(C) PLOS One This story was originally published by PLOS One and is unaltered. . . . . . . . . . . Stroboscopic visual training: The potential for clinical application in neurological populations [1] ['Julia Das', 'Department Of Sport', 'Exercise', 'Rehabilitation', 'Northumbria University', 'Newcastle Upon Tyne', 'United Kingdom', 'Northumbria Healthcare Nhs Foundation Trust', 'North Tyneside General Hospital', 'North Shields'] Date: 2023-10 Abstract Visual problems are common in people who have neurological injury or disease, with deficits linked to postural control and gait impairment. Vision therapy could be a useful intervention for visual impairment in various neurological conditions such as stroke, head injury, or Parkinson’s disease. Stroboscopic visual training (SVT) has been shown to improve aspects of visuomotor and cognitive performance in healthy populations, but approaches vary with respect to testing protocols, populations, and outcomes. The purpose of this structured review was to examine the use of strobe glasses as a training intervention to inform the development of robust protocols for use in clinical practice. Within this review, any studies using strobe glasses as a training intervention with visual or motor performance–related outcomes was considered. PubMed, Scopus, and ProQuest databases were searched in January 2023. Two independent reviewers (JD and RM) screened articles that used strobe glasses as a training tool. A total of 33 full text articles were screened, and 15 met inclusion/exclusion criteria. Reported outcomes of SVT included improvements in short–term memory, attention, and visual response times, with emerging evidence for training effects translating to balance and physical performance. However, the lack of standardisation across studies for SVT protocols, variation in intervention settings, duration and outcomes, and the limited evidence within clinical populations demonstrates that further work is required to determine optimal strobe dosage and delivery. This review highlights the potential benefits, and existing research gaps regarding the use of SVT in clinical practice, with recommendations for clinicians considering adopting this technology as part of future studies in this emerging field. Author summary Visual problems are common in people who have neurological disease and can affect balance and walking. Vision therapy could be a useful intervention for visual problems in various neurological conditions such as stroke, head injury, or Parkinson’s disease. Stroboscopic visual training (SVT) is a type of visual training that involves the use of specialist glasses equipped with liquid crystal technology lenses. These lenses regulate visual information by producing an intermittent clear and opaque flicker effect without light or flash being used. Training with these glasses has been shown to improve aspects of visuomotor and cognitive (thinking) performance in healthy populations, but approaches to training vary. Here, we examine the use of strobe glasses as a training intervention with the aim to help develop protocols for use in clinical practice. We found evidence that SVT can improve visual skills, with the potential to enhance aspects of physical performance such as balance. However, we also found a lack of standardisation across studies for SVT protocols, and there was limited evidence for use of SVT within clinical populations. Our review not only highlights the potential benefits of using SVT in clinical practice but also emphasises where there are gaps in the current research. Based on our finding, we have made recommendations to help guide future research in this emerging field. Citation: Das J, Walker R, Barry G, Vitório R, Stuart S, Morris R (2023) Stroboscopic visual training: The potential for clinical application in neurological populations. PLOS Digit Health 2(8): e0000335. https://doi.org/10.1371/journal.pdig.0000335 Editor: Danilo Pani, University of Cagliari: Universita degli Studi Di Cagliari, ITALY Published: August 23, 2023 Copyright: © 2023 Das et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: This work forms part of a PhD study being undertaken by JD and has been funded by a Northumbria University PhD studentship in collaboration with Senaptec Inc. (Beaverton, Oregon, USA) (PIs: RM and SS). This work was also supported by a British Geriatric Society Movement Disorder Research Grant (PI: SS). SS (co-author) is supported, in part, by a Parkinson’s Foundation Post-doctoral Fellowship for Basic Scientists (PF-FBS-1898-18-21) and a Clinical Research Award (PF-CRA-2073). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing interests: The authors have declared that no competing interests exist. 