Matteo Candidi

Mapping implied body actions in the human motor system.

The human visual system is highly tuned to perceive actual motion as well as to extrapolate dynamic information from static pictures of objects or creatures captured in the middle of motion. Processing of implied motion activates higher-order visual areas that are also involved in processing biological motion. Imagery and observation of actual movements performed by others engenders selective activation of motor and premotor areas that are part of a mirror-neuron system matching action observation and execution. By using single-pulse transcranial magnetic stimulation, we found that the mere observation of static snapshots of hands suggesting a pincer grip action induced an increase in corticospinal excitability as compared with observation of resting, relaxed hands, or hands suggesting a completed action. This facilitatory effect was specific for the muscle that would be activated during actual execution of the observed action. We found no changes in responsiveness of the tested muscles during observation of nonbiological entities with (e.g., waterfalls) or without (e.g., icefalls) implied motion. Thus, extrapolation of motion information concerning human actions induced a selective activation of the motor system. This indicates that overlapping motor regions are engaged in the visual analysis of physical and implied body actions. The absence of motor evoked potential modulation during observation of end posture stimuli may indicate that the observation–execution matching system is preferentially activated by implied, ongoing but not yet completed actions.

Motor facilitation during action observation: topographic mapping of the target muscle and influence of the onlooker's posture

Transcranial magnetic stimulation (TMS) studies report that viewing a given action performed by a model activates the neural representation of the onlookers muscles that are activated during the actual execution of the observed action. Here we sought to determine whether this mirror observation‐execution facilitation reflects only muscular specificity or whether it is also influenced by postural congruency between onlooker/model body parts. We recorded motor potentials evoked by single‐pulse TMS from the first dorsal interosseous (FDI) and abductor digiti minimi (ADM) muscles during observation of the right index and little finger abduction/adduction movements of models who kept their hands in a palm‐down or palm‐up position. Moreover, in different experiments observers kept their right hand palm down or palm up. Selective motor facilitation was observed during observation of movements that map the motor function of the targeted muscles, regardless of the posture of the observed hand. Modulation of FDI, however, was obtained only when participants kept their hand palm down; by contrast, modulation of ADM was obtained only when participants kept their hand palm up. Interestingly, electromyographic recordings showed that FDI is mostly active when index abduction/adduction movements are performed in the palm‐down position, whereas ADM is mostly active when little finger abduction/adduction movements are performed in the palm‐up position. Results show that the influence of the onlookers hand posture is comparable in action execution and observation, thus indicating a fine‐grain functional correspondence between these two processes.

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.

Virtual lesion of ventral premotor cortex impairs visual perception of biomechanically possible but not impossible actions.

Abstract Single-pulse transcranial magnetic stimulation (TMS) studies show that action observation facilitates the onlookers cortico-spinal system supporting the notion of motor mirroring. Repetitive transcranial magnetic stimulation (rTMS) over ventral premotor cortex (vPMc) impairs visual discrimination of body actions. Although studies suggest that the action observation–execution matching system may map only actions that belong to the observers motor repertoire, we demonstrated comparable motor and premotor facilitation during observation of biomechanically possible as well as impossible actions. It has also been shown that seeing impossible body movements activates the extrastriate body area (EBA). Using event-related rTMS, we sought to determine whether vPMc and EBA are actively involved in the visual discrimination of actions performed through biomechanically possible or impossible kinematics and of their biomechanical plausibility. Stimulation of vPMc impaired discrimination of possible actions while leaving intact the discrimination of biomechanically impossible actions and of biomechanical plausibility. No effect of EBA rTMS on any type of action processing was found. Thus, vPMc is crucial for discrimination of the goal of actions that can be actually performed suggesting that this area is involved in the visual processing of goal-directed actions.

Kinematics fingerprints of leader and follower role-taking during cooperative joint actions.

Performing online complementary motor adjustments is quintessential to joint actions since it allows interacting people to coordinate efficiently and achieve a common goal. We sought to determine whether, during dyadic interactions, signaling strategies and simulative processes are differentially implemented on the basis of the interactional role played by each partner. To this aim, we recorded the kinematics of the right hand of pairs of individuals who were asked to grasp as synchronously as possible a bottle-shaped object according to an imitative or complementary action schedule. Task requirements implied an asymmetric role assignment so that participants performed the task acting either as (1) Leader (i.e., receiving auditory information regarding the goal of the task with indications about where to grasp the object) or (2) Follower (i.e., receiving instructions to coordinate their movements with their partner’s by performing imitative or complementary actions). Results showed that, when acting as Leader, participants used signaling strategies to enhance the predictability of their movements. In particular, they selectively emphasized kinematic parameters and reduced movement variability to provide the partner with implicit cues regarding the action to be jointly performed. Thus, Leaders make their movements more “communicative” even when not explicitly instructed to do so. Moreover, only when acting in the role of Follower did participants tend to imitate the Leader, even in complementary actions where imitation is detrimental to joint performance. Our results show that mimicking and signaling are implemented in joint actions according to the interactional role of the agent, which in turn is reflected in the kinematics of each partner.

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.

