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Neuroscience of Virtual Reality: From Virtual Exposure to Embodied Medicine

Neuroscience of Virtual Reality: From Virtual Exposure to Embodied Medicine Is virtual reality (VR) already a reality in behavioral health? To answer this question, a meta-review was conducted to assess the meta-analyses and systematic and narrative reviews published in this field in the last twenty-two months. Twenty-five different articles demonstrated the clinical potential of this technology in both the diagnosis and the treatment of mental health disorders: VR compares favorably to existing treatments in anxiety disorders, eating and weight disorders, and pain management, with long-term effects that generalize to the real world. But why is VR so effective? Here, the following answer is suggested: VR shares with the brain the same basic mechanism: embodied simulations. According to neuroscience, to regulate and control the body in the world effectively, the brain creates an embodied simulation of the body in the world used to represent and predict actions, concepts, and emotions. VR works in a similar way: the VR experience tries to predict the sensory consequences of an individual’s movements, providing to him/her the same scene he/she will see in the real world. To achieve this, the VR system, like the brain, maintains a model (simulation) of the body and the space around it. If the presence in the body is the outcome of different embodied simulations, concepts are embodied simulations, and VR is an embodied technology, this suggests a new clinical approach discussed in this article: the possibility of altering the experience of the body and facilitating cognitive modeling/change by designing targeted virtual environments able to simulate both the external and the internal world/body. Virtual Reality in Behavioral Health: A Meta-Review contribution in many different areas, from anxiety and eating disorders to psychosis and addiction. his special issue presented and discussed different The most common use of VR in behavioral health is for Tvirtual reality (VR) applications for behavioral health. But exposure therapy (VR exposure [VRE]). VRE is similar to 10,16,26 is VR already a reality in behavioral health? To answer this classic exposure therapy —the patient is exposed to a question, a meta-review was conducted to assess the meta- graded exposure hierarchy—with the only difference being analyses and systematic and narrative reviews (see Fig. 1 for that VR is substituted for other exposure techniques (e.g., the methodology) published in this field in the last 22 months. in vivo or imaginal exposure). In the treatment of complex 1–25 Twenty-five different articles (see Table 1 for the ar- anxiety disorders, the use of VRE is often combined with ticles’ list and a summary of their conclusions) demonstrated other techniques such as breathing or relaxation exercises, 28 29,30 the clinical potential of this technology in both the diagno- attentional and autonomic control training, biofeedback, sis and the treatment of mental health disorders. Nine arti- and/or cognitive restructuring. 1,2,6,9,14,15,19,18,22 11,16 5,8,10 cles reviewed the available literature on the Five articles, including a meta-analysis, spe- effectiveness of VR in psychiatric/mental health treatment. cifically explored the use of VRE in the treatment of anx- All of the articles suggest that VR is suitable for the treat- iety disorders. The available data show that VR is able to ment of mental health problems and could make an important reduce anxiety symptoms significantly in different anxiety Applied Technology for Neuro-Psychology Lab, IRCCS Istituto Auxologico Italiano, Milan, Italy. Department of Psychology, Universita` Cattolica del Sacro Cuore, Milan, Italy. Virtual Reality Medical Center, La Jolla, California. Virtual Reality Medical Institute, Brussels, Belgium. Department of Human Sciences for Education, Universita` degli Studi di Milano-Bicocca, Milan, Italy. ª Giuseppe Riva et al. 2019; Published by Mary Ann Liebert, Inc. This Open Access article is distributed under the terms of the Creative Commons License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. 82 NEUROSCIENCE OF VIRTUAL REALITY 83 Articles identified through database Number of duplicates (N = 345) searching (N = 1,220) Articles not meeting inclusion Articles screened after duplicates removed (N = 875) criteria (N = 848) Reasons for exclusion: review had Full-text articles assessed for a limited focus on virtual reality eligibility (N =27) (N =2) Studies included in qualitative synthesis (N = 25) FIG. 1. Meta-review methodology. Using the Google Scholar and Scopus databases, a systematic search was conducted to identify reviews (both systematic and narrative) and meta-analyses that reported on the effects of virtual reality (VR) in the assessment and treatment in behavioral health: anxiety disorders, pain management, schizophrenia spectrum disorders, eating and weight disorders, autism spectrum disorders, personality disorders, and substance use disorders. Guidelines for conducting a systematic review discussed by Uman were followed. The ‘‘free-form’’ question was as follows: ‘‘Do virtual environments perform equal-to-or-better-than traditional modalities in behavioral health?’’ The outcome of interest was reviews and meta-analyses answering this question in any area of behavioral health. The following search terms were used: ((‘‘Virtual Reality’’ AND (‘‘Review’’ OR ‘‘Meta-analysis’’ OR ‘‘metaanalysis’’)) AND (‘‘anxiety’’ OR ‘‘phobia’’ OR ‘‘fear’’ OR ‘‘stress’’ OR ‘‘pain’’ OR ‘‘schizophrenia’’ OR ‘‘psychosis’’ OR ‘‘obesity’’ OR ‘‘eating disorders’’ OR ‘‘bu- limia’’ OR ‘‘binge eating’’ OR ‘‘anorexia’’, OR ‘‘autism’’ OR ‘‘Asperger’’ OR ‘‘substance’’ OR ‘‘drug’’ OR ‘‘nicotine’’ OR ‘‘cocaine’’ OR ‘‘opioids’’). The search targeted articles published between November 2, 2016, and August 1, 2018. Inclusion criteria included (a) reviews or meta-analyses, (b) English language journals, and (c) peer-reviewed journals. Exclusion criteria included (a) articles related to the use of VR in surgery or in physical and cognitive rehabilitation; and (b) articles lacking basic information about the selection of the discussed articles. The meta-review flow diagram is shown. 32 33 51,52 disorders: phobias, post-traumatic stress disorders, panic ‘‘body swapping’’ —VR is used to induce the illusory 34 35 disorder and agoraphobia, social anxiety disorders, psy- feeling of ownership of a virtual body with a different shape 36 37 chological stress, and generalized anxiety disorders. and/or size. Even if the number of available controlled stud- The clinical outcome is generally superior to waitlist con- ies is less than for anxiety disorders, the field has rapidly trol conditions and comparable to in vivo exposure-based evolved. Specifically, four different randomized controlled 53 54 interventions. trials—one with eating disorders, one withmorbidobesity, 3,12,13,17,23 55 A second group of five articles evaluated the one with binge-eating, and one with binge-eating and efficacy of VR in the treatment of eating and weight disor- bulimia —have shown after 6-month and 12-month follow- ders. In this field, VR is used in two different ways. First, ups that VR had a higher efficacy than the gold standard in the VR cue exposure to critical stimuli (e.g., food or human field, that is, cognitive–behavioral therapy. 20,21,24 bodies) allows both a reduction in the level of anxiety eli- A third group of three articles analyzed the use of VR cited by them and disruption of the reconsolidation of in pediatric psychology, with a specific focus on VR applica- 39,40 negative memories. Second, VR is used to facilitate the tions for the assessment of children suspected of having autism 41,42 57 58,59 update of existing body representations. According to a spectrum disorder or other neurodevelopmental disorders 43–47 recent theory, eating and weight disorders may be the (e.g., attention-deficit hyperactivity disorder). In this field, dif- outcome of a broader impairment in multisensory body in- ferent from the previous ones, the level of clinical evidence tegration that locks the individuals to an old memory of the available is still low, even if the existing data suggest moderate 48 24 body. In this view, even if the subject is able to lose weight evidence about the effectiveness of VR-based treatments. In after a diet, the multisensory impairment does not allow relation to this topic, another article specifically explored the her/him to experience the new body and reduce the level of use of VR for the assessment of psychiatric disorders, finding body dissatisfaction. VR allows a wrong representation that virtual worlds are able to induce and assess psychiatric of the body to be updated through two different strategies. symptoms simultaneously, with significant correlations be- 49,50 In the first—‘‘reference frame shifting’’ —the subject re- tween VR measures and traditional diagnostic tools. Moreover, experiences in VR a negative situation related to the body VR is also effective in assessing cue reactivity : its use is able 61,62 (e.g., teasing) in both the first and third person (e.g., seeing and to increase subjective craving in smokers, alcohol drink- 63 64 65 supporting her/his avatar in the VR world). In the second— ers, eaters, and cocaine-dependent individuals. 84 Table 1. Meta-Analyses and Systematic and Narrative Reviews Published in the Last 12 Months Related to the Use of Virtual Reality in the Diagnosis and Treatment of Mental Health Disorders Review type Article Included studies Conclusions (from the articles) Systematic Riva G, Ban˜os RM, Botella C, et al. 27 systematic ‘‘The available data support the use of this technology in the treatment meta-review Transforming experience: the potential of reviews and of anxiety disorders, pain management, obesity and eating disorders, augmented reality and virtual reality for meta-analyses and stress-related disorders. But still, there is no clear good quality enhancing personal and clinical change. evidence for or against using VR for the treatment of depression and Frontiers in Psychiatry 2016; 7:164. schizophrenia.’’ Systematic review (mental Freeman D, Reeve S, Robinson A, et al. 285 studies ‘‘VR environments can elicit psychiatric symptoms, manipulation of VR health) Virtual reality in the assessment, can inform the understanding of disorders, and simpler psychological understanding, and treatment of mental treatments can be successfully administered in VR. health disorders. Psychological Medicine The most established finding is that VR exposure-based treatments can 2017; 47:2393–2400. reduce anxiety disorders, but there are numerous research and treatment avenues of promise.’’ Reply to the above systematic Riva G. Letter to the editor: virtual reality in 3 studies ‘‘Three different RCTs have shown at 1-year follow-up that VR for review (eating and weight the treatment of eating and weight eating and weight disorders has a higher efficacy than the gold disorders) disorders. Psychological Medicine 2017; standard in the field, i.e. cognitive–behavioral therapy (CBT).’’ 