1. Introduction The concept of visual training (also known as vision therapy) as a noninvasive intervention for visual impairment has been around for almost a century. Unlike lenses, prisms, filters, and occluders, which compensate for vision problems, or eye surgery that alters the anatomy of the eye or surrounding muscles, visual training uses sensory-motor-perceptual stimulation to enhance visual skills (such as eye movement control and eye coordination) as well as visual processing [1–4]. Vision training has also been used to enhance visual performance in healthy individuals [5,6], where oculomotor exercises or interruption of normal visual input have been associated with changes in motor function and improved physical performance [7–9]. Stroboscopic visual training (SVT) is a form of vision training aimed at improving aspects of visual and cognitive-perceptual performance [1]. SVT has taken a number of different forms since its first use over 20 years ago from the application of strobe lights in dark settings to digitally controlled eyewear [7,10]. Research has indicated that SVT may result in improved visual–motor actions such as driving performance [11], as well as reductions in symptoms that result from visual–motor conflict, such as motion sickness [12,13]. Interest in the use of SVT as a sports training tool began a decade ago following the findings of a study by Appelbaum and colleagues, which showed improved attention and motion detection following SVT in cohorts of university team–based athletes [9]. Subsequent studies using SVT in healthy individuals have shown promising results in improving visual acuity [14], visual attention [15], and visuomotor performance [16–18]. While research has yet to identify the exact mechanisms of action driving SVT, the approach is based on the basic premise that by intermittently disrupting vision, individuals reduce their reliance on visual feedback. This may lead to increased sensitisation and better visual skills when they return to normal visual conditions, as well as resulting in more effective utilisation of other sensory modalities, such as kinaesthetic awareness and auditory information [1]. Indeed, stroboscopic visual perturbation has been shown to be a valid assessment method for sensory dependence, promoting sensory reweighting and improving balance control [19–21]. Visual problems are common in people who have neurological injury or disease, such as stroke and traumatic brain injury or Parkinson’s disease [22], with deficits linked to postural control and locomotion impairment [23]. Vision therapy, particularly SVT, could be a useful intervention for visual impairment in various neurological conditions. Indeed, vision therapy has been used for treatment of binocular and accommodative dysfunctions, strabismus, amblyopia, oculomotor dysfunctions in acquired brain injury and mild traumatic brain injury (concussion) and visual information processing disorders [4,24]. However, it is unclear how to implement visual training to intervene in visual impairment within clinical populations. For example, within mild traumatic brain injury, visual training duration varies depending on the diagnosis and the patient, typically ranging from several months to longer periods of time [4]. Clinicians or researchers who wish to use or investigate visual training methods are left without any clear guidance on how to implement such methods. Therefore, a structured review with recommendations on specific visual training methods is warranted. A previous review of the impact of SVT showed initial efficacy of SVT in improving visual performance in healthy individuals [1], but little information about the SVT methodology was reviewed. In order to develop robust interventional protocols, it is important to understand how SVT has been effectively deployed, such as what cohorts it has been used in (healthy, clinical, etc.), duration of training, strobe frequency, type of SVT device, exercises coupled with SVT, etc. The purpose of this review is to identify all previously peer-reviewed research that has investigated the use of strobe glasses as a training intervention with a visual or motor performance related outcome in healthy and clinical populations. The review aimed to (1) examine the methods involved in SVT; (2) present the commonly reported outcomes and explore how SVT influences these; and (3) provide clinical and future research recommendations. 4. Discussion This structured review examined 15 studies that reported the use of SVT in healthy and clinical populations with the aim to summarise the impact of SVT on visual and/or motor performance. All research studies identified in this review were conducted since 2011, making SVT a relatively new area of study. A major strength of SVT compared to other paper or computer-based visual training tools is that it allows for training to take place in real-world environments. However, its application in a variety of different training contexts has led to significant variability between and within interventions. In this review, we sought to determine what research has been conducted in neurological cohorts, as previous evidence suggests that training visual skills may benefit symptoms in this population. 