Action anticipation beyond the action observation network: a functional magnetic resonance imaging study in expert basketball players.

The ability to predict the actions of others is quintessential for effective social interactions, particularly in competitive contexts (e.g. in sport) when knowledge about upcoming movements allows anticipating rather than reacting to opponents. Studies suggest that we predict what others are doing by using our own motor system as an internal forward model and that the fronto-parietal action observation network (AON) is fundamental for this ability. However, multiple-duty cells dealing with action perception and execution have been found in a variety of cortical regions. Here we used functional magnetic resonance imaging to explore, in expert basketball athletes and novices, whether the ability to make early predictions about the fate of sport-specific actions (i.e. free throws) is underpinned by neural regions beyond the classical AON. We found that, although involved in action prediction, the fronto-parietal AON was similarly activated in novices and experts. Importantly, athletes exhibited relatively greater activity in the extrastriate body area during the prediction task, probably due to their expert reading of the observed action kinematics. Moreover, experts exhibited higher activation in the bilateral inferior frontal gyrus and in the right anterior insular cortex when producing errors, suggesting that they might become aware of their own errors. Correct action prediction induced higher posterior insular cortex activity in experts and higher orbito-frontal activity in novices, suggesting that body awareness is important for performance monitoring in experts, whereas novices rely more on higher-order decision-making strategies. This functional reorganization highlights the tight relationship between action anticipation, error awareness and motor expertise leading to body-related processing and differences in decision-making processes.

Massive somatic deafferentation and motor deefferentation of the lower part of the body impair its visual recognition: a psychophysical study of patients with spinal cord injury.

Embodied cognition theories postulate that perceiving and understanding the body states of other individuals are underpinned by the neural structures activated during first-hand experience of the same states. This suggests that one's own sensorimotor system may be used to identify the actions and sensations of others. Virtual and real brain lesion studies show that visual processing of body action and body form relies upon neural activity in the ventral premotor and the extrastriate body areas, respectively. We explored whether visual body perception may also be altered in the absence of damage to the above cortical regions by testing healthy controls and spinal cord injury (SCI) patients whose brain was unable to receive somatic information from and send motor commands to the lower limbs. Participants performed tasks investigating the ability to visually discriminate changes in the form or action of body parts affected by somatosensory and motor disconnection. SCI patients showed a specific, cross-modal deficit in the visual recognition of the disconnected lower body parts. This deficit affected both body action and body form perception, hinting at a pervasive influence of ongoing body signals on the brain network dedicated to visual body processing. Testing SCI patients who did or did not practise sports allowed us to test the influence of motor practice on visual body recognition. We found better upper body action recognition in sport-practising SCI patients, indicating that motor practice is useful for maintaining visual representation of actions after deafferentation and deefferentation. This may be a potential resource to be exploited for rehabilitation.

Extrastriate body area underlies aesthetic evaluation of body stimuli.

Humans appear to be the only animals to have developed the practice and culture of art. This practice presumably relies on special processing circuits within the human brain associated with a distinct subjective experience, termed aesthetic experience, and preferentially evoked by artistic stimuli. We assume that positive or negative aesthetic judgments are an important function of neuroaesthetic circuits. The localisation of these circuits in the brain remains unclear, though neuroimaging studies have suggested several possible neural correlates of aesthetic preference. We applied repetitive transcranial magnetic stimulation (rTMS) over candidate brain areas to disrupt aesthetic processing while healthy volunteers made aesthetic preference judgments between pairs of dance postures, or control non-body stimuli. Based on evidence from visual body perception studies, we targeted the ventral premotor cortex (vPMC) and extrastriate body area (EBA), in the left and right hemispheres. rTMS over EBA reduced aesthetic sensitivity for body stimuli relative to rTMS over vPMC, while no such difference was found for non-body stimuli. We interpret our results within the framework of dual routes for visual body processing. rTMS over either EBA or vPMC reduced the contributions of the stimulated area to body processing, leaving processing more reliant on the unaffected route. Disruption of EBA reduces the local processing of the stimuli and reduced observers' aesthetic sensitivity. Conversely, disruption of the global route via vPMC increased the relative contribution of the local route via EBA and thus increased aesthetic sensitivity. In this way, we suggest a complementary contribution of both local and global routes to aesthetic processing.