47:2567–2568. Narrative review (mental Mishkind MC, Norr AM, Katz AC, et al. Not reported ‘‘More research is needed before VRE may be considered standard of health therapy) Review of virtual reality treatment in care in some areas; however, for patients with PTSD or anxiety, and psychiatry: evidence versus current especially patients not responding or not willing to participate in diffusion and use. Current Psychiatry traditional therapy, the use of VRE may be considered as an option. Reports 2017; 19:80. The use of VR for other conditions such as chronic pain, rehabilitation, and addictions also shows clinical promise.’’ Systematic review (mental van Bennekom MJ, de Koning PP, Denys D. 39 studies ‘‘Nearly all VR environments studied were able to simultaneously health assessment) Virtual reality objectifies the diagnosis of provoke and measure psychiatric symptoms. Furthermore, in 14 psychiatric disorders: a literature review. studies, significant correlations were found between VR measures and Frontiers in Psychiatry 2017; 8:163. traditional diagnostic measures. Relatively small clinical sample sizes were used, impeding definite conclusions.’’ Narrative review (anxiety Lindner P, Miloff A, Hamilton W, et al. Not reported ‘‘While having been researched for decades and proven efficacious for disorders) Creating state of the art, next-generation the treatment of anxiety disorders, the pending and ongoing release of virtual reality exposure therapies for consumer-targeted VR hardware platforms signals an opportune time anxiety disorders using consumer to develop the next generation of VR exposure therapies for hardware platforms: design considerations widespread dissemination as self-help applications and integration and future directions. Cognitive Behaviour into regular health care settings.’’ Therapy 2017; 46:404–420. Systematic review (mental Massetti T, Crocetta TB, Silva TDD, et al. 11 studies ‘‘The use of tDCS combined with VR showed positive results in both health) Application and outcomes of therapy healthy and impaired patients including pain management. Future combining transcranial direct current studies with larger sample sizes and homogeneous participants are stimulation and virtual reality: a required to confirm the benefits of tDCS and VR.’’ systematic review. Disability & Rehabilitation: Assistive Technology 2017; 12:551–559. (continued) 85 Table 1. (Continued) Review type Article Included studies Conclusions (from the articles) Systematic review (mental Jerdan SW, Grindle M, van Woerden HC, 82 studies ‘‘Our review demonstrated that VR is effective in provoking realistic health) Kamel Boulos MN. Head-Mounted Virtual reactions to feared stimuli, particularly for anxiety; moreover, it Reality and Mental Health: Critical proved that the immersive nature of VR is an ideal fit for the Review of Current Research. JMIR management of pain. However, the lack of studies surrounding Serious Games 2018; 6:e14. depression and stress highlight the literature gaps that still exist.’’ Systematic review and meta- Arroll B, Wallace HB, Mount V, et al. 16 studies ‘‘A range of therapies are effective for acrophobia in the short term but analysis (acrophobia) A systematic review and meta-analysis not in the long term. Many of the comparative studies showed of treatments for acrophobia. Med J Aust equivalence between therapies, but this finding may be due to a type II 2017; 206:263–267. statistical error. The quality of reporting was poor in most studies.’’ Narrative review (psychosis) Rus-Calafell M, Garety P, Sason E, et al. 50 studies ‘‘Virtual reality is a promising method to be used in the assessment of Virtual reality in the assessment and neurocognitive deficits and the study of relevant clinical symptoms. treatment of psychosis: a systematic Furthermore, preliminary findings suggest that it can be applied to the review of its utility, acceptability and delivery of cognitive rehabilitation, social skills training interventions effectiveness. Psychological Medicine and virtual reality-assisted therapies for psychosis.’’ 2017 Jul 24 [Epub ahead of print]. Systematic reviews (phobias) Botella C, Ferna´ndez-Alvarez J, Guille´nV,etal. 11 studies ‘‘VRET applications have become an effective alternative that can equal Recent progress in virtual reality exposure the results of traditional treatments for phobias from an efficacy point therapy for phobias: a systematic review. of view. However, they are also tools capable of enhancing the Current Psychiatry Reports 2017; 19:42. psychological treatment field.’’ Narrative review (anxiety Maples-Keller JL, Yasinski C, Manjin N, Not reported ‘‘VRE is consistent with models of extinction learning and provides disorders) et al. Virtual reality-enhanced extinction several advantages for use within exposure-based interventions. of phobias and post-traumatic stress. Broadly, extant research provides support for the effectiveness of Neurotherapeutics 2017; 14:554–563. VRE in reducing symptoms of specific phobias and PTSD, with outcomes generally superior to waitlist controls and comparable with traditional exposure therapy.’’ Meta-analysis (flight anxiety) Cardos x RAI, David OA, David, DO. Virtual 11 studies ‘‘Results pointed out significant overall efficiency of VRET in flight reality exposure therapy in flight anxiety: a anxiety at post-test and follow-up. Analysis highlighted the quantitative meta-analysis. Computers in superiority of VRET vs. control conditions at post-test and follow-up Human Behavior 2017; 72:371–380. and the superiority of VRET vs. classical evidence-based interventions at post-test and follow-up.’’ Narrative review (weight Castelnuovo G, Pietrabissa G, Manzoni GM, Not reported ‘‘Another current and future scenario where CBT could be improved in disorders) et al. Cognitive behavioral therapy to aid the management of obesity is represented by virtual reality (VR) weight loss in obese patients: current applications, such as the VR-enhanced CBT that is a sort of enhanced perspectives. Psychology Research & CBT of obesity with a VR module focused on unlocking the negative Behavior Management 2017; 10:165– memory of the body, changing its dysfunctional behavioral correlates, 173. and managing negative emotional states.’’ (continued) 86 Table 1. (Continued) Review type Article Included studies Conclusions (from the articles) Narrative review (weight Paul L, Van Der Heiden C, Hoek HW. Not reported ‘‘Although empirical evidence is still scare, results show that CBT is disorders) Cognitive behavioral therapy and effective in reducing disordered eating disorders and depression in predictors of weight loss in bariatric bariatric patients. New techniques for applying CBR by virtual reality surgery patients. Current Opinion in potentially make CBT more accessible and less costly.’’ Psychiatry 2017; 30:474–479. Systematic review (clinical Dascal J, Reid M, Ishak WW, et al. Virtual 11 studies ‘‘Data from 11 eligible studies provide insight into three current medical medicine) reality and medical inpatients: a applications of VR technology: pain distraction, eating disorders, and systematic review of randomized, cognitive/motor rehabilitation. Overall, a majority of studies from the controlled trials. Innovations in Clinical past decade found VR to be efficacious, easy to use, safe, and Neuroscience 2017; 14:14–21. contributing to high patient satisfaction.’’ Systematic review and meta- Chan E, Foster S, Sambell R, Leong P. 20 studies ‘‘VR may have a role in acutely painful procedures, however included analysis (procedural pain) Clinical efficacy of virtual reality for acute studies were clinically and statistically heterogenous. Further research procedural pain management: A is required to validate findings, establish cost efficacy and optimal systematic review and meta-analysis. clinical settings for usage. Future trials should report in accordance PLoS ONE 2018; 13:e0200987. with established guidelines.’’ Narrative review (clinical Li L, Yu F, Shi D, et al. Application of virtual Not reported ‘‘VR has shown to be effective in reduction of burn-induced pain and medicine) reality technology in clinical medicine. management of pain in other situations. Virtual reality exposure therapy American Journal of Translational and virtual reality cognitive behavior therapy have become effective Research 2017; 9:3867–3880. choices for patients with anxiety disorders and other phobias like fear of flying, claustrophobia, acrophobia or generalized social phobia’’ Narrative review (mental Maples-Keller JL, Bunnell BE, Kim SJ, et al. Not reported ‘‘VR has emerged as a viable tool to help in a number of different health) The use of virtual reality technology in the disorders, with the most strength of evidence for use in exposure treatment of anxiety and other psychiatric therapy for patients with anxiety disorders, cue exposure therapy for disorders. Harvard Review of Psychiatry patients with substance use disorders, and distraction for patients with 2017; 25:103–113. acute pain requiring painful procedures.’’ Systematic review (eating de Carvalho M, Dias T, Duchesne M, et al. 19 studies ‘‘Two different randomized, controlled trials have shown at one-year disorders) Virtual reality as a promising strategy in follow-up that VR had a higher efficacy than the gold standard in the the assessment and treatment of bulimia field, i.e., cognitive behavioral therapy (CBT). In conclusion, based nervosa and binge eating disorder: a on the current available data VR-based environments may be systematic review. Behavioral Sciences considered a promising strategy for the assessment and treatment of 2017; 7:43. BN and BED.’’ Systematic review (clinical Pourmand A, Davis S, Lee D, et al. 45 studies ‘‘These articles provide data, which strongly support the hypothesis that medicine) Emerging utility of virtual reality as a VR simulations can enhance pain management (by reducing patient multidisciplinary tool in clinical medicine. perception of pain and anxiety), can augment clinical training Games for Health Journal 2017; 6:263– curricula and physical rehabilitation protocols (through immersive 270. audiovisual environments), and can improve clinical assessment of cognitive function (through improved ecological validity).’’ (continued) 87 Table 1. (Continued) Review type Article Included studies Conclusions (from the articles) Systematic review (autism) Duffield TC, Parsons TD, Landry A, et al. 5 studies ‘‘Psychometric comparisons of these tools for the neuropsychological Virtual environments as an assessment assessment of pediatric individuals with ASD are lacking as the modality with pediatric ASD populations: current review demonstrated, although the use of VEs. This is a a brief report. Child Neuropsychology particularly important area of future research considering most 2017 Sep 13 [Epub ahead of print]. identification, and thus testing, treatment, and training occur in childhood for ASD.’’ Narrative review (pediatrics) Parsons TD, Riva G, Parsons S, et al. Virtual Not reported ‘‘VR can offer safe, repeatable, and diversifiable interventions that can reality in pediatric psychology. Pediatrics benefit assessments and learning in both typically developing children 2017; 140:S86–S91. and children with disabilities. Research has also pointed to VR’s capacity to reduce children’s experience of aversive stimuli and reduce anxiety levels.’’ Systematic review (autism) Mesa-Gresa P, Gil-Gomez H, Lozano-Quilis 31 studies There is moderate evidence that VR-based treatments can help children JA, Gil-Gomez JA. Effectiveness of with ASD. The lack of definitive findings does not allow us to state virtual reality for children and adolescents that VR-based treatments can improve the results of traditional with autism spectrum disorder: an treatments. Nevertheless, the promising results and the advantages of evidence-based systematic review. Sensors VR (especially considering ASD symptomatology) should encourage (Basel) 2018; 18:pii:E2486. the scientific community to develop new VR-based treatments. Systematic review (eating Clus D, Larsen ME, Lemey C, Berrouiguet 26 studies Overall, VR techniques enable the evaluation of pathological eating disorders) S. The use of virtual reality in patients behaviors and body image distortions. In addition to CBT, use of VR with eating disorders: systematic review. J techniques by patients with eating disorders decreased their negative Med Internet Res 2018; 20:e157. emotional responses to virtual food stimuli or exposure to their body shape. 88 RIVA ET AL. Three final articles explored the use of VR in the assess- achieve benefit from VR therapy. As noted by Price and ment and treatment of psychosis and in pain manage- Anderson, ‘‘The results support presence as a conduit that 6,25 ment. For psychosis, the available studies confirm the enabled phobic anxiety to be expressed during exposure to a efficacy of VR for the multimodal assessment of cognitive virtual environment. However, presence was not supported 7 66 functioning, including social cognition/competence and as contributing to treatment outcome. This suggests feeling hallucinations/paranoid ideations. For treatment, even if present during exposure may be necessary but not sufficient 68–70 92(p750) the available studies are very promising, there is a lack to achieve benefit from VR exposure.’’ of randomized controlled trials demonstrating whether VR is A new argument that is introduced and discussed in this more efficacious or efficient than other interventions. article is that VR shares with the brain the same basic 43,93 In relation to the use of VR for pain management, older mechanism: embodied simulations. 71,72 systematic reviews demonstrated the efficacy of VR 73–75 76 distraction for reducing experimental pain, as well as VR as Simulative Technology 77–79 80–82 the one generated by burn injury care, chronic pain, 83–85 6 94–96 and procedural pain. Hence, the first new one focused An increasingly popular hypothesis—predictive coding — its analysis on the integrated use of VR with brain stimula- suggests that the brain actively maintains an internal model tion (transcranial direct-current stimulation) in pain man- (simulation) of the body and the space around it, which pro- agement. Again, even if the level of clinical evidence is still vides predictions about the expected sensory input and tries to low, a study demonstrated the efficacy of this approach in minimize the amount of prediction errors (or ‘‘surprise’’). An reducing the severity of neuropathic pain and various neu- in-depth discussion of these concepts is not offered here be- ropathic pain subtypes. Finally, the second new one, sug- cause authoritative and thorough accounts have been provided 94–99 gests that VR may have a role in acutely painful procedures, elsewhere. However, herein, the focus is on the concept even if further research is required. of simulation introduced by this paradigm to understand better Overall, this meta-review indicated that VR is a powerful the links between the brain and VR. clinical tool for behavioral health, able to provide effective One of the main tenets of predictive coding is that to assessment and treatment options for a variety of mental regulate and control the body in the world effectively, the health disorders. Specifically, the 25 meta-analyses and brain creates an embodied simulation of the body in the systematic and narrative reviews indicated that VR compares world. There are two main characteristics of this simulation. favorably to existing treatments in anxiety disorders, eating First, different from other internal models used in cognitive and weight disorders, and pain management, with long-term science—such as Tolman’s cognitive maps or Johhson– effects that generalize to the real world. Moreover, they show Laird’s internal models—they are simulations of sensory the potential of VR as assessment tool with practical appli- motor experiences. In this view, they include visceral/auto- cations that range from social and cognitive deficits to ad- nomic (interoceptive), motor (proprioceptive), and sensory diction. Finally, they suggest a clinical potential in the (e.g., visual, auditory) information. Second, embodied sim- treatment of psychosis and in the pediatric field, even if there ulations reactivate multimodal neural networks, which have is no definitive evidence for or against the use of VR. produced the simulated/expected effect before. This approach is used not only for actions, but also for concepts and emotions. Specifically, a concept is a group of The Effectiveness of VR as a Clinical Tool distributed multimodal ‘‘patterns’’ of activity across differ- An open issue not directly addressed by most of these ent populations of neurons (motor, somatosensory, limbic, 100,101 articles is why VR is an effective clinical tool. In many and frontal areas) that support a goal achievement. So, articles, attention is focused on the high level of control and the simulation of a concept involves its reenactment in 1,2,9,10,87 customization allowed by this technology. VR al- modality-specific brain areas. Moreover, the brain uses lows the level of fit between the content of the exposure and emotion concepts to categorize sensations. As underlined by the feared stimuli to be optimized. Moreover, using it, the Barrett, ‘‘That is, the brain constructs meaning by correctly therapist has a total control—limited only by the specific anticipating (predicting and adjusting to) incoming sensa- features of the used software—on the contents of the expe- tions. Sensations are categorized so that they are (a) ac- rience. Finally, it offers a safer and more private context for tionable in a situated way and therefore (b) meaningful, the patient that facilitates his/her engagement. based on past experience. When past experiences of emotion Another important point suggested by different articles is (e.g., happiness) are used to categorize the predicted sensory the level of ‘‘presence’’ provided by the virtual experience. array and guide action, then one experiences or perceives 100(p9) In fact, VR provides a digital place to the individual where that emotion (happiness).’’ In this view, the feeling of he/she can be placed and live a synthetic but realistic expe- presence in a space can be considered as an evolutive tool rience. As noted by some colleagues, VR can be considered used to track the difference between the predicted sensations 89,90 an advanced imaginal system : an advanced form of and those that are incoming from the sensory world, both 93,102,103 imagery that is as effective as reality in inducing experiences externally and internally. and emotions. For example, as demonstrated by a recent VR works in a similar way: it uses computer technology to meta-analysis, presence and anxiety are associated with each create a simulated world that individuals can manipulate and other during VRE therapy for the treatment of anxiety. This explore as if they were in it. In other words, the VR expe- allows a level of self-reflectiveness that is both more pre- rience tries to predict the sensory consequences of your dictable and controllable than the one offered by reality, but movements, showing to you the same scene you will see in higher than the one provided by memory and imagination. the real world. Specifically, VR hardware tracks the motion However, presence alone is necessary but not sufficient to of the user, while VR software adjusts the images on the NEUROSCIENCE OF VIRTUAL REALITY 89 117,118 user’s display to reflect the changes produced by the motion of the brain by directly targeting the processes behind 119–121 in the virtual world. To achieve it, like the brain, the VR system real-world behaviors. maintains a model (simulation) of the body and the space But what is the real clinical potential of VR as an em- around it. This prediction is then used to provide the expected bodied technology? According to neuroscience, the body 105,106,122,123 sensory input using the VR hardware. Obviously, to be realistic, matrix serves to maintain the integrity of the the VR model tries to mimic the brain model as much as body at both the homeostatic and psychological levels by possible: the more the VR model is similar to the brain model, supervising the cognitive and physiological resources nec- 93,104 the more the individual feels present in the VR world. essary to protect the body and the space around it. Specifically, the body matrix plays a critical role in high-end cognitive processes such as motivation, emotion, social cognition, and VR as Embodied Technology 124–126 self-awareness, while exerting a top-down modulation As has just been seen, the brain creates multiple multi- over basic physiological mechanisms such as thermoregula- 100 127,128 123 sensory simulations to predict : (a) upcoming sensory tory control and the immune system. 114,116,129,130 events both inside and outside the body, and (b) the best In this view, different authors have recently action to deal with the impending sensory events. Moseley suggested that an altered functioning of the body matrix and/ et al. suggested that these simulations are integrated with or its related processes might be the cause of different neu- sensory data in the ‘‘body matrix,’’ a coarse supramodal rological and psychiatric conditions. If this is true, VR can multisensory representation of the body and the space around be the core of a new trans-disciplinary research field— 105–107 115,116 it. Specifically, the contents of the body matrix are embodied medicine —the main goal of which is the use defined by top-down predictive signals, integrating the of advanced technology for altering the body matrix, with the multisensory (motor and visceromotor) simulations of the goal of improving people’s health and well-being. causes of perceived sensory events. The different simu- As has been seen in the first section of this article, two 51,52 different VR embodiment techniques—body swapping lations are then ranked and included in the body matrix ac- 49,50 and reference frame shifting —are currentlyusedinthe cording to their relevance for the intentions of the self (selective attention). At the same time, the content and the treatment of eating and weight disorders. The first one, priority of the different simulations are corrected by bottom- body swapping, replaces the contents of the bodily self- up prediction errors that signal mismatches between pre- consciousness with synthetic ones (synthetic embodiment). dicted and actual contents of sensory events. This has been used in eating and weight disorders to im- At the end of this process, the body matrix defines where prove the experience of the body in both clinical (anorexia 131,132 133–135 the self is present, that is, in the body that our brain considers and morbid obesity) and non-clinical subjects. 