Combined EEG and immersive virtual reality unveil dopaminergic modulation of error monitoring in Parkinson's Disease.

Detecting errors in your own and others' actions is associated with discrepancies between intended and expected outcomes. The processing of salient events is associated with dopamine release, the balance of which is altered in Parkinson's disease (PD). Errors in observed actions trigger various electrocortical indices (e.g. mid-frontal theta, error-related delta, and error positivity [oPe]). However, the impact of dopamine depletion to observed errors in the same individual remains unclear. Healthy controls (HCs) and PD patients observed ecological reach-to-grasp-a-glass actions performed by a virtual arm from a first-person perspective. PD patients were tested under their dopaminergic medication (on-condition) and after dopaminergic withdrawal (off-condition). Analyses of oPe, delta, and theta-power increases indicate that while the formers were elicited after incorrect vs. correct actions in all groups, the latter were observed in on-condition but altered in off-condition PD. Therefore, different EEG error signatures may index the activity of distinct mechanisms, and error-related theta power is selectively modulated by dopamine depletion. Our findings may facilitate discovering dopamine-related biomarkers for error-monitoring dysfunctions that may have crucial theoretical and clinical implications.

What the study of spinal cord injured patients can tell us about the significance of the body in cognition.

Although in the last three decades philosophers, psychologists and neuroscientists have produced numerous studies on human cognition, the debate concerning its nature is still heated and current views on the subject are somewhat antithetical. On the one hand, there are those who adhere to a view implying 'disembodiment' which suggests that cognition is based entirely on symbolic processes. On the other hand, a family of theories referred to as the Embodied Cognition Theories (ECT) postulate that creating and maintaining cognition is linked with varying degrees of inherence to somatosensory and motor representations. Spinal cord injury induces a massive body-brain disconnection with the loss of sensory and motor bodily functions below the lesion level but without directly affecting the brain. Thus, SCI may represent an optimal model for testing the role of the body in cognition. In this review, we describe post-lesional cognitive modifications in relation to body, space and action representations and various instances of ECT. We discuss the interaction between body-grounded and symbolic processes in adulthood with relevant modifications after body-brain disconnection.

Doing it Wrong: A Systematic Review on Electrocortical and Behavioral Correlates of Error Monitoring in Patients with Neurological Disorders.

Detecting errors in one's own and other's actions is a crucial ability for learning and adapting behavior to everchanging, highly volatile environments. Studies in healthy people demonstrate that monitoring errors in one's own and others' actions are underpinned by specific neural systems that are dysfunctional in a variety of neurological disorders. In this review, we first briefly discuss the main findings concerning error detection and error awareness in healthy subjects, the current theoretical models, and the tasks usually applied to investigate these processes. Then, we report a systematic search for evidence of dysfunctional error monitoring among neurological populations (basal ganglia, neurodegenerative, white-matter diseases and acquired brain injury). In particular, we examine electrophysiological and behavioral evidence for specific alterations of error processing in neurological disorders. Error-related negativity (ERN) amplitude were reduced in most (although not all) neurological patient groups, whereas Positivity Error (Pe) amplitude appeared not to be affected in most patient groups. Also theta activity was reduced in some neurological groups, but consistent evidence on the oscillatory activity has not been provided thus far. Behaviorally, we did not observe relevant patterns of pronounced dysfunctional (post-) error processing. Finally, we discuss limitations of the existing literature, conclusive points, open questions and new possible methodological approaches for clinical studies.

Predicting the fate of basketball throws: an EEG study on expert action prediction in wheelchair basketball players.