Finger recognition and gesture imitation in Gerstmann's syndrome.

We report the association between finger agnosia and gesture imitation deficits in a right-handed, right-hemisphere damaged patient with Gerstmann's syndrome (GS), a neuropsychological syndrome characterized by finger and toe agnosia, left-right disorientation and dyscalculia. No language deficits were found. The patient showed a gestural imitation deficit that specifically involved finger movements and postures. The association between finger recognition and imitation deficits suggests that both static and dynamic aspects of finger representations are impaired in GS. We suggest that GS is a disorder of body representation that involves hands and fingers, that is, the non-facial body parts most involved in social interactions.

Autistic traits predict poor integration between top-down contextual expectations and movement kinematics during action observation.

Autism is associated with difficulties in predicting and understanding other people's actions. There is evidence that autistic traits are distributed across a spectrum and that subclinical forms of autistic impairments can also be measured in the typical population. To investigate the association between autistic traits and motor responses to others' actions, we quantified these traits and measured cortico-spinal excitability modulations in M1 during the observation of actions embedded in congruent, incongruent and ambiguous contexts. In keeping with previous studies, we found that actions observed in congruent contexts elicited an early facilitation of M1 responses, and actions observed in incongruent contexts, resulted in a later inhibition. Correlational analysis revealed no association between autistic traits and the facilitation for congruent contexts. However, we found a significant correlation between motor inhibition and autistic traits, specifically related to social skills and attention to details. Importantly, the influence of these factors was independent from each other, and from the observer's gender. Thus, results suggest that individuals with higher social deficits and greater detail-processing style are more impaired in suppressing action simulation in M1 when a mismatch between kinematics and context occurs. This points to difficult integration between kinematics and contextual representations in the autistic-like brain.

Different contributions of visual and motor brain areas during liking judgments of same- and different-gender bodies.

Previous neuroimaging studies have shown that body aesthetic appreciation involves the activation of both visual and motor areas, supporting a role of sensorimotor embodiment in aesthetic processing. Causative evidence, however, that neural activity in these areas is crucial for reliable aesthetic body appreciation has so far provided only for extrastriate body area (EBA), while the functional role played by premotor regions remained less clear. Here, we applied short trains of repetitive transcranial magnetic stimulation (rTMS) over bilateral dorsal premotor cortex (dPMC) and EBA during liking judgments of female and male bodies varying in weight and implied motion. We found that both dPMC and EBA are necessary for aesthetic body appreciation, but their relative contribution depends on the model's gender. While dPMC-rTMS decreased the liking judgments of same-, but not of different-gender models, EBA-rTMS increased the liking judgments of different-, but not of same-gender models. Relative contributions of motor and visual areas may reflect processing of diverse aesthetic properties, respectively implied motion vs. body form, and/or greater sensorimotor embodiment of same- vs. different-gender bodies. Results suggest that aesthetic body processing is subserved by a network of motor and visual areas, whose relative contribution may depend on the specific stimulus and task.

Visual body recognition in a prosopagnosic patient.

Conspicuous deficits in face recognition characterize prosopagnosia. Information on whether agnosic deficits may extend to non-facial body parts is lacking. Here we report the neuropsychological description of FM, a patient affected by a complete deficit in face recognition in the presence of mild clinical signs of visual object agnosia. His deficit involves both overt and covert recognition of faces (i.e. recognition of familiar faces, but also categorization of faces for gender or age) as well as the visual mental imagery of faces. By means of a series of matching-to-sample tasks we investigated: (i) a possible association between prosopagnosia and disorders in visual body perception; (ii) the effect of the emotional content of stimuli on the visual discrimination of faces, bodies and objects; (iii) the existence of a dissociation between identity recognition and the emotional discrimination of faces and bodies. Our results document, for the first time, the co-occurrence of body agnosia, i.e. the visual inability to discriminate body forms and body actions, and prosopagnosia. Moreover, the results show better performance in the discrimination of emotional face and body expressions with respect to body identity and neutral actions. Since FM's lesions involve bilateral fusiform areas, it is unlikely that the amygdala-temporal projections explain the relative sparing of emotion discrimination performance. Indeed, the emotional content of the stimuli did not improve the discrimination of their identity. The results hint at the existence of two segregated brain networks involved in identity and emotional discrimination that are at least partially shared by face and body processing.