110–112 136 as the most likely to be its one. As underlined by Apps Nevertheless, the potential of this approach is wider. For and Tsakiris, ‘‘The mental representation of the physical example, it may offer a non-pharmacological way to reduce properties of one’s self are, therefore, also probabilistic. That chronic pain. As has been seen in the first section of this is, one’s own body is the one that has the highest probability article, VR distraction is effectively used to reduce acute pain. of being ‘me,’ since other objects are probabilistically less Nevertheless, according to Tsay et al., ‘‘available findings likely to evoke the same sensory inputs. In short, the notion present compelling evidence for a novel multisensory and that there is a ‘self’ is the most parsimonious and accurate multimodal approach to therapies for chronic pain disor- 137(p249) 110(p88) explanation for sensory inputs.’’ ders’’ In this view, the use of VR embodiment may 138–140 If presence in the body is the outcome of different em- offer new treatment options for pain management. bodied simulations, and VR is a simulation technology, this Some studies have suggested the possibility of using VR body suggests the possibility of altering the experience of the body swapping to improve body perception disturbance in patients 113 141,142 by designing targeted virtual environments. In this view, with complex regional pain syndrome. VR can be defined as an ‘‘embodied technology’’ for its The second technique, reference frame shifting, structures possibility of modifying the embodiment experience of its the individual’s bodily self-consciousness through the focus 114–116 50,143 users. As noted by Riva et al., ‘‘using VR, subjects can and reorganization of its contents (mindful embodiment). experience the synthetic environment as if it was ‘their sur- It has been successfully used in different randomized trials in 54,55 patients with eating and weight disorders to update the rounding world’ (incarnation: the physical body is within a contents of their body memory. But again, its applications are virtual environment) or can experience their synthetic ava- tars as if they were ‘their own body’ (embodiment: the probably wider. For example, Osimo et al. integrated body 1(p9) physical body is replaced by the virtual one).’’ In other swapping (in the avatar of Sigmund Freud) and reference words, VR is able to fool the predictive coding mechanisms frame shifting to improve mood and happiness in a non-clinical used by the brain generating the feeling of presence in a sample. virtual body and in the digital space around it. A final emerging approach is the use of VR to augment the Up to now, VR has been used to simulate external reality, bodily experience through the awareness of internal (and that is, to make people feel ‘‘real’’ what is actually not really difficult to sense) bodily information, or the mapping of a there (i.e., the environment). However, the ability of VR to sensory channel to a different one—for example vision to 144,145 fool the predictive coding mechanisms that regulate the ex- touch or to hearing (augmented embodiment). For ex- perience of the body also allows it to make people feel ample, Suzuki et al. implemented an innovative ‘‘cardiac ‘‘real’’ what they are not. In other words, VR can offer new rubber hand illusion’’ that combined computer-generated ways for structuring, augmenting, and/or replacing the ex- augmented reality with feedback of interoceptive informa- 114–116 perience of the body for clinical goals. Moreover, it tion. Their results showed that the virtual-hand ownership is may offer new embodied ways for assessing the functioning enhanced by cardio-visual feedback in time with the actual 90 RIVA ET AL. heartbeat, supporting the use of this technique to improve The first outcome of an integrated VR platform able to emotion regulation. simulate both the external and the inner world is the possi- bility of structuring, augmenting, and/or replacing all the different experiential aspects of bodily self-consciousness, VR as Cognitive Technology with clinical applications in the treatment of psychiatric 151,152 153–155 disorders, such as depression or schizophrenia, VR is an embodied technology for its ability to modify the 137,156 and neurological disorders, such as chronic pain and experience of the body. However, the body is not simply an 157,158 93,147,148 neglect. object like any other; it has a special status. It is The final long-term outcome of this possibility may be the perceived in a multisensory way, from the outside (ex- embodied virtual training machine described by the science- teroception, the body perceived through the senses) as well fiction thriller The Matrix. In this movie, the heroes, Trinity as from within (inner body, including interoception, the and Neo, learned how to fight martial-arts battles and drive sense of the physiological condition of the body; proprio- motorcycles and helicopters by experiencing the bodily pro- ception, the sense of the position of the body/body segments; cesses and concepts related to the skill through an embodied and vestibular input, the sense of motion of the body) and simulation. from memory. This is true also for the simulative code used by the brain for creating concepts. As has been seen before, it integrates visceral/autonomic (interoceptive), motor (pro- Conclusions prioceptive), and sensory information. If concepts are em- bodied simulations, and VR is an embodied technology, it The first article discussing a VR application in the field of should be possible to facilitate cognitive modeling and behavioral health was published in 1995. Now, more than change by designing targeted virtual environments able to 20 years later, VR is a reality in this field. This is the result of modify concepts both from outside and from inside. a meta-review presented in this article assessing the meta- Nevertheless, there is a critical shortcoming that at the analyses and systematic and narrative reviews published in moment is limiting this possibility: VR simulates the exter- this field in the last 22 months. Twenty-five different articles nal world/body but not the internal one. In fact, actual VR have demonstrated the clinical potential of this technology in technology is very effective in reproducing the exteroceptive both the diagnosis and the treatment of mental health dis- (external) features of the body using vision and hearing, but orders. Specifically, they indicate that VR compares favor- less effective in reproducing the other senses (i.e., touch and ably to existing treatments in anxiety disorders, eating and smell ). It is partially effective in reproducing the propri- weight disorders, and pain management, with long-term ef- oceptive (motor) features of the body using haptic technol- fects that generalize to the real world. ogies, but it is not yet able to reproduce the interoceptive/ But why is VR so effective? Here, the following an- vestibular (internal) features of the body. swer is suggested: VR shares with the brain the same basic Recently, Riva et al. introduced the concept of ‘‘sono- mechanism—embodied simulations. ception,’’ a novel noninvasive technological paradigm based According to neuroscience, to regulate and control the on wearable acoustic and vibrotactile transducers, as a pos- body in the world effectively, the brain creates an embodied sible approach to structure, augment, and/or replace the simulation of the body in the world used to represent and contents of the inner body. This approach should be able to predict actions, concepts, and emotions. Specifically, it is modulate the inner body (interoception, proprioception, and used to predict: (a) upcoming sensory events both inside and vestibular input) through the stimulation of both mechano- outside the body, and (b) the best action to deal with the receptors in different parts of the body—the stomach, the impending sensory events. There are two main charac- heart, the muscles—and the otolith organs of the vestibular teristics of this simulation. First, it simulates sensory motor system (see Fig. 2). experiences, including visceral/autonomic (interoceptive), FIG. 2. The technology of ‘‘sonoception.’’ NEUROSCIENCE OF VIRTUAL REALITY 91 motor (proprioceptive), and sensory (e.g., visual, auditory) Acknowledgments information. Second, embodied simulations reactivate mul- This article was supported by the Italian MIUR research timodal neural networks which have produced the simulated/ project ‘‘Unlocking the memory of the body: Virtual Reality expected effect before. in Anorexia Nervosa’’ (201597WTTM) and by the Italian VR works in a similar way: the VR experience tries to Ministry of Health research project ‘‘High-end and low-end predict the sensory consequences of the individual’s move- virtual reality systems for the rehabilitation of frailty in the ments, providing to him/her the same scene he/she will see in elderly’’ (PE-2013-0235594). the real world. To achieve this, the VR system, like the brain, maintains a model (simulation) of the body and the space Author Disclosure Statement around it. If presence in the body is the outcome of different em- No competing financial interests exist. bodied simulations, and VR is a simulation technology, this suggests the possibility of altering the experience of the References body by designing targeted virtual environments. In this view, VR can be defined as an ‘‘embodied technology’’ for 1. Riva G, Ban˜os RM, Botella C, et al. Transforming expe- its possibility of modifying the embodiment experience of rience: the potential of augmented reality and virtual re- 114–116 its users. In other words, VR is able to fool the pre- ality for enhancing personal and clinical change. Frontiers dictive coding mechanisms used by the brain, generating the in Psychiatry 2016; 7:164. feeling of presence in a virtual body and in the digital space 2. Freeman D, Reeve S, Robinson A, et al. Virtual reality in around it. the assessment, understanding, and treatment of mental health disorders. 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Department of Psychology 158. Lenggenhager B, Loetscher T, Kavan N, et al. Paradoxical Universita Cattolica del Sacro Cuore extension into the contralesional hemispace in spatial Largo Gemelli 1 neglect. Cortex 2012; 48:1320–1328. 159. Rothbaum BO, Hodges LF, Kooper R, et al. Effectiveness 20123, Milan of computer-generated (virtual reality) graded exposure in Italy the treatment of acrophobia. American Journal of Psy- chiatry 1995; 152:626–628. E-mail: giuseppe.riva@unicatt.it http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Cyberpsychology Behavior and Social Networking Pubmed Central

Neuroscience of Virtual Reality: From Virtual Exposure to Embodied Medicine

Cyberpsychology Behavior and Social Networking , Volume 22 (1) – Jan 14, 2019

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Pubmed Central
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© Giuseppe Riva et al. 2019; Published by Mary Ann Liebert, Inc.
