Cosimo Urgesi

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.

Magnetic Stimulation of Extrastriate Body Area Impairs Visual Processing of Nonfacial Body Parts

Functional magnetic resonance imaging indicates that observation of the human body induces a selective activation of a lateral occipitotemporal cortical area called extrastriate body area (EBA). This area is responsive to static and moving images of the human body and parts of it, but it is insensitive to faces and stimulus categories unrelated to the human body. With event-related repetitive transcranial magnetic stimulation, we tested the possible causal relation between neural activity in EBA and visual processing of body-related, nonfacial stimuli. Facial and noncorporeal stimuli were used as a control. Interference with neural activity in EBA induced a clear impairment, consisting of a significant increase in discriminative reaction time, in the visual processing of body parts. The effect was selective for stimulus type, because it affected responses to nonfacial body stimuli but not to noncorporeal and facial stimuli, and for locus of stimulation, because the effect from the interfering stimulation of EBA was absent during a corresponding stimulation of primary visual cortex. The results provide strong evidence that neural activity in EBA is not only correlated with but also causally involved in the visual processing of the human body and its parts, except the face.

Transcranial magnetic stimulation reveals two cortical pathways for visual body processing

Visual recognition of human bodies is more difficult for upside down than upright presentations. This body inversion effect implies that body perception relies on configural rather than local processing. Although neuroimaging studies indicate that the visual processing of human bodies engages a large fronto-temporo-parietal network, information about the neural underpinnings of configural body processing is meager. Here, we used repetitive transcranial magnetic stimulation (rTMS) to study the causal role of premotor, visual, and parietal areas in configural processing of human bodies. Eighteen participants performed a delayed matching-to-sample task with upright or inverted static body postures. Event-related, dual-pulse rTMS was applied 150 ms after the sample stimulus onset, over left ventral premotor cortex (vPMc), right extrastriate body area (EBA), and right superior parietal lobe (SPL) and, as a control site, over the right primary visual cortex (V1). Interfering stimulation of vPMc significantly reduced accuracy of matching judgments for upright bodies. In contrast, EBA rTMS significantly reduced accuracy for inverted but not for upright bodies. Furthermore, a significant body inversion effect was observed after interfering stimulation of EBA and V1 but not of vPMc and SPL. These results demonstrate an active contribution of the fronto-parietal mirror network to configural processing of bodies and suggest a novel, embodied aspect of visual perception. In contrast, the local processing of the body, possibly based on the form of individual body parts instead of on the whole body unit, appears to depend on EBA. Therefore, we propose two distinct cortical routes for the visual processing of human bodies.

The Neural Basis of Body Form and Body Action Agnosia

Visual analysis of faces and nonfacial body stimuli brings about neural activity in different cortical areas. Moreover, processing body form and body action relies on distinct neural substrates. Although brain lesion studies show specific face processing deficits, neuropsychological evidence for defective recognition of nonfacial body parts is lacking. By combining psychophysics studies with lesion-mapping techniques, we found that lesions of ventromedial, occipitotemporal areas induce face and body recognition deficits while lesions involving extrastriate body area seem causatively associated with impaired recognition of body but not of face and object stimuli. We also found that body form and body action recognition deficits can be double dissociated and are causatively associated with lesions to extrastriate body area and ventral premotor cortex, respectively. Our study reports two category-specific visual deficits, called body form and body action agnosia, and highlights their neural underpinnings.

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.

Motor facilitation of the human cortico-spinal system during observation of bio-mechanically impossible movements

Neurophysiological and neuroimaging studies in the human and the monkey brain indicate that links between action observation and execution are much tighter than previously believed. Indeed, the mere observation of movements performed by other individuals brings about a clear increase in activity in specific fronto-parietal neural networks (mirror system). Here, we report a series of four single-pulse transcranial magnetic stimulation studies of the motor system, which show that observation of index and little finger movements brings about a facilitation of potentials recorded from muscles that would be involved in the actual execution of the observed action. Remarkably, however, a clear representational selectivity was found also during observation of bio-mechanically impossible index or little finger movements. Thus, in movement observation tasks, the human cortico-spinal system reacts similarly to the vision of bio-mechanically possible and impossible movements but it is able to detect which muscle would be involved in the actual execution of the observed movement. Importantly, this system may be more related to coding body part movements than precisely simulating their execution.

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.

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.

The Spiritual Brain: Selective Cortical Lesions Modulate Human Self-Transcendence

The predisposition of human beings toward spiritual feeling, thinking, and behaviors is measured by a supposedly stable personality trait called self-transcendence. Although a few neuroimaging studies suggest that neural activation of a large fronto-parieto-temporal network may underpin a variety of spiritual experiences, information on the causative link between such a network and spirituality is lacking. Combining pre- and post-neurosurgery personality assessment with advanced brain-lesion mapping techniques, we found that selective damage to left and right inferior posterior parietal regions induced a specific increase of self-transcendence. Therefore, modifications of neural activity in temporoparietal areas may induce unusually fast modulations of a stable personality trait related to transcendental self-referential awareness. These results hint at the active, crucial role of left and right parietal systems in determining self-transcendence and cast new light on the neurobiological bases of altered spiritual and religious attitudes and behaviors in neurological and mental disorders.

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.