The ability to anticipate and detect changes in human movement helps people to modify their behaviors in ever changing environments. Studies indicate that expertise modulates observation of domain-specific actions in sports-a process that is crucial for adapting rapidly to a new situation, often before awareness of environmental changes is achieved. Here, we explored the electrophysiological underpinnings of wheelchair basketball players predicting the fate of free throws performed by wheelchair basketball athletes. We performed electroencephalography (EEG) in semi-professional wheelchair players with different degrees of expertise (players) and in ambulant, non-expert people (controls) while they observed movie stimuli of a free throw that could land inside or outside the basket. On each trial, participants were asked to predict the outcome of the throw. For each group, event-related potentials (ERPs) were averaged as a function of condition, using only the trials that were correctly predicted. Results show that compared to controls, expert players exhibit a greater negative amplitude of oCNV over Pz (an observational contingent negative variation-like waveform which is considered a marker of action effect prediction) during the wrist movement preceding the ball release (the last 100 ms of the shot), which carries the most crucial kinematic information regarding the fate of the throw. Our data provide further support to the view that functional modulation of the action observation network is associated with expertise.

An fMRI study on the neural correlates of social conformity to a sexual minority.

Social conformity refers to the tendency to align one's own behaviors, beliefs and values to those of others. Little is known about social influence coming from a minority group. To test whether social pressure from sexual minorities triggers avoidance-motivated behaviors, we explored how being influenced by the preferences of gay peers modifies the behavioral and neural reactivity of individuals defined as in- vs. out- groups on the basis of sexual orientation. To this aim, we combined fMRI with a social conformity paradigm in which heterosexual and gay/bisexual (hereafter non-exclusively heterosexual, NEH) individuals provided with male body attractiveness ratings by a fictitious group of gay students may or may not alter their previous rating and may or may not conform to the mean. Behaviorally, conformity to the minority preference was found in in-group NEH more than in out-group heterosexuals. Analysis of BOLD signal showed that social pressure brought about increased brain activity in frontal and parietal regions associated with the detection of social conflict. These results show that members of a sexual majority group display a smaller level of conformity when a sexual minority group exerts social influence. However, the neural correlates of this modulation are yet to be clarified.

Influence of cognitive stance and physical perspective on subjective and autonomic reactivity to observed pain and pleasure: An immersive virtual reality study.

Observing others' pain may induce a reaction called personal distress that may be influenced by top-down (imagine self or other in pain, i.e., self- vs other-oriented stance) and bottom-up (physical perspective of those who suffer, i.e., first vs third person perspective- 1PP vs 3PP) processes. The different contributions of these processes have not been teased apart. By capitalizing on the power of Immersive Virtual Reality, we explored how behavioural (subjective ratings) and physiological reactivity (skin conductance reactivity, SCR) to pain and pleasure delivered to an avatar was influenced by Cognitive stance and Physical perspective. Taking an Other-Oriented stance leads to attributing higher congruent valence (i.e. pain rated as unpleasant and pleasure as pleasant) and intensity to the stimuli and induces reduced SCR. Ownership over the virtual limb was maximal in 1PP where physiological reactivity to the stimuli was comparable. Our results highlight different components underpinning reactivity to pain and pleasure.

Wronger than wrong: Graded mapping of the errors of an avatar in the performance monitoring system of the onlooker.

EEG studies show that observing errors in one's own or others' actions triggers specific electro-cortical signatures in the onlooker's brain, but whether the brain error-monitoring system operates according to graded or discrete rules is still largely unknown. To explore this issue, we combined immersive virtual reality with EEG recording in participants who observed an avatar reaching-to-grasp a glass from a first-person perspective. The avatar could perform correct or erroneous actions. Erroneous grasps were defined as small or large depending on the magnitude of the trajectory deviation from the to-be-grasped glass. Results show that electro-cortical indices of error detection (indexed by ERN and mid-frontal theta oscillations), but not those of error awareness (indexed by error-Positivity), were gradually modulated by the magnitude of the observed errors. Moreover, the phase connectivity analysis revealed that enhancement of mid-frontal theta phase synchronization paralleled the magnitude of the observed error. Thus, theta oscillations represent an electro-cortical index of the degree of control exerted by mid-frontal regions whose activation depends on how much an observed action outcome results maladaptive for the onlooker. Our study provides novel neurophysiological evidence that the error monitoring system maps observed errors of different magnitude according to fine-grain, graded rather than all-or-none rules.

