An immersive virtual reality tool for assessing left and right unilateral spatial neglect.

The reported rate of the occurrence of unilateral spatial neglect (USN) is highly variable likely due to the lack of validity and low sensitivity of classical tools used to assess it. Virtual reality (VR) assessments try to overcome these limitations by proposing immersive and complex environments. Nevertheless, existing VR-based tasks are mostly focused only on near space and lack analysis of psychometric properties and/or clinical validation. The present study evaluates the clinical validity and sensitivity of a new immersive VR-based task to assess USN in the extra-personal space and examines the neuronal correlates of deficits of far space exploration. The task was administrated to two groups of patients with right (N = 28) or left (N = 11) hemispheric brain lesions, also undergoing classical paper-and-pencil assessment, as well as a group of healthy participants. Our VR-based task detected 44% of neglect cases compared to 31% by paper-and-pencil tests in the total sample. Importantly, 30% of the patients (with right or left brain lesions) with no clear sign of USN on the paper-and-pencil tests performed outside the normal range in the VR-based task. Voxel lesion-symptom mapping revealed that deficits detected in VR were associated with lesions in insular and temporal cortex, part of the neural network involved in spatial processing. These results show that our immersive VR-based task is efficient and sensitive in detecting mild to strong manifestations of USN affecting the extra-personal space, which may be undetected using standard tools.

An immersive virtual reality system for ecological assessment of peripersonal and extrapersonal unilateral spatial neglect.

BACKGROUND: Unilateral spatial neglect (USN) is a debilitating neuropsychological syndrome that often follows brain injury, in particular a stroke affecting the right hemisphere. In current clinical practice, the assessment of neglect is based on old-fashioned paper-and-pencil and behavioral tasks, and sometimes relies on the examiner's subjective judgment. Therefore, there is a need for more exhaustive, objective and ecological assessments of USN. METHODS: In this paper, we present two tasks in immersive virtual reality to assess peripersonal and extrapersonal USN. The tasks are designed with several levels of difficulty to increase sensitivity of the assessment. We then validate the feasibility of both assessments in a group of healthy adult participants. RESULTS: We report data from a study with a group of neurologically unimpaired participants (N = 39). The results yield positive feedback on comfort, usability and design of the tasks. We propose new objective scores based on participant's performance captured by head gaze and hand position information, including, for instance, time of exploration, moving time towards left/right and time-to-reach, which could be used for the evaluation of the attentional spatial bias with neurological patients. Together with the number of omissions, the new proposed parameters can result in lateralized index ratios as a measure of asymmetry in space exploration. CONCLUSIONS: We presented two innovative assessments for USN based on immersive virtual reality, evaluating the far and the near space, using ecological tasks in multimodal, realistic environments. The proposed protocols and objective scores can help distinguish neurological patients with and without USN.

Movement-Related Cortical Potentials in Embodied Virtual Mirror Visual Feedback.

Background: Mirror therapy is thought to drive interhemispheric communication, resulting in a balanced activation. We hypothesized that embodied virtual mirror visual feedback (VR-MVF) presented on a computer screen may produce a similar activation. In this proof-of-concept study, we investigated differences in movement-related cortical potentials (MRCPs) in the electroencephalogram (EEG) from different visual feedback of user movements in 1 stroke patient and 13 age-matched adults. Methods: A 60-year-old right-handed (Edinburgh score >95) male ischemic stroke [left paramedian pontine, National Institutes of Health Stroke Scale (NIHSS) = 6] patient and 13 age-matched right-handed (Edinburgh score >80) healthy adults (58 ± 9 years; six female) participated in the study. We recorded 16-electrode electroencephalogram (EEG), while participants performed planar center-out movements in two embodied visual feedback conditions: (i) direct (movements translated to the avatar's ipsilateral side) and (ii) mirror (movements translated to the avatar's contralateral side) with left (direct left/mirror left) or right (direct right/mirror right) arms. Results: As hypothesized, we observed more balanced MRCP hemispheric negativity in the mirror right compared to the direct right condition [statistically significant at the FC4 electrode; 99.9% CI, (0.81, 13)]. MRCPs in the stroke participant showed reduced lateralized negativity in the direct left (non-paretic) situation compared to healthy participants. Interestingly, the potentials were stronger in the mirror left (non-paretic) compared to direct left case, with significantly more bilateral negativity at FC3 [95% CI (0.758 13.2)] and C2 [95% CI (0.04 9.52)]. Conclusions: Embodied mirror visual feedback is likely to influence bilateral sensorimotor cortical subthreshold activity during movement preparation and execution observed in MRCPs in both healthy participants and a stroke patient.