4.1 Participants With the vast majority of studies including only healthy young participants, the generalisability of findings from this review to older or clinical populations is limited. Recruitment was predominantly through university cohorts or sports teams (with the exception of the study by Shalmoni and Kalron, which was based in an MS specialist medical centre) [42] with sample sizes varying across the studies (i.e., n = 6 to 157). A history of epilepsy/seizures, migraines (or more broadly “neurological disorder”) were commonly cited exclusion criteria, although 7 of the reviewed articles made no reference to exclusion criteria, which is perhaps reflective of the fact that the earlier studies were from nonclinical sporting disciplines involving young and healthy individuals. Reporting biases in relation to participant demographics also limit cross-study comparisons. To understand the potential application and efficacy of SVT in clinical populations, further studies conducted in different clinical cohorts and older populations are required. Some authors selected to use nonstrobing eyewear for their control group participants, while others used lens-free glasses or normal vision, but in the absence of a true placebo or blinding option, it is not possible to determine whether motivational effects exist. Indeed, the one study that collected qualitative data regarding SVT revealed that participants believed that their visual, perceptual, and sporting performance all improved as a result of the SVT, indicating the potential of participant bias in favour of SVT [44]. Research is needed to determine whether SVT is perceived as positively by participants from clinical populations in order to identify the most appropriate control methods for future study protocols. 4.2 Protocols 4.2.1 Stroboscopic devices. There was a lack of standardisation of stroboscopic instrumentation employed across the studies. The 5 devices used in the studies all had different manufacturer operating levels, so there was no consistent method of reporting the frequency of the strobe effect or “blink rate.” For example, the Senaptec Strobes operate at a level between 1 and 8, with level 1 representing the fastest/easiest setting at a frequency of 6 Hz (calculated according to the number of transparent-opaque cycles per second) and level 8 representing the slowest/hardest setting at a frequency of 1 Hz [52]. In comparison, the Visionup strobes are adjustable by 10 levels whereby level 1 equates to 1 Hz (based on the frequency of the opaque phase), and level 10 equates to 150 Hz [53]. Even for studies utilising the same strobe device, reporting of the strobe setting varied. For example, Kim and colleagues refer to the operating levels of the Senaptec Strobes (i.e., levels 1 to 8) [50], whereas Hülsdünker and colleagues record frequency settings (i.e., 15 Hz to 8 Hz) [40]. The illuminance value (i.e., degree of light transmission provided through the lenses; measured in lux) was only measured by Bennett and colleagues [45], in relation to the Nike Vapor Strobes and the PLATO goggles, but was not reported in any of the other papers in this review… The Visionup and MJ Strobe glasses have the option to adjust the “duty ratio” (or level of brightness of the lenses), to create darker conditions and, therefore, a more challenging visual environment. Direct comparisons between studies using different brands of eyewear are therefore confounded by the variation in functionality of the different devices, description of lens characteristics, luminance values, and methods of reporting. This was highlighted by Wilkins and Gray who suggested that their use of PLATO goggles (as opposed to the Nike Vapor Strobes) may have contributed to the discrepancy in their findings with previous research [48]. It is evident from this review that more clarity around strobe frequencies and setting levels is required (both from manufacturers of the devices and researchers themselves) to provide clear understanding and accurate interpretation for future clinical application. 4.2.2 Strobe settings. There was a lack of standardisation with regard to (1) the frequency of strobe settings and (2) the use of fixed versus variable strobe frequency settings. Smith and Mitroff examined the effect of SVT delivered at a fixed frequency of 4 Hz (Nike Vapor Strobes: level 3, 100 ms clear: 150 ms opaque) and found that participants in the intervention group had significantly better anticipation immediately after a single session of SVT [49]. Subsequent studies have since used these findings to justify their selection of strobe rate settings [18,46]. The most recent study by Symeonido and Ferris applied a much lower fixed frequency visual perturbation to participants as they walked on a treadmill-mounted balance beam for 30 minutes [51]. Balance performance, in number of step-offs of the beam, improved by 78% for the SVT group on the same day of the training. While the earlier studies in this review support a link between visual stimuli and motor learning, Symeonidou and Ferris attributed their much larger training effect to their use of lower frequency strobe settings [51]. For the 8 studies that adopted a variable frequency approach, training protocols generally started on the easiest (fastest) strobe setting before the strobe rate was reduced