Measuring mimicry: general corticospinal facilitation during observation of naturalistic behaviour.

Mimicry of others' postures and behaviours forms an implicit yet indispensable component of social interactions. However, whereas numerous behavioural studies have investigated the occurrence of mimicry and its social sensitivity, the underlying neurocognitive mechanisms remain elusive. In this study, single-pulse transcranial magnetic stimulation was used to measure corticospinal facilitation during a naturalistic behaviour observation task adapted from the behavioural mimicry literature. Motor evoked potentials (MEPs) in participants' right hands were measured as they observed stimulus videos of a confederate describing photographs. MEPs were recorded while confederates were and were not carrying out hand and leg behaviours that also differed in spatial extent (i.e. large behaviours: face rubbing and leg crossing; small behaviours: finger tapping and foot bouncing). Importantly, the cover task instructions did not refer to the behaviours but instead required participants to focus on the confederates' photograph descriptions in order to later perform a recognition test. A general arousal effect was found, with higher MEPs during stimulus video observation than during a fixation-cross baseline, regardless of whether or not the confederate was carrying out a behaviour at the time of the pulse. When controlling for this general arousal effect, results showed that MEPs during observation of the larger two behaviours were significantly higher than the smaller two behaviours, irrespective of effector. Thus, using a controlled yet naturalistic paradigm, this study suggests that general sensorimotor arousal during social interactions could play a role in implicit behavioural mimicry.

Seeing pain and pleasure on self and others: behavioral and psychophysiological reactivity in immersive virtual reality.

Studies have explored behavioral and neural responses to the observation of pain in others. However, much less is known about how taking a physical perspective influences reactivity to the observation of others' pain and pleasure. To explore this issue we devised a novel paradigm in which 24 healthy participants immersed in a virtual reality scenario observed a virtual: needle penetrating (pain), caress (pleasure), or ball touching (neutral) the hand of an avatar seen from a first (1PP)- or a third (3PP)-person perspective. Subjective ratings and physiological responses [skin conductance responses (SCR) and heart rate (HR)] were collected in each trial. All participants reported strong feelings of ownership of the virtual hand only in 1PP. Subjective measures also showed that pain and pleasure were experienced as more salient than neutral. SCR analysis demonstrated higher reactivity in 1PP than in 3PP. Importantly, vicarious pain induced stronger responses with respect to the other conditions in both perspectives. HR analysis revealed equally lower activity during pain and pleasure with respect to neutral. SCR may reflect egocentric perspective, and HR may merely index general arousal. The results suggest that behavioral and physiological indexes of reactivity to seeing others' pain and pleasure were qualitatively similar in 1PP and 3PP. Our paradigm indicates that virtual reality can be used to study vicarious sensation of pain and pleasure without actually delivering any stimulus to participants' real body and to explore behavioral and physiological reactivity when they observe pain and pleasure from ego- and allocentric perspectives.

Electrocortical signatures of detecting errors in the actions of others: An EEG study in pianists, non-pianist musicians and musically naïve people.

Detecting others' action errors plays a critical role in social life. Studies indicate that executing action errors and observing other's errors activate a specific cerebral system specialized for performance monitoring and detecting mismatches between an internal model of the action and the executed/observed one. Such a system may be particularly important for highly skilled performance. By recording electro-encephalographic (EEG) activity in expert pianists, non-pianist musicians and musically naïve individuals while they observed correct or incorrect mute piano sequences, we explored the link between sensorimotor expertise, the ability to detect another's erroneous action (indexed by positivity error, Pe) and action simulation (indexed by mu frequency suppression). Superior error detection in pianists was paralleled by a larger Pe, hinting at the selective activation of the parietal error-monitoring system in visuo-motor experts. Moreover, only in pianists did action observation induce left lateralized mu suppression in the 10-12 Hz band, reflecting somatotopic sensorimotor simulation. A mediation analysis showed that mu suppression and performance (indexed by d') were mediated by Pe amplitude, indicating that the higher the simulation, the higher the sensitivity to errors for large Pe amplitude. This study shows that specific electrocortical indices link motor simulation and detection of errors in the actions of others.