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2152-2715
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10.1089/cyber.2017.29099.gri
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Abstract

Is virtual reality (VR) already a reality in behavioral health? To answer this question, a meta-review was conducted to assess the meta-analyses and systematic and narrative reviews published in this field in the last twenty-two months. Twenty-five different articles demonstrated the clinical potential of this technology in both the diagnosis and the treatment of mental health disorders: VR compares favorably to existing treatments in anxiety disorders, eating and weight disorders, and pain management, with long-term effects that generalize to the real world. But why is VR so effective? Here, the following answer is suggested: VR shares with the brain the same basic mechanism: embodied simulations. According to neuroscience, to regulate and control the body in the world effectively, the brain creates an embodied simulation of the body in the world used to represent and predict actions, concepts, and emotions. VR works in a similar way: the VR experience tries to predict the sensory consequences of an individual’s movements, providing to him/her the same scene he/she will see in the real world. To achieve this, the VR system, like the brain, maintains a model (simulation) of the body and the space around it. If the presence in the body is the outcome of different embodied simulations, concepts are embodied simulations, and VR is an embodied technology, this suggests a new clinical approach discussed in this article: the possibility of altering the experience of the body and facilitating cognitive modeling/change by designing targeted virtual environments able to simulate both the external and the internal world/body. Virtual Reality in Behavioral Health: A Meta-Review contribution in many different areas, from anxiety and eating disorders to psychosis and addiction. his special issue presented and discussed different The most common use of VR in behavioral health is for Tvirtual reality (VR) applications for behavioral health. But exposure therapy (VR exposure [VRE]). VRE is similar to 10,16,26 is VR already a reality in behavioral health? To answer this classic exposure therapy —the patient is exposed to a question, a meta-review was conducted to assess the meta- graded exposure hierarchy—with the only difference being analyses and systematic and narrative reviews (see Fig. 1 for that VR is substituted for other exposure techniques (e.g., the methodology) published in this field in the last 22 months. in vivo or imaginal exposure). In the treatment of complex 1–25 Twenty-five different articles (see Table 1 for the ar- anxiety disorders, the use of VRE is often combined with ticles’ list and a summary of their conclusions) demonstrated other techniques such as breathing or relaxation exercises, 28 29,30 the clinical potential of this technology in both the diagno- attentional and autonomic control training, biofeedback, sis and the treatment of mental health disorders. Nine arti- and/or cognitive restructuring. 1,2,6,9,14,15,19,18,22 11,16 5,8,10 cles reviewed the available literature on the Five articles, including a meta-analysis, spe- effectiveness of VR in psychiatric/mental health treatment. cifically explored the use of VRE in the treatment of anx- All of the articles suggest that VR is suitable for the treat- iety disorders. The available data show that VR is able to ment of mental health problems and could make an important reduce anxiety symptoms significantly in different anxiety Applied Technology for Neuro-Psychology Lab, IRCCS Istituto Auxologico Italiano, Milan, Italy. Department of Psychology, Universita` Cattolica del Sacro Cuore, Milan, Italy. Virtual Reality Medical Center, La Jolla, California. Virtual Reality Medical Institute, Brussels, Belgium. Department of Human Sciences for Education, Universita` degli Studi di Milano-Bicocca, Milan, Italy. ª Giuseppe Riva et al. 2019; Published by Mary Ann Liebert, Inc. This Open Access article is distributed under the terms of the Creative Commons License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. 82 NEUROSCIENCE OF VIRTUAL REALITY 83 Articles identified through database Number of duplicates (N = 345) searching (N = 1,220) Articles not meeting inclusion Articles screened after duplicates removed (N = 875) criteria (N = 848) Reasons for exclusion: review had Full-text articles assessed for a limited focus on virtual reality eligibility (N =27) (N =2) Studies included in qualitative synthesis (N = 25) FIG. 1. Meta-review methodology. Using the Google Scholar and Scopus databases, a systematic search was conducted to identify reviews (both systematic and narrative) and meta-analyses that reported on the effects of virtual reality (VR) in the assessment and treatment in behavioral health: anxiety disorders, pain management, schizophrenia spectrum disorders, eating and weight disorders, autism spectrum disorders, personality disorders, and substance use disorders. Guidelines for conducting a systematic review discussed by Uman were followed. The ‘‘free-form’’ question was as follows: ‘‘Do virtual environments perform equal-to-or-better-than traditional modalities in behavioral health?’’ The outcome of interest was reviews and meta-analyses answering this question in any area of behavioral health. The following search terms were used: ((‘‘Virtual Reality’’ AND (‘‘Review’’ OR ‘‘Meta-analysis’’ OR ‘‘metaanalysis’’)) AND (‘‘anxiety’’ OR ‘‘phobia’’ OR ‘‘fear’’ OR ‘‘stress’’ OR ‘‘pain’’ OR ‘‘schizophrenia’’ OR ‘‘psychosis’’ OR ‘‘obesity’’ OR ‘‘eating disorders’’ OR ‘‘bu- limia’’ OR ‘‘binge eating’’ OR ‘‘anorexia’’, OR ‘‘autism’’ OR ‘‘Asperger’’ OR ‘‘substance’’ OR ‘‘drug’’ OR ‘‘nicotine’’ OR ‘‘cocaine’’ OR ‘‘opioids’’). The search targeted articles published between November 2, 2016, and August 1, 2018. Inclusion criteria included (a) reviews or meta-analyses, (b) English language journals, and (c) peer-reviewed journals. Exclusion criteria included (a) articles related to the use of VR in surgery or in physical and cognitive rehabilitation; and (b) articles lacking basic information about the selection of the discussed articles. The meta-review flow diagram is shown. 32 33 51,52 disorders: phobias, post-traumatic stress disorders, panic ‘‘body swapping’’ —VR is used to induce the illusory 34 35 disorder and agoraphobia, social anxiety disorders, psy- feeling of ownership of a virtual body with a different shape 36 37 chological stress, and generalized anxiety disorders. and/or size. Even if the number of available controlled stud- The clinical outcome is generally superior to waitlist con- ies is less than for anxiety disorders, the field has rapidly trol conditions and comparable to in vivo exposure-based evolved. Specifically, four different randomized controlled 53 54 interventions. trials—one with eating disorders, one withmorbidobesity, 3,12,13,17,23 55 A second group of five articles evaluated the one with binge-eating, and one with binge-eating and efficacy of VR in the treatment of eating and weight disor- bulimia —have shown after 6-month and 12-month follow- ders. In this field, VR is used in two different ways. First, ups that VR had a higher efficacy than the gold standard in the VR cue exposure to critical stimuli (e.g., food or human field, that is, cognitive–behavioral therapy. 20,21,24 bodies) allows both a reduction in the level of anxiety eli- A third group of three articles analyzed the use of VR cited by them and disruption of the reconsolidation of in pediatric psychology, with a specific focus on VR applica- 39,40 negative memories. Second, VR is used to facilitate the tions for the assessment of children suspected of having autism 41,42 57 58,59 update of existing body representations. According to a spectrum disorder or other neurodevelopmental disorders 43–47 recent theory, eating and weight disorders may be the (e.g., attention-deficit hyperactivity disorder). In this field, dif- outcome of a broader impairment in multisensory body in- ferent from the previous ones, the level of clinical evidence tegration that locks the individuals to an old memory of the available is still low, even if the existing data suggest moderate 48 24 body. In this view, even if the subject is able to lose weight evidence about the effectiveness of VR-based treatments. In after a diet, the multisensory impairment does not allow relation to this topic, another article specifically explored the her/him to experience the new body and reduce the level of use of VR for the assessment of psychiatric disorders, finding body dissatisfaction. VR allows a wrong representation that virtual worlds are able to induce and assess psychiatric of the body to be updated through two different strategies. symptoms simultaneously, with significant correlations be- 49,50 In the first—‘‘reference frame shifting’’ —the subject re- tween VR measures and traditional diagnostic tools. Moreover, experiences in VR a negative situation related to the body VR is also effective in assessing cue reactivity : its use is able 61,62 (e.g., teasing) in both the first and third person (e.g., seeing and to increase subjective craving in smokers, alcohol drink- 63 64 65 supporting her/his avatar in the VR world). In the second— ers, eaters, and cocaine-dependent individuals. 84 Table 1. Meta-Analyses and Systematic and Narrative Reviews Published in the Last 12 Months Related to the Use of Virtual Reality in the Diagnosis and Treatment of Mental Health Disorders Review type Article Included studies Conclusions (from the articles) Systematic Riva G, Ban˜os RM, Botella C, et al. 27 systematic ‘‘The available data support the use of this technology in the treatment meta-review Transforming experience: the potential of reviews and of anxiety disorders, pain management, obesity and eating disorders, augmented reality and virtual reality for meta-analyses and stress-related disorders. But still, there is no clear good quality enhancing personal and clinical change. evidence for or against using VR for the treatment of depression and Frontiers in Psychiatry 2016; 7:164. schizophrenia.’’ Systematic review (mental Freeman D, Reeve S, Robinson A, et al. 285 studies ‘‘VR environments can elicit psychiatric symptoms, manipulation of VR health) Virtual reality in the assessment, can inform the understanding of disorders, and simpler psychological understanding, and treatment of mental treatments can be successfully administered in VR. health disorders. Psychological Medicine The most established finding is that VR exposure-based treatments can 2017; 47:2393–2400. reduce anxiety disorders, but there are numerous research and treatment avenues of promise.’’ Reply to the above systematic Riva G. Letter to the editor: virtual reality in 3 studies ‘‘Three different RCTs have shown at 1-year follow-up that VR for review (eating and weight the treatment of eating and weight eating and weight disorders has a higher efficacy than the gold disorders) disorders. Psychological Medicine 2017; standard in the field, i.e. cognitive–behavioral therapy (CBT).’’ 