Brain-computer interfaces and virtual reality for neurorehabilitation.

Brain-computer interfaces (BCIs) and virtual reality (VR) are two technologic advances that are changing our way of interacting with the world. BCIs can be used to influence and can serve as a control mechanism in navigation tasks, communication, or other assistive functions. VR can create ad hoc interactive scenarios that involve all our senses, stimulate the brain in a multisensory fashion, and increase the motivation and fun with game-like environments. VR and motion tracking enable natural human-computer interaction at cognitive and physical levels. This includes both brain and body in the design of meaningful VR experiences; these cases in which participants feel naturally present could help augment the benefits of BCIs for assistive and neurorehabilitation applications for the relearning of motor and cognitive skills. VR technology is now available at the consumer level thanks to the proliferation of affordable head-mounted displays (HMDs). Merging both technologies into simplified, practical devices may help democratize these technologies.

Virtual reality experiences, embodiment, videogames and their dimensions in neurorehabilitation.

BACKGROUND: In the context of stroke rehabilitation, new training approaches mediated by virtual reality and videogames are usually discussed and evaluated together in reviews and meta-analyses. This represents a serious confounding factor that is leading to misleading, inconclusive outcomes in the interest of validating these new solutions. MAIN BODY: Extending existing definitions of virtual reality, in this paper I put forward the concept of virtual reality experience (VRE), generated by virtual reality systems (VRS; i.e. a group of variable technologies employed to create a VRE). Then, I review the main components composing a VRE, and how they may purposely affect the mind and body of participants in the context of neurorehabilitation. In turn, VRS are not anymore exclusive from VREs but are currently used in videogames and other human-computer interaction applications in different domains. Often, these other applications receive the name of virtual reality applications as they use VRS. However, they do not necessarily create a VRE. I put emphasis on exposing fundamental similarities and differences between VREs and videogames for neurorehabilitation. I also recommend describing and evaluating the specific features encompassing the intervention rather than evaluating virtual reality or videogames as a whole. CONCLUSION: This disambiguation between VREs, VRS and videogames should help reduce confusion in the field. This is important for databases searches when looking for specific studies or building metareviews that aim at evaluating the efficacy of technology-mediated interventions.

Virtual Reality as a Vehicle to Empower Motor-Cognitive Neurorehabilitation.

In this paper, we advocate the combination of four key ingredients that we believe are necessary to design long-lasting effective treatments for neurorehabilitation: (i) motor-cognitive training, (ii) evidence-based neuroscience principles, in particular those related to body perception, (iii) motivational games, and (iv) empowerment techniques. Then, we propose virtual reality (VR) as the appropriate medium to encompass all the requirements mentioned above. VR is arguably one of the most suitable technologies for neurorehabilitation able to integrate evidence-based neurorehabilitation techniques and neuroscience principles into motivating training approaches that promote self-management by empowering patients to own their recovery process. We discuss the advantages and challenges of such an approach on several exemplary applications and outline directions for future developments. We strongly believe that the combination of positive psychology and positive technology mediated by VR-based interventions can heavily impact the rehabilitation outcomes of motor-cognitive functions along all the stages of the rehabilitation path.

Selective distortion of body image by asynchronous visuotactile stimulation.

In the rubber hand illusion (RHI), a rubber hand is felt as being part of one's body. This illusion is evoked by providing synchronous visuotactile stimulation to the fake and real hands. Asynchronous visuotactile stimulation is known not to produce such an illusion of ownership, being commonly used as the control condition. Here we explored the impact of synchronous and asynchronous visuotactile stimulation on the body image. We combined the induction of the RHI with a quantitative test for the internal representation of body metrics (i.e., the positions of key fiducial points on the body relative to each other). We found a significant recalibration of the upper/lower arm lengths following asynchronous visuotactile stimulation. In particular, we observed a selective elongation of the lower arm, a distortion typical of deafferentation. Conversely, synchronous visuotactile stimulation did not alter the estimation of the arm segments' length. Our findings are consistent with a dynamic internal representation of body image that is continuously updated based on incoming multisensory information. Furthermore, the use of asynchronous multisensory stimulation as a neutral condition should be reconsidered since it introduces changes in the body image.