Do Not Resonate with Actions: Sentence Polarity Modulates Cortico-Spinal Excitability during Action-Related Sentence Reading

Background Theories of embodied language suggest that the motor system is differentially called into action when processing motor-related versus abstract content words or sentences. It has been recently shown that processing negative polarity action-related sentences modulates neural activity of premotor and motor cortices. Methods and Findings We sought to determine whether reading negative polarity sentences brought about differential modulation of cortico-spinal motor excitability depending on processing hand-action related or abstract sentences. Facilitatory paired-pulses Transcranial Magnetic Stimulation (pp-TMS) was applied to the primary motor representation of the right-hand and the recorded amplitude of induced motor-evoked potentials (MEP) was used to index M1 activity during passive reading of either hand-action related or abstract content sentences presented in both negative and affirmative polarity. Results showed that the cortico-spinal excitability was affected by sentence polarity only in the hand-action related condition. Indeed, in keeping with previous TMS studies, reading positive polarity, hand action-related sentences suppressed cortico-spinal reactivity. This effect was absent when reading hand action-related negative polarity sentences. Moreover, no modulation of cortico-spinal reactivity was associated with either negative or positive polarity abstract sentences. Conclusions Our results indicate that grammatical cues prompting motor negation reduce the cortico-spinal suppression associated with affirmative action sentences reading and thus suggest that motor simulative processes underlying the embodiment may involve even syntactic features of language.

Hands on the future: Facilitation of cortico-spinal hand-representation when reading the future tense of hand-related action verbs

Reading action‐related verbs brings about sensorimotor neural activity, suggesting that the linguistic representation of actions impinges upon neural structures largely overlapping with those involved in actual action execution. While studies of direct action observation indicate that motor mirroring is inherently anticipatory, no information is currently available on whether deriving action‐related knowledge from language also takes into account the temporal deployment of actions. Using transcranial magnetic stimulation, here we sought to determine whether reading action verbs conjugated in the future induced higher cortico‐spinal activity with respect to when the same verbs were conjugated in the past tense. We recorded motor‐evoked potentials (MEPs) from relaxed hand and leg muscles of healthy subjects who were reading silently hand‐ or leg‐related action, sensorial (non‐somatic) and abstract verbs conjugated either in future or past tense. The amplitude of MEPs recorded from the hand was higher during reading hand‐related action verbs conjugated in the future than in the past. No future‐related modulation of leg muscles activity was found during reading leg‐related action verbs. In a similar vein, no future‐related change of hand or leg muscles reactivity was found for abstract or sensorial verbs. These results indicate that the anticipatory mirroring of hand actions may be triggered by linguistic representations and not only by direct action observation.

Prejudiced interactions: Implicit racial bias reduces predictive simulation during joint action with an out-group avatar

During social interactions people automatically apply stereotypes in order to rapidly categorize others. Racial differences are among the most powerful cues that drive these categorizations and modulate our emotional and cognitive reactivity to others. We investigated whether implicit racial bias may also shape hand kinematics during the execution of realistic joint actions with virtual in- and out-group partners. Caucasian participants were required to perform synchronous imitative or complementary reach-to-grasp movements with avatars that had different skin color (white and black) but showed identical action kinematics. Results demonstrate that stronger visuo-motor interference (indexed here as hand kinematics differences between complementary and imitative actions) emerged: i) when participants were required to predict the partners action goal in order to on-line adapt their own movements accordingly; ii) during interactions with the in-group partner, indicating the partners racial membership modulates interactive behaviors. Importantly, the in-group/out-group effect positively correlated with the implicit racial bias of each participant. Thus visuo-motor interference during joint action, likely reflecting predictive embodied simulation of the partners movements, is affected by cultural inter-individual differences.

Early and Phasic Cortical Metabolic Changes in Vestibular Neuritis Onset

Functional brain activation studies described the presence of separate cortical areas responsible for central processing of peripheral vestibular information and reported their activation and interactions with other sensory modalities and the changes of this network associated to strategic peripheral or central vestibular lesions. It is already known that cortical changes induced by acute unilateral vestibular failure (UVF) are various and undergo variations over time, revealing different cortical involved areas at the onset and recovery from symptoms. The present study aimed at reporting the earliest change in cortical metabolic activity during a paradigmatic form of UVF such as vestibular neuritis (VN), that is, a purely peripheral lesion of the vestibular system, that offers the opportunity to study the cortical response to altered vestibular processing. This research reports [18F]fluorodeoxyglucose positron emission tomography brain scan data concerning the early cortical metabolic activity associated to symptoms onset in a group of eight patients suffering from VN. VN patients’ cortical metabolic activity during the first two days from symptoms onset was compared to that recorded one month later and to a control healthy group. Beside the known cortical response in the sensorimotor network associated to vestibular deafferentation, we show for the first time the involvement of Entorhinal (BAs 28, 34) and Temporal (BA 38) cortices in early phases of symptomatology onset. We interpret these findings as the cortical counterparts of the attempt to reorient oneself in space counteracting the vertigo symptom (Bas 28, 34) and of the emotional response to the new pathologic condition (BA 38) respectively. These interpretations were further supported by changes in patients’ subjective ratings in balance, anxiety, and depersonalization/derealization scores when tested at illness onset and one month later. The present findings contribute in expanding knowledge about early, fast-changing, and complex cortical responses to pathological vestibular unbalanced processing.