47:2567–2568. Narrative review (mental Mishkind MC, Norr AM, Katz AC, et al. Not reported ‘‘More research is needed before VRE may be considered standard of health therapy) Review of virtual reality treatment in care in some areas; however, for patients with PTSD or anxiety, and psychiatry: evidence versus current especially patients not responding or not willing to participate in diffusion and use. Current Psychiatry traditional therapy, the use of VRE may be considered as an option. Reports 2017; 19:80. The use of VR for other conditions such as chronic pain, rehabilitation, and addictions also shows clinical promise.’’ Systematic review (mental van Bennekom MJ, de Koning PP, Denys D. 39 studies ‘‘Nearly all VR environments studied were able to simultaneously health assessment) Virtual reality objectifies the diagnosis of provoke and measure psychiatric symptoms. Furthermore, in 14 psychiatric disorders: a literature review. studies, significant correlations were found between VR measures and Frontiers in Psychiatry 2017; 8:163. traditional diagnostic measures. Relatively small clinical sample sizes were used, impeding definite conclusions.’’ Narrative review (anxiety Lindner P, Miloff A, Hamilton W, et al. Not reported ‘‘While having been researched for decades and proven efficacious for disorders) Creating state of the art, next-generation the treatment of anxiety disorders, the pending and ongoing release of virtual reality exposure therapies for consumer-targeted VR hardware platforms signals an opportune time anxiety disorders using consumer to develop the next generation of VR exposure therapies for hardware platforms: design considerations widespread dissemination as self-help applications and integration and future directions. Cognitive Behaviour into regular health care settings.’’ Therapy 2017; 46:404–420. Systematic review (mental Massetti T, Crocetta TB, Silva TDD, et al. 11 studies ‘‘The use of tDCS combined with VR showed positive results in both health) Application and outcomes of therapy healthy and impaired patients including pain management. Future combining transcranial direct current studies with larger sample sizes and homogeneous participants are stimulation and virtual reality: a required to confirm the benefits of tDCS and VR.’’ systematic review. Disability & Rehabilitation: Assistive Technology 2017; 12:551–559. (continued) 85 Table 1. (Continued) Review type Article Included studies Conclusions (from the articles) Systematic review (mental Jerdan SW, Grindle M, van Woerden HC, 82 studies ‘‘Our review demonstrated that VR is effective in provoking realistic health) Kamel Boulos MN. Head-Mounted Virtual reactions to feared stimuli, particularly for anxiety; moreover, it Reality and Mental Health: Critical proved that the immersive nature of VR is an ideal fit for the Review of Current Research. JMIR management of pain. However, the lack of studies surrounding Serious Games 2018; 6:e14. depression and stress highlight the literature gaps that still exist.’’ Systematic review and meta- Arroll B, Wallace HB, Mount V, et al. 16 studies ‘‘A range of therapies are effective for acrophobia in the short term but analysis (acrophobia) A systematic review and meta-analysis not in the long term. Many of the comparative studies showed of treatments for acrophobia. Med J Aust equivalence between therapies, but this finding may be due to a type II 2017; 206:263–267. statistical error. The quality of reporting was poor in most studies.’’ Narrative review (psychosis) Rus-Calafell M, Garety P, Sason E, et al. 50 studies ‘‘Virtual reality is a promising method to be used in the assessment of Virtual reality in the assessment and neurocognitive deficits and the study of relevant clinical symptoms. treatment of psychosis: a systematic Furthermore, preliminary findings suggest that it can be applied to the review of its utility, acceptability and delivery of cognitive rehabilitation, social skills training interventions effectiveness. Psychological Medicine and virtual reality-assisted therapies for psychosis.’’ 2017 Jul 24 [Epub ahead of print]. Systematic reviews (phobias) Botella C, Ferna´ndez-Alvarez J, Guille´nV,etal. 11 studies ‘‘VRET applications have become an effective alternative that can equal Recent progress in virtual reality exposure the results of traditional treatments for phobias from an efficacy point therapy for phobias: a systematic review. of view. However, they are also tools capable of enhancing the Current Psychiatry Reports 2017; 19:42. psychological treatment field.’’ Narrative review (anxiety Maples-Keller JL, Yasinski C, Manjin N, Not reported ‘‘VRE is consistent with models of extinction learning and provides disorders) et al. Virtual reality-enhanced extinction several advantages for use within exposure-based interventions. of phobias and post-traumatic stress. Broadly, extant research provides support for the effectiveness of Neurotherapeutics 2017; 14:554–563. VRE in reducing symptoms of specific phobias and PTSD, with outcomes generally superior to waitlist controls and comparable with traditional exposure therapy.’’ Meta-analysis (flight anxiety) Cardos x RAI, David OA, David, DO. Virtual 11 studies ‘‘Results pointed out significant overall efficiency of VRET in flight reality exposure therapy in flight anxiety: a anxiety at post-test and follow-up. Analysis highlighted the quantitative meta-analysis. Computers in superiority of VRET vs. control conditions at post-test and follow-up Human Behavior 2017; 72:371–380. and the superiority of VRET vs. classical evidence-based interventions at post-test and follow-up.’’ Narrative review (weight Castelnuovo G, Pietrabissa G, Manzoni GM, Not reported ‘‘Another current and future scenario where CBT could be improved in disorders) et al. Cognitive behavioral therapy to aid the management of obesity is represented by virtual reality (VR) weight loss in obese patients: current applications, such as the VR-enhanced CBT that is a sort of enhanced perspectives. Psychology Research & CBT of obesity with a VR module focused on unlocking the negative Behavior Management 2017; 10:165– memory of the body, changing its dysfunctional behavioral correlates, 173. and managing negative emotional states.’’ (continued) 86 Table 1. (Continued) Review type Article Included studies Conclusions (from the articles) Narrative review (weight Paul L, Van Der Heiden C, Hoek HW. Not reported ‘‘Although empirical evidence is still scare, results show that CBT is disorders) Cognitive behavioral therapy and effective in reducing disordered eating disorders and depression in predictors of weight loss in bariatric bariatric patients. New techniques for applying CBR by virtual reality surgery patients. Current Opinion in potentially make CBT more accessible and less costly.’’ Psychiatry 2017; 30:474–479. Systematic review (clinical Dascal J, Reid M, Ishak WW, et al. Virtual 11 studies ‘‘Data from 11 eligible studies provide insight into three current medical medicine) reality and medical inpatients: a applications of VR technology: pain distraction, eating disorders, and systematic review of randomized, cognitive/motor rehabilitation. Overall, a majority of studies from the controlled trials. Innovations in Clinical past decade found VR to be efficacious, easy to use, safe, and Neuroscience 2017; 14:14–21. contributing to high patient satisfaction.’’ Systematic review and meta- Chan E, Foster S, Sambell R, Leong P. 20 studies ‘‘VR may have a role in acutely painful procedures, however included analysis (procedural pain) Clinical efficacy of virtual reality for acute studies were clinically and statistically heterogenous. Further research procedural pain management: A is required to validate findings, establish cost efficacy and optimal systematic review and meta-analysis. clinical settings for usage. Future trials should report in accordance PLoS ONE 2018; 13:e0200987. with established guidelines.’’ Narrative review (clinical Li L, Yu F, Shi D, et al. Application of virtual Not reported ‘‘VR has shown to be effective in reduction of burn-induced pain and medicine) reality technology in clinical medicine. management of pain in other situations. Virtual reality exposure therapy American Journal of Translational and virtual reality cognitive behavior therapy have become effective Research 2017; 9:3867–3880. choices for patients with anxiety disorders and other phobias like fear of flying, claustrophobia, acrophobia or generalized social phobia’’ Narrative review (mental Maples-Keller JL, Bunnell BE, Kim SJ, et al. Not reported ‘‘VR has emerged as a viable tool to help in a number of different health) The use of virtual reality technology in the disorders, with the most strength of evidence for use in exposure treatment of anxiety and other psychiatric therapy for patients with anxiety disorders, cue exposure therapy for disorders. Harvard Review of Psychiatry patients with substance use disorders, and distraction for patients with 2017; 25:103–113. acute pain requiring painful procedures.’’ Systematic review (eating de Carvalho M, Dias T, Duchesne M, et al. 19 studies ‘‘Two different randomized, controlled trials have shown at one-year disorders) Virtual reality as a promising strategy in follow-up that VR had a higher efficacy than the gold standard in the the assessment and treatment of bulimia field, i.e., cognitive behavioral therapy (CBT). In conclusion, based nervosa and binge eating disorder: a on the current available data VR-based environments may be systematic review. Behavioral Sciences considered a promising strategy for the assessment and treatment of 2017; 7:43. BN and BED.’’ Systematic review (clinical Pourmand A, Davis S, Lee D, et al. 45 studies ‘‘These articles provide data, which strongly support the hypothesis that medicine) Emerging utility of virtual reality as a VR simulations can enhance pain management (by reducing patient multidisciplinary tool in clinical medicine. perception of pain and anxiety), can augment clinical training Games for Health Journal 2017; 6:263– curricula and physical rehabilitation protocols (through immersive 270. audiovisual environments), and can improve clinical assessment of cognitive function (through improved ecological validity).’’ (continued) 87 Table 1. (Continued) Review type Article Included studies Conclusions (from the articles) Systematic review (autism) Duffield TC, Parsons TD, Landry A, et al. 5 studies ‘‘Psychometric comparisons of these tools for the neuropsychological Virtual environments as an assessment assessment of pediatric individuals with ASD are lacking as the modality with pediatric ASD populations: current review demonstrated, although the use of VEs. This is a a brief report. Child Neuropsychology particularly important area of future research considering most 2017 Sep 13 [Epub ahead of print]. identification, and thus testing, treatment, and training occur in childhood for ASD.’’ Narrative review (pediatrics) Parsons TD, Riva G, Parsons S, et al. Virtual Not reported ‘‘VR can offer safe, repeatable, and diversifiable interventions that can reality in pediatric psychology. Pediatrics benefit assessments and learning in both typically developing children 2017; 140:S86–S91. and children with disabilities. Research has also pointed to VR’s capacity to reduce children’s experience of aversive stimuli and reduce anxiety levels.’’ Systematic review (autism) Mesa-Gresa P, Gil-Gomez H, Lozano-Quilis 31 studies There is moderate evidence that VR-based treatments can help children JA, Gil-Gomez JA. Effectiveness of with ASD. The lack of definitive findings does not allow us to state virtual reality for children and adolescents that VR-based treatments can improve the results of traditional with autism spectrum disorder: an treatments. Nevertheless, the promising results and the advantages of evidence-based systematic review. Sensors VR (especially considering ASD symptomatology) should encourage (Basel) 2018; 18:pii:E2486. the scientific community to develop new VR-based treatments. Systematic review (eating Clus D, Larsen ME, Lemey C, Berrouiguet 26 studies Overall, VR techniques enable the evaluation of pathological eating disorders) S. The use of virtual reality in patients behaviors and body image distortions. In addition to CBT, use of VR with eating disorders: systematic review. J techniques by patients with eating disorders decreased their negative Med Internet Res 2018; 20:e157. emotional responses to virtual food stimuli or exposure to their body shape. 88 RIVA ET AL. Three final articles explored the use of VR in the assess- achieve benefit from VR therapy. As noted by Price and ment and treatment of psychosis and in pain manage- Anderson, ‘‘The results support presence as a conduit that 6,25 ment. For psychosis, the available studies confirm the enabled phobic anxiety to be expressed during exposure to a efficacy of VR for the multimodal assessment of cognitive virtual environment. However, presence was not supported 7 66 functioning, including social cognition/competence and as contributing to treatment outcome. This suggests feeling hallucinations/paranoid ideations. For treatment, even if present during exposure may be necessary but not sufficient 68–70 92(p750) the available studies are very promising, there is a lack to achieve benefit from VR exposure.’’ of randomized controlled trials demonstrating whether VR is A new argument that is introduced and discussed in this more efficacious or efficient than other interventions. article is that VR shares with the brain the same basic 43,93 In relation to the use of VR for pain management, older mechanism: embodied simulations. 71,72 systematic reviews demonstrated the efficacy of VR 73–75 76 distraction for reducing experimental pain, as well as VR as Simulative Technology 77–79 80–82 the one generated by burn injury care, chronic pain, 83–85 6 94–96 and procedural pain. Hence, the first new one focused An increasingly popular hypothesis—predictive coding — its analysis on the integrated use of VR with brain stimula- suggests that the brain actively maintains an internal model tion (transcranial direct-current stimulation) in pain man- (simulation) of the body and the space around it, which pro- agement. Again, even if the level of clinical evidence is still vides predictions about the expected sensory input and tries to low, a study demonstrated the efficacy of this approach in minimize the amount of prediction errors (or ‘‘surprise’’). An reducing the severity of neuropathic pain and various neu- in-depth discussion of these concepts is not offered here be- ropathic pain subtypes. Finally, the second new one, sug- cause authoritative and thorough accounts have been provided 94–99 gests that VR may have a role in acutely painful procedures, elsewhere. However, herein, the focus is on the concept even if further research is required. of simulation introduced by this paradigm to understand better Overall, this meta-review indicated that VR is a powerful the links between the brain and VR. clinical tool for behavioral health, able to provide effective One of the main tenets of predictive coding is that to assessment and treatment options for a variety of mental regulate and control the body in the world effectively, the health disorders. Specifically, the 25 meta-analyses and brain creates an embodied simulation of the body in the systematic and narrative reviews indicated that VR compares world. There are two main characteristics of this simulation. favorably to existing treatments in anxiety disorders, eating First, different from other internal models used in cognitive and weight disorders, and pain management, with long-term science—such as Tolman’s cognitive maps or Johhson– effects that generalize to the real world. Moreover, they show Laird’s internal models—they are simulations of sensory the potential of VR as assessment tool with practical appli- motor experiences. In this view, they include visceral/auto- cations that range from social and cognitive deficits to ad- nomic (interoceptive), motor (proprioceptive), and sensory diction. Finally, they suggest a clinical potential in the (e.g., visual, auditory) information. Second, embodied sim- treatment of psychosis and in the pediatric field, even if there ulations reactivate multimodal neural networks, which have is no definitive evidence for or against the use of VR. produced the simulated/expected effect before. This approach is used not only for actions, but also for concepts and emotions. Specifically, a concept is a group of The Effectiveness of VR as a Clinical Tool distributed multimodal ‘‘patterns’’ of activity across differ- An open issue not directly addressed by most of these ent populations of neurons (motor, somatosensory, limbic, 100,101 articles is why VR is an effective clinical tool. In many and frontal areas) that support a goal achievement. So, articles, attention is focused on the high level of control and the simulation of a concept involves its reenactment in 1,2,9,10,87 customization allowed by this technology. VR al- modality-specific brain areas. Moreover, the brain uses lows the level of fit between the content of the exposure and emotion concepts to categorize sensations. As underlined by the feared stimuli to be optimized. Moreover, using it, the Barrett, ‘‘That is, the brain constructs meaning by correctly therapist has a total control—limited only by the specific anticipating (predicting and adjusting to) incoming sensa- features of the used software—on the contents of the expe- tions. Sensations are categorized so that they are (a) ac- rience. Finally, it offers a safer and more private context for tionable in a situated way and therefore (b) meaningful, the patient that facilitates his/her engagement. based on past experience. When past experiences of emotion Another important point suggested by different articles is (e.g., happiness) are used to categorize the predicted sensory the level of ‘‘presence’’ provided by the virtual experience. array and guide action, then one experiences or perceives 100(p9) In fact, VR provides a digital place to the individual where that emotion (happiness).’’ In this view, the feeling of he/she can be placed and live a synthetic but realistic expe- presence in a space can be considered as an evolutive tool rience. As noted by some colleagues, VR can be considered used to track the difference between the predicted sensations 89,90 an advanced imaginal system : an advanced form of and those that are incoming from the sensory world, both 93,102,103 imagery that is as effective as reality in inducing experiences externally and internally. and emotions. For example, as demonstrated by a recent VR works in a similar way: it uses computer technology to meta-analysis, presence and anxiety are associated with each create a simulated world that individuals can manipulate and other during VRE therapy for the treatment of anxiety. This explore as if they were in it. In other words, the VR expe- allows a level of self-reflectiveness that is both more pre- rience tries to predict the sensory consequences of your dictable and controllable than the one offered by reality, but movements, showing to you the same scene you will see in higher than the one provided by memory and imagination. the real world. Specifically, VR hardware tracks the motion However, presence alone is necessary but not sufficient to of the user, while VR software adjusts the images on the NEUROSCIENCE OF VIRTUAL REALITY 89 117,118 user’s display to reflect the changes produced by the motion of the brain by directly targeting the processes behind 119–121 in the virtual world. To achieve it, like the brain, the VR system real-world behaviors. maintains a model (simulation) of the body and the space But what is the real clinical potential of VR as an em- around it. This prediction is then used to provide the expected bodied technology? According to neuroscience, the body 105,106,122,123 sensory input using the VR hardware. Obviously, to be realistic, matrix serves to maintain the integrity of the the VR model tries to mimic the brain model as much as body at both the homeostatic and psychological levels by possible: the more the VR model is similar to the brain model, supervising the cognitive and physiological resources nec- 93,104 the more the individual feels present in the VR world. essary to protect the body and the space around it. Specifically, the body matrix plays a critical role in high-end cognitive processes such as motivation, emotion, social cognition, and VR as Embodied Technology 124–126 self-awareness, while exerting a top-down modulation As has just been seen, the brain creates multiple multi- over basic physiological mechanisms such as thermoregula- 100 127,128 123 sensory simulations to predict : (a) upcoming sensory tory control and the immune system. 114,116,129,130 events both inside and outside the body, and (b) the best In this view, different authors have recently action to deal with the impending sensory events. Moseley suggested that an altered functioning of the body matrix and/ et al. suggested that these simulations are integrated with or its related processes might be the cause of different neu- sensory data in the ‘‘body matrix,’’ a coarse supramodal rological and psychiatric conditions. If this is true, VR can multisensory representation of the body and the space around be the core of a new trans-disciplinary research field— 105–107 115,116 it. Specifically, the contents of the body matrix are embodied medicine —the main goal of which is the use defined by top-down predictive signals, integrating the of advanced technology for altering the body matrix, with the multisensory (motor and visceromotor) simulations of the goal of improving people’s health and well-being. causes of perceived sensory events. The different simu- As has been seen in the first section of this article, two 51,52 different VR embodiment techniques—body swapping lations are then ranked and included in the body matrix ac- 49,50 and reference frame shifting —are currentlyusedinthe cording to their relevance for the intentions of the self (selective attention). At the same time, the content and the treatment of eating and weight disorders. The first one, priority of the different simulations are corrected by bottom- body swapping, replaces the contents of the bodily self- up prediction errors that signal mismatches between pre- consciousness with synthetic ones (synthetic embodiment). dicted and actual contents of sensory events. This has been used in eating and weight disorders to im- At the end of this process, the body matrix defines where prove the experience of the body in both clinical (anorexia 131,132 133–135 the self is present, that is, in the body that our brain considers and morbid obesity) and non-clinical subjects. 