in response to the correct execution of training drills or to increase task difficulty over time. The exact duration with which participants trained at each strobe level was poorly documented in the majority of studies, making it difficult to extrapolate the findings (Table 2). The study by Wilkins and Gray was the only one to directly compare training with a fixed strobe rate and a variable strobe rate [48]. Motion in depth sensitivity significantly improved posttraining, but no significant differences were found between the fixed and the variable rate groups. Further work is therefore required not only to determine whether there is an optimal frequency of strobe setting required for both visual and motor learning to occur but also to establish whether the effects of SVT are greater (or indeed reduced) if participants remain on a fixed strobe frequency [1]. 4.2.3 Frequency and duration of interventions. This review demonstrates that there was significant variability regarding the frequency, duration, and number of SVT interventions carried out within the studies (a finding that has been reported across other forms of vision therapy) [54,55]. Interventions ranged from a single session of SVT to multiple sessions over 10 weeks (Table 2). Further complicating interpretation in this review is the lack of clarity provided about the intervention protocols in some papers. For example, Zavlin and colleagues found that SVT had a significant positive effect on the performance of surgical suturing tasks by medical students after 5 sessions of training, but no detail is provided on how long each training session lasted [47]. This makes it difficult to make comparisons between studies because the exact duration of SVT is not known. In this review, immediate visual improvements were reported after a single session lasting as little as 5 to 7 minutes in some studies [18,49]. This is a significantly lower duration than the 4- to 8-week length of visual training that has been shown to be effective in previous nonstroboscopic research involving athletes [5,56,57]. In contrast with the findings of Smith and Mitroff and Ellison and colleagues [18,49], however, 5 minutes of SVT was not sufficient to improve time to collision judgements of approaching objects in Braly and colleagues’ study [46]. The differing protocols in this review mean that currently no conclusions can be drawn regarding the optimal frequency and duration of SVT that is necessary for a successful outcome in any population. 4.2.4 Training interventions. The lack of standardised training interventions across the studies in this review reflects the fact that SVT allows for training to take place in a variety of “real-world” contexts in addition to more controlled laboratory-based settings. Furthermore, the reporting of the precise details of the training interventions were vague in a number of the studies due to the logistical constraints imposed by using athletic populations, which limits interpretation of their findings [9,15,43]. While some studies using athletic populations did provide a detailed description of the SVT intervention (for example, Hülsdünker and colleagues described 2 badminton-specific protocols), making inferences on these studies remains challenging due to the sport-specific nature of the interventions provided. Nike developed a series of videos showing exercises for SVT in 2010s. These mostly comprised variations on simple ball catching tasks (such as the wall-ball catch, the front catch, the turn and catch, and the power ball drop). These exercises formed the basis of interventions for 3 of the reviewed studies [42,44,48]. Kim and colleagues also used throwing/catching exercises alongside static and dynamic balance tasks as part of their SVT intervention [50]. Unlike the study by Shalmoni and Kalron who implemented ball drills intended for athletes in an intervention for people with MS [42], to our knowledge, Kim and colleagues’ study is the first to demonstrate how SVT might be used to increase the challenge of standardised exercises, thereby further improving sensorimotor control [50]. Their intervention is supported by the findings of Symeonido and colleagues, who also used SVT to enhance the effects of balance training [51]. Further work is required to determine how best to proceed with the introduction of stroboscopic training protocols in clinical populations. Evidence from this review suggests that one approach would be to use strobe glasses as an adjunct to existing rehabilitation practices whereby interventions are composed of standardised exercise programmes performed with and without stroboscopic glasses. 4.2.5 Posttraining test points. Posttests were carried out within 24 hours in all the studies, providing evidence of the immediate effects of SVT on a range of outcomes. Retention-test data, which are arguably of more interest in relation to the clinical application of SVT, were collected in only 4 of the studies, which limits our understanding of the long-term effectiveness of SVT in any population. Future studies are required to determine whether the effects of SVT last beyond 4 to 6 weeks and, indeed, whether the duration and frequency of SVT affects retention. 