Influence of warmth and competence on the promotion of safe in-group selection: Stereotype content model and social categorization of faces.

Categorizing an individual as a friend or foe plays a pivotal role in navigating the social world. According to the stereotype content model (SCM), social perception relies on two fundamental dimensions, warmth and competence, which allow us to process the intentions of others and their ability to enact those intentions, respectively. Social cognition research indicates that, in categorization tasks, people tend to classify other individuals as more likely to belong to the out-group than the in-group (in-group overexclusion effect, IOE) when lacking diagnostic information, probably with the aim of protecting in-group integrity. Here, we explored the role of warmth and competence in group-membership decisions by testing 62 participants in a social-categorization task consisting of 150 neutral faces. We assessed whether (a) warmth and competence ratings could predict the in-group/out-group categorization, and (b) the reliance on these two dimensions differed in low-IOE versus high-IOE participants. Data showed that high ratings of warmth and competence were necessary to categorize a face as in-group. Moreover, while low-IOE participants relied on warmth, high-IOE participants relied on competence. This finding suggests that the proneness to include/exclude unknown identities in/from one's own in-group is related to individual differences in the reliance on SCM social dimensions. Furthermore, the primacy of the warmth effect seems not to represent a universal phenomenon adopted in the context of social evaluation.

Re-establishing the disrupted sensorimotor loop in deafferented and deefferented people: The case of spinal cord injuries.

Acting efficiently in the world depends on the activity of motor and somatosensory systems, the integration of which is necessary for the proper functioning of the sensorimotor loop (SL). Profound alterations of SL functioning follow spinal cord injury (SCI), a condition that brings about a disconnection of the body from the brain. Such disconnection creates a substantial deprivation of somatosensorial inputs and motor outputs. Consequent somatic deficits and motor paralysis affect the body below the lesion level. A complete restoration of normal functions of the SL cannot be expected until basic neuroscience has found a way to re-establish the interrupted neural connectivity. Meanwhile, studies should focus on the development of technical solutions for dealing with the disruption of the sensorimotor loop. This review discusses the structural and functional adaptive reorganization of the brain after SCI, and the maladaptive mechanisms that impact on the processing of body related information, which alter motor imagery strategies and EEG signals. Studies that show how residual functions (e.g. face tactile sensitivity) may help people to restore a normal body image are also reviewed. Finally, data on how brain and residual body signals may be used to improve brain computer interface systems is discussed in relation to the issue of how such systems may help SCI people to re-enter the world and interact with objects and other individuals.

Mere observation of body discontinuity affects perceived ownership and vicarious agency over a virtual hand.

The mental representation of one's body typically implies the continuity of its parts. Here, we used immersive virtual reality to explore whether mere observation of visual discontinuity between the hand and limb of an avatar could influence a person's sense of ownership of the virtual body (feeling of ownership, FO) and being the agent of its actions (vicarious agency, VA). In experiment 1, we tested whether placing different amounts of visual discontinuity between a virtual hand and limb differently modulate the perceived FO and VA. Participants passively observed from a first-person perspective four different versions of a virtual limb: (1) a full limb; a hand detached from the proximal part of the limb because of deletion of (2) the wrist; (3) the wrist and forearm; (4) and the wrist, forearm and elbow. After observing the static or moving virtual limb, participants reported their feeling of ownership (FO) and vicarious agency (VA) over the hand. We found that even a small visual discontinuity between the virtual hand and arm significantly decreased participants' FO over the hand during observation of the static limb. Moreover, in the same condition, we found that passive observation of the avatar's actions induced a decrease in both FO and VA. We replicated the same results in a second study (experiment 2) where we investigated the modulation of FO and VA by comparing the visual body discontinuity with a condition in which the virtual limb was partially occluded. Our data show that mere observation of limb discontinuity can change a person's ownership and agency over a virtual body observed from a first-person perspective, even in the absence of any multisensory stimulation of the real body. These results shed new light on the role of body visual continuity in modulating self-awareness and agency in immersive virtual reality.