Increasing upper limb training intensity in chronic stroke using embodied virtual reality: a pilot study.

BACKGROUND: Technology-mediated neurorehabilitation is suggested to enhance training intensity and therefore functional gains. Here, we used a novel virtual reality (VR) system for task-specific upper extremity training after stroke. The system offers interactive exercises integrating motor priming techniques and embodied visuomotor feedback. In this pilot study, we examined (i) rehabilitation dose and training intensity, (ii) functional improvements, and (iii) safety and tolerance when exposed to intensive VR rehabilitation. METHODS: Ten outpatient stroke survivors with chronic (>6 months) upper extremity paresis participated in a ten-session VR-based upper limb rehabilitation program (2 sessions/week). RESULTS: All participants completed all sessions of the treatment. In total, they received a median of 403 min of upper limb therapy, with 290 min of effective training. Within that time, participants performed a median of 4713 goal-directed movements. Importantly, training intensity increased progressively across sessions from 13.2 to 17.3 movements per minute. Clinical measures show that despite being in the chronic phase, where recovery potential is thought to be limited, participants showed a median improvement rate of 5.3% in motor function (Fugl-Meyer Assessment for Upper Extremity; FMA-UE) post intervention compared to baseline, and of 15.4% at one-month follow-up. For three of them, this improvement was clinically significant. A significant improvement in shoulder active range of motion (AROM) was also observed at follow-up. Participants reported very low levels of pain, stress and fatigue following each session of training, indicating that the intensive VR intervention was well tolerated. No severe adverse events were reported. All participants expressed their interest in continuing the intervention at the hospital or even at home, suggesting high levels of adherence and motivation for the provided intervention. CONCLUSIONS: This pilot study showed how a dedicated VR system could deliver high rehabilitation doses and, importantly, intensive training in chronic stroke survivors. FMA-UE and AROM results suggest that task-specific VR training may be beneficial for further functional recovery both in the chronic stage of stroke. Longitudinal studies with higher doses and sample sizes are required to confirm the therapy effectiveness. TRIAL REGISTRATION: This trial was retrospectively registered at ClinicalTrials.gov database (registration number NCT03094650 ) on 14 March 2017.

Virtual reality for assessment of patients suffering chronic pain: a case study.

The study of body representation and ownership has been a very active research area in recent years. Synchronous multisensory stimulation has been used for the induction of the illusion of ownership over virtual body parts and even full bodies, and it has provided experimental paradigms for the understanding of the brain processing of body representation. However, the illusion of ownership of a virtual body has rarely been used for patient evaluation and diagnosis. Here we propose a method that exploits ownership of a virtual body in combination with a simple brain computer interface (BCI) and basic physiological measures to complement neurological assessment. A male patient presenting a fixed posture dystonia featuring a permanently closed left fist participated in this case study. The patient saw a virtual body that substituted his own after donning a head-mounted display and thereby entering the virtual reality. The left virtual hand had the same posture as his corresponding real hand. After inducing virtual hand ownership by correlated visuo-tactile stimulation and dynamic reflections in a virtual mirror, the virtual hand would open either automatically or through a cognitive task assessed through a BCI that required him to focus attention on the virtual hand. The results reveal that body ownership induced changes on electromyography and BCI performance in the patient that were different from those in five healthy controls. Overall, the case study shows that the induction of virtual body ownership combined with simple electrophysiological measures could be useful for the diagnosis of patients with neurological conditions.

A fully immersive set-up for remote interaction and neurorehabilitation based on virtual body ownership.

Although telerehabilitation systems represent one of the most technologically appealing clinical solutions for the immediate future, they still present limitations that prevent their standardization. Here we propose an integrated approach that includes three key and novel factors: (a) fully immersive virtual environments, including virtual body representation and ownership; (b) multimodal interaction with remote people and virtual objects including haptic interaction; and (c) a physical representation of the patient at the hospital through embodiment agents (e.g., as a physical robot). The importance of secure and rapid communication between the nodes is also stressed and an example implemented solution is described. Finally, we discuss the proposed approach with reference to the existing literature and systems.

Is my hand connected to my body? The impact of body continuity and arm alignment on the virtual hand illusion.