110–112 136 as the most likely to be its one. As underlined by Apps Nevertheless, the potential of this approach is wider. For and Tsakiris, ‘‘The mental representation of the physical example, it may offer a non-pharmacological way to reduce properties of one’s self are, therefore, also probabilistic. That chronic pain. As has been seen in the first section of this is, one’s own body is the one that has the highest probability article, VR distraction is effectively used to reduce acute pain. of being ‘me,’ since other objects are probabilistically less Nevertheless, according to Tsay et al., ‘‘available findings likely to evoke the same sensory inputs. In short, the notion present compelling evidence for a novel multisensory and that there is a ‘self’ is the most parsimonious and accurate multimodal approach to therapies for chronic pain disor- 137(p249) 110(p88) explanation for sensory inputs.’’ ders’’ In this view, the use of VR embodiment may 138–140 If presence in the body is the outcome of different em- offer new treatment options for pain management. bodied simulations, and VR is a simulation technology, this Some studies have suggested the possibility of using VR body suggests the possibility of altering the experience of the body swapping to improve body perception disturbance in patients 113 141,142 by designing targeted virtual environments. In this view, with complex regional pain syndrome. VR can be defined as an ‘‘embodied technology’’ for its The second technique, reference frame shifting, structures possibility of modifying the embodiment experience of its the individual’s bodily self-consciousness through the focus 114–116 50,143 users. As noted by Riva et al., ‘‘using VR, subjects can and reorganization of its contents (mindful embodiment). experience the synthetic environment as if it was ‘their sur- It has been successfully used in different randomized trials in 54,55 patients with eating and weight disorders to update the rounding world’ (incarnation: the physical body is within a contents of their body memory. But again, its applications are virtual environment) or can experience their synthetic ava- tars as if they were ‘their own body’ (embodiment: the probably wider. For example, Osimo et al. integrated body 1(p9) physical body is replaced by the virtual one).’’ In other swapping (in the avatar of Sigmund Freud) and reference words, VR is able to fool the predictive coding mechanisms frame shifting to improve mood and happiness in a non-clinical used by the brain generating the feeling of presence in a sample. virtual body and in the digital space around it. A final emerging approach is the use of VR to augment the Up to now, VR has been used to simulate external reality, bodily experience through the awareness of internal (and that is, to make people feel ‘‘real’’ what is actually not really difficult to sense) bodily information, or the mapping of a there (i.e., the environment). However, the ability of VR to sensory channel to a different one—for example vision to 144,145 fool the predictive coding mechanisms that regulate the ex- touch or to hearing (augmented embodiment). For ex- perience of the body also allows it to make people feel ample, Suzuki et al. implemented an innovative ‘‘cardiac ‘‘real’’ what they are not. In other words, VR can offer new rubber hand illusion’’ that combined computer-generated ways for structuring, augmenting, and/or replacing the ex- augmented reality with feedback of interoceptive informa- 114–116 perience of the body for clinical goals. Moreover, it tion. Their results showed that the virtual-hand ownership is may offer new embodied ways for assessing the functioning enhanced by cardio-visual feedback in time with the actual 90 RIVA ET AL. heartbeat, supporting the use of this technique to improve The first outcome of an integrated VR platform able to emotion regulation. simulate both the external and the inner world is the possi- bility of structuring, augmenting, and/or replacing all the different experiential aspects of bodily self-consciousness, VR as Cognitive Technology with clinical applications in the treatment of psychiatric 151,152 153–155 disorders, such as depression or schizophrenia, VR is an embodied technology for its ability to modify the 137,156 and neurological disorders, such as chronic pain and experience of the body. However, the body is not simply an 157,158 93,147,148 neglect. object like any other; it has a special status. It is The final long-term outcome of this possibility may be the perceived in a multisensory way, from the outside (ex- embodied virtual training machine described by the science- teroception, the body perceived through the senses) as well fiction thriller The Matrix. In this movie, the heroes, Trinity as from within (inner body, including interoception, the and Neo, learned how to fight martial-arts battles and drive sense of the physiological condition of the body; proprio- motorcycles and helicopters by experiencing the bodily pro- ception, the sense of the position of the body/body segments; cesses and concepts related to the skill through an embodied and vestibular input, the sense of motion of the body) and simulation. from memory. This is true also for the simulative code used by the brain for creating concepts. As has been seen before, it integrates visceral/autonomic (interoceptive), motor (pro- Conclusions prioceptive), and sensory information. If concepts are em- bodied simulations, and VR is an embodied technology, it The first article discussing a VR application in the field of should be possible to facilitate cognitive modeling and behavioral health was published in 1995. Now, more than change by designing targeted virtual environments able to 20 years later, VR is a reality in this field. This is the result of modify concepts both from outside and from inside. a meta-review presented in this article assessing the meta- Nevertheless, there is a critical shortcoming that at the analyses and systematic and narrative reviews published in moment is limiting this possibility: VR simulates the exter- this field in the last 22 months. Twenty-five different articles nal world/body but not the internal one. In fact, actual VR have demonstrated the clinical potential of this technology in technology is very effective in reproducing the exteroceptive both the diagnosis and the treatment of mental health dis- (external) features of the body using vision and hearing, but orders. Specifically, they indicate that VR compares favor- less effective in reproducing the other senses (i.e., touch and ably to existing treatments in anxiety disorders, eating and smell ). It is partially effective in reproducing the propri- weight disorders, and pain management, with long-term ef- oceptive (motor) features of the body using haptic technol- fects that generalize to the real world. ogies, but it is not yet able to reproduce the interoceptive/ But why is VR so effective? Here, the following an- vestibular (internal) features of the body. swer is suggested: VR shares with the brain the same basic Recently, Riva et al. introduced the concept of ‘‘sono- mechanism—embodied simulations. ception,’’ a novel noninvasive technological paradigm based According to neuroscience, to regulate and control the on wearable acoustic and vibrotactile transducers, as a pos- body in the world effectively, the brain creates an embodied sible approach to structure, augment, and/or replace the simulation of the body in the world used to represent and contents of the inner body. This approach should be able to predict actions, concepts, and emotions. Specifically, it is modulate the inner body (interoception, proprioception, and used to predict: (a) upcoming sensory events both inside and vestibular input) through the stimulation of both mechano- outside the body, and (b) the best action to deal with the receptors in different parts of the body—the stomach, the impending sensory events. There are two main charac- heart, the muscles—and the otolith organs of the vestibular teristics of this simulation. First, it simulates sensory motor system (see Fig. 2). experiences, including visceral/autonomic (interoceptive), FIG. 2. The technology of ‘‘sonoception.’’ NEUROSCIENCE OF VIRTUAL REALITY 91 motor (proprioceptive), and sensory (e.g., visual, auditory) Acknowledgments information. Second, embodied simulations reactivate mul- This article was supported by the Italian MIUR research timodal neural networks which have produced the simulated/ project ‘‘Unlocking the memory of the body: Virtual Reality expected effect before. in Anorexia Nervosa’’ (201597WTTM) and by the Italian VR works in a similar way: the VR experience tries to Ministry of Health research project ‘‘High-end and low-end predict the sensory consequences of the individual’s move- virtual reality systems for the rehabilitation of frailty in the ments, providing to him/her the same scene he/she will see in elderly’’ (PE-2013-0235594). the real world. To achieve this, the VR system, like the brain, maintains a model (simulation) of the body and the space Author Disclosure Statement around it. If presence in the body is the outcome of different em- No competing financial interests exist. bodied simulations, and VR is a simulation technology, this suggests the possibility of altering the experience of the References body by designing targeted virtual environments. In this view, VR can be defined as an ‘‘embodied technology’’ for 1. Riva G, Ban˜os RM, Botella C, et al. Transforming expe- its possibility of modifying the embodiment experience of rience: the potential of augmented reality and virtual re- 114–116 its users. In other words, VR is able to fool the pre- ality for enhancing personal and clinical change. Frontiers dictive coding mechanisms used by the brain, generating the in Psychiatry 2016; 7:164. feeling of presence in a virtual body and in the digital space 2. Freeman D, Reeve S, Robinson A, et al. Virtual reality in around it. the assessment, understanding, and treatment of mental health disorders. 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