor imagery increases the corticospinal excitability of the primary motor cortex in the area corresponding to the representation of the muscle involved in the imagined movement. This research, however, has been limited to imagery of oneself in motion. We extend the TMS research by contrasting first person imagery and third person imagery of index finger abduction-adduction movements. Motor evoked potentials were recorded from first dorsal interosseous (FDI) and abductor digiti minimi (ADM) during single pulse TMS. Participants performed first and third person motor imagery, visual imagery, and static imagery. Visual imagery involved non biological motion while static imagery involved a first person perspective of the unmoving hand. Relative to static imagery, excitability during imagined movement increased in FDI but not ADM. The facilitation in first person imagery adds to previous findings. A greater facilitation of MEPs recorded from FDI was found in third person imagery where the action was clearly attributable to another person. We interpret this novel result in the context of observed action and imagined observation of self action, and attribute the result to activation of mirror systems for matching the imagined action with an inner visuo-motor template.

Fronto-parietal areas necessary for a multisensory representation of peripersonal space in humans: An rtms study

A network of brain regions including the ventral premotor cortex (vPMc) and the posterior parietal cortex (PPc) is consistently recruited during processing of multisensory stimuli within peripersonal space (PPS). However, to date, information on the causal role of these fronto-parietal areas in multisensory PPS representation is lacking. Using low-frequency repetitive TMS (rTMS; 1 Hz), we induced transient virtual lesions to the left vPMc, PPc, and visual cortex (V1, control site) and tested whether rTMS affected audio–tactile interaction in the PPS around the hand. Subjects performed a timed response task to a tactile stimulus on their right (contralateral to rTMS) hand while concurrent task-irrelevant sounds were presented either close to the hand or 1 m far from the hand. When no rTMS was delivered, a sound close to the hand reduced RT-to-tactile targets as compared with when a far sound was presented. This space-dependent, auditory modulation of tactile perception was specific to a hand-centered reference frame. Such a specific form of multisensory interaction near the hand can be taken as a behavioral hallmark of PPS representation. Crucially, virtual lesions to vPMc and PPc, but not to V1, eliminated the speeding effect due to near sounds, showing a disruption of audio–tactile interactions around the hand. These findings indicate that multisensory interaction around the hand depends on the functions of vPMc and PPc, thus pointing to the necessity of this human fronto-parietal network in multisensory representation of PPS.

Neuroanatomical substrates of action perception and understanding: an anatomic likelihood estimation meta-analysis of lesion-symptom mapping studies in brain injured patients.

Several neurophysiologic and neuroimaging studies suggested that motor and perceptual systems are tightly linked along a continuum rather than providing segregated mechanisms supporting different functions. Using correlational approaches, these studies demonstrated that action observation activates not only visual but also motor brain regions. On the other hand, brain stimulation and brain lesion evidence allows tackling the critical question of whether our action representations are necessary to perceive and understand others’ actions. In particular, recent neuropsychological studies have shown that patients with temporal, parietal, and frontal lesions exhibit a number of possible deficits in the visual perception and the understanding of others’ actions. The specific anatomical substrates of such neuropsychological deficits however, are still a matter of debate. Here we review the existing literature on this issue and perform an anatomic likelihood estimation meta-analysis of studies using lesion-symptom mapping methods on the causal relation between brain lesions and non-linguistic action perception and understanding deficits. The meta-analysis encompassed data from 361 patients tested in 11 studies and identified regions in the inferior frontal cortex, the inferior parietal cortex and the middle/superior temporal cortex, whose damage is consistently associated with poor performance in action perception and understanding tasks across studies. Interestingly, these areas correspond to the three nodes of the action observation network that are strongly activated in response to visual action perception in neuroimaging research and that have been targeted in previous brain stimulation studies. Thus, brain lesion mapping research provides converging causal evidence that premotor, parietal and temporal regions play a crucial role in action recognition and understanding.

Don't do it! cortical inhibition and self-attribution during action observation

Numerous studies suggest that both self-generated and observed actions of others activate overlapping neural networks, implying a shared, agent-neutral representation of self and other. Contrary to the shared representation hypothesis, we recently showed that the human motor system is not neutral with respect to the agent of an observed action [Schtz-Bosbach, S., Mancini, B., Aglioti, S. M., & Haggard, P. Self and other in the human motor system. Current Biology, 16, 18301834, 2006]. Observation of actions attributed to another agent facilitated the motor system, whereas observation of identical actions linked to the self did not. Here we investigate whether the absence of motor facilitation for observing ones own actions reflects a specific process of cortical inhibition associated with self-representation. We analyzed the duration of the silent period induced by transcranial magnetic stimulation of the motor cortex in active muscles as an indicator of motor inhibition. We manipulated whether an observed action was attributed to another agent, or to the subjects themselves, using a manipulation of body ownership on the basis of the rubber hand illusion. Observation of actions linked to the self led to longer silent periods than observation of a static hand, but the opposite effect occurred when observing identical actions attributed to another agent. This finding suggests a specific inhibition of the motor system associated with self-representation. Cortical suppression for actions linked to the self might prevent inappropriate perseveration within the motor system.

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.

Motor mapping of implied actions during perception of emotional body language

BACKGROUND Perceiving and understanding emotional cues is critical for survival. Using the International Affective Picture System (IAPS) previous TMS studies have found that watching humans in emotional pictures increases motor excitability relative to seeing landscapes or household objects, suggesting that emotional cues may prime the body for action. OBJECTIVE/HYPOTHESIS Here we tested whether motor facilitation to emotional pictures may reflect the simulation of the human motor behavior implied in the pictures occurring independently of its emotional valence. METHODS Motor-evoked potentials (MEPs) to single-pulse TMS of the left motor cortex were recorded from hand muscles during observation and categorization of emotional and neutral pictures. In experiment 1 participants watched neutral, positive and negative IAPS stimuli, while in experiment 2, they watched pictures depicting human emotional (joyful, fearful), neutral body movements and neutral static postures. RESULTS Experiment 1 confirms the increase in excitability for emotional IAPS stimuli found in previous research and shows, however, that more implied motion is perceived in emotional relative to neutral scenes. Experiment 2 shows that motor excitability and implied motion scores for emotional and neutral body actions were comparable and greater than for static body postures. CONCLUSIONS In keeping with embodied simulation theories, motor response to emotional pictures may reflect the simulation of the action implied in the emotional scenes. Action simulation may occur independently of whether the observed implied action carries emotional or neutral meanings. Our study suggests the need of controlling implied motion when exploring motor response to emotional pictures of humans.