Weighing the stigma of weight: An fMRI study of neural reactivity to the pain of obese individuals.

Explicit negative attitudes and blameful beliefs (e.g. poor diet, laziness) towards obese individuals are well documented and are pervasive even among health professionals. Here we sought to determine whether obesity stigma is reflected in a fundamental feature of intersubjectivity namely the automatic neural resonance with others' affective experiences. During fMRI, normal-weight female participants observed short clips depicting normal-weight (NW) and obese (Ob) models experiencing pain. Importantly, participants believed that half of the Ob were overweight due to a hormonal disorder (HormOb) and ignored the cause of obesity of the remaining models (Unknown obese models; UnkOb). Analyses of hemodynamic responses showed reduced activity to the pain of Ob compared to that of NW in areas associated with pain processing and early visual processing. The comparison between the two Ob conditions revealed a further decrease of activity to HormOb's pain compared to UnkOb's (and NW) pain in the right inferior frontal gyrus, an area associated with emotional resonance. Our study demonstrates that stigma for obese individuals can be observed at implicit levels, and that it is modulated by knowledge concerning the etiology of obesity, with the seemingly surprising result that obesity due to disease may result in greater stigmatization. Moreover, the perceived similarity with the models and the ambivalent emotion of pity may index biased brain responses to obese individuals' pain. The study highlights a possibly important neural link between resonance with the pain of others and obesity stigma.

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.

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.

The primary somatosensory cortex largely contributes to the early part of the cortical response elicited by nociceptive stimuli.

Research on the cortical sources of nociceptive laser-evoked brain potentials (LEPs) began almost two decades ago (Tarkka and Treede, 1993). Whereas there is a large consensus on the sources of the late part of the LEP waveform (N2 and P2 waves), the relative contribution of the primary somatosensory cortex (S1) to the early part of the LEP waveform (N1 wave) is still debated. To address this issue we recorded LEPs elicited by the stimulation of four limbs in a large population (n=35). Early LEP generators were estimated both at single-subject and group level, using three different approaches: distributed source analysis, dipolar source modeling, and probabilistic independent component analysis (ICA). We show that the scalp distribution of the earliest LEP response to hand stimulation was maximal over the central-parietal electrodes contralateral to the stimulated side, while that of the earliest LEP response to foot stimulation was maximal over the central-parietal midline electrodes. Crucially, all three approaches indicated hand and foot S1 areas as generators of the earliest LEP response. Altogether, these findings indicate that the earliest part of the scalp response elicited by a selective nociceptive stimulus is largely explained by activity in the contralateral S1, with negligible contribution from the secondary somatosensory cortex (S2).

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.

Motor imagery beyond the joint limits: a transcranial magnetic stimulation study.

The processes and neural bases used for motor imagery are also used for the actual execution of correspondent movements. Humans, however, can imagine movements they cannot perform. Here we explored whether plausibility of movements is mapped on the corticospinal motor system and whether the process is influenced by visuomotor vs. kinesthetic-motor first person imagery strategy. Healthy subjects imagined performing possible or biomechanically impossible right index finger movements during single pulse TMS of the left motor cortex. We found an increase of corticospinal excitability during motor imagery which was higher for impossible than possible movements and specific for the muscle involved in the actual execution of the imagined movement. We expand our previous action observation studies, suggesting that the plausibility of a movement is computed in regions upstream the primary motor cortex, and that motor imagery is a higher-order process not fully constrained by the rules that govern motor execution.

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.