When a rubber hand is placed on a table top in a plausible position as if part of a person's body, and is stroked synchronously with the person's corresponding hidden real hand, an illusion of ownership over the rubber hand can occur (Botvinick and Cohen 1998). A similar result has been found with respect to a virtual hand portrayed in a virtual environment, a virtual hand illusion (Slater et al. 2008). The conditions under which these illusions occur have been the subject of considerable study. Here we exploited the flexibility of virtual reality to examine four contributory factors: visuo-tactile synchrony while stroking the virtual and the real arms, body continuity, alignment between the real and virtual arms, and the distance between them. We carried out three experiments on a total of 32 participants where these factors were varied. The results show that the subjective illusion of ownership over the virtual arm and the time to evoke this illusion are highly dependent on synchronous visuo-tactile stimulation and on connectivity of the virtual arm with the rest of the virtual body. The alignment between the real and virtual arms and the distance between these were less important. It was found that proprioceptive drift was not a sensitive measure of the illusion, but was only related to the distance between the real and virtual arms.

Writing through a robot: a proof of concept for a brain-machine interface.

This paper describes a non-invasive human brain-actuated robotic arm experiment, which allows remote writing. In the local environment, the participant decides on an arbitrary word to transmit. A mental speller interface is then used to select the letters. A robot arm placed in the remote environment writes the word on a whiteboard in real time. A multidisciplinary framework such as the one presented here exemplifies a class of interactive applications with possible relevance in a variety of fields, such as entertainment and clinical environments.

Inducing illusory ownership of a virtual body.

We discuss three experiments that investigate how virtual limbs and bodies can come to feel like real limbs and bodies. The first experiment shows that an illusion of ownership of a virtual arm appearing to project out of a person's shoulder can be produced by tactile stimulation on a person's hidden real hand and synchronous stimulation on the seen virtual hand. The second shows that the illusion can be produced by synchronous movement of the person's hidden real hand and a virtual hand. The third shows that a weaker form of the illusion can be produced when a brain-computer interface is employed to move the virtual hand by means of motor imagery without any tactile stimulation. We discuss related studies that indicate that the ownership illusion may be generated for an entire body. This has important implications for the scientific understanding of body ownership and several practical applications.

Inducing a virtual hand ownership illusion through a brain-computer interface.

The apparently stable brain representation of our bodies is easily challenged. We have recently shown that the illusion of ownership of a three-dimensional virtual hand can be evoked through synchronous tactile stimulation of a person's hidden real hand and that of the virtual hand. This reproduces the well-known rubber-hand illusion, but in virtual reality. Here we show that some aspects of the illusion can also occur through motor imagery used to control movements of a virtual hand. When movements of the virtual hand followed motor imagery, the illusion of ownership of the virtual hand was evoked and muscle activity measured through electromyogram correlated with movements of the virtual arm. Using virtual bodies has a great potential in the fields of physical and neural rehabilitation, making the understanding of ownership of a virtual body highly relevant.

Quantification of cognitive-induced brain activity: an efficient method for online applications.

Electrical brain responses during performance of cognitive tasks contain not only evoked, but also induced activity reflecting different processes. These activities are often partially overlapped in time and frequency, so that they are even more difficult to be separated in single-trial. Therefore, online applications based on induced brain activity require specific online processing methods to separate both activities efficiently. Here we propose a module-based methodology for the online extraction and quantification of induced brain activity during cognitive-related tasks. Further, the role of electrode montages and the minimization of the evoked activity are examined in both simulated and real data as part of the optimization process.

Towards a digital body: the virtual arm illusion.

The integration of the human brain with computers is an interesting new area of applied neuroscience, where one application is replacement of a person's real body by a virtual representation. Here we demonstrate that a virtual limb can be made to feel part of your body if appropriate multisensory correlations are provided. We report an illusion that is invoked through tactile stimulation on a person's hidden real right hand with synchronous virtual visual stimulation on an aligned 3D stereo virtual arm projecting horizontally out of their shoulder. An experiment with 21 male participants showed displacement of ownership towards the virtual hand, as illustrated by questionnaire responses and proprioceptive drift. A control experiment with asynchronous tapping was carried out with a different set of 20 male participants who did not experience the illusion. After 5 min of stimulation the virtual arm rotated. Evidence suggests that the extent of the illusion was also correlated with the degree of muscle activity onset in the right arm as measured by EMG during this period that the arm was rotating, for the synchronous but not the asynchronous condition. A completely virtual object can therefore be experienced as part of one's self, which opens up the possibility that an entire virtual body could be felt as one's own in future virtual reality applications or online games, and be an invaluable tool for the understanding of the brain mechanisms underlying body ownership.