4.3 Outcomes Various outcomes were used to assess the efficacy of SVT across the studies, including measures of visual skills (e.g., reaction time, visual memory, processing speed) and motor performance (e.g., balance, sport-specific skills). The paper by Shalmoni and Kalron was one of only 4 studies to include measures of both visual and motor function [42]. They demonstrated immediate improvements in information processing speed in people with multiple sclerosis after a single SVT session lasting between 40 and 50 minutes [42]. Their primary findings were largely consistent with the other studies in healthy adults, which have reported visual improvements following SVT [9,15,16,48,49]. In contrast with the improvements seen in information processing speed, however, no differences were observed in gait and balance outcomes after the single SVT session [42]. However, Symeonido and Ferris found that a single 30-minute session of SVT while walking on a treadmill-mounted balance beam was sufficient to enhance motor performance in young healthy adults [51]. These findings provide strong support for the beneficial training effects of using SVT for task-specific dynamic balance training at least in younger adults and highlight the need for future clinical studies to consider their choice of outcomes in relation to the SVT tasks being provided. 4.4 User experience None of the studies in this review included any participant feedback with regard to the usability of the glasses. A study by Wilkins and colleagues was novel in its inclusion of qualitative data collection methods, but the small sample size (n = 3) and lack of detail pertaining to the methodological and analytical processes limits the credibility and transferability of their findings [58]. The lack of work evaluating the acceptability of SVT is perhaps surprising given that wearable comfort is recognised as a key factor affecting end user adoption [59]. Exploring the wearability of the strobe glasses and understanding the needs of the user are particularly important in clinical populations as these are factors likely to influence engagement with SVT within rehabilitation [60–62]. 4.5 Safety and adverse effects No adverse events were reported in any of the studies in this review, which is somewhat surprising given that prior research suggests that there may be the potential for individuals to experience irritation or headaches as a result of working under stroboscopic lighting conditions [63,64]. In their methodology, Kim and colleagues did state that “the training session was stopped if dizziness or any adverse event was observed,” but no further reference was made to this in the paper so it is not known how many (if any) participants experienced adverse events as a result of the SVT [50]. Hülsdünker and colleagues reported that “only training drills without head rotation were used” and later recommended that “exercises involving head rotation movements should be avoided because the vestibulo–ocular information mismatch may induce discomfort and increase the risk of injuries” [40]. It is unclear how the authors came to this conclusion, as there was no reporting on adverse events in this paper. Wilkins and Appelbaum and Carrolla and colleagues both acknowledge the potential for “physical hazards” as a result of training in conditions of interrupted vision, but this is again an area that has not been explored in any of the SVT studies to date [1,65]. The potential for experiencing adverse effects such as trips or falls as a result of disrupted vision, or symptoms of discomfort due to the strobe effect, may be even greater in older individuals or those living with long-term conditions because of their dependence on visual input to compensate for sensory or motor losses [66,67]. Future studies therefore need to explore the feasibility of SVT in clinical populations to determine if individuals are able to safely tolerate the strobe effect without experiencing discomfort or unsteadiness. 5. Clinical implications The variation in how SVT research has been carried out means that there is still no consensus with regard to the optimal length of training with strobes (per session and total length) and the most effective strobe frequency at which to train. Furthermore, with all but one study [42] being conducted in healthy cohorts, there is insufficient evidence to inform decisions about the use of SVT in areas of clinical practice involving older adults or individuals with long-term conditions such as Parkinson’s disease, stroke, and MS. Despite these limitations, the findings of this review suggest that SVT may have a role to play in healthcare. SVT can enhance visual skills with some evidence for training effects translating to balance and physical performance in both healthy and clinical populations [42,51]. Although it is still not known whether SVT can have a functional impact, multiple sessions of training (as opposed to a single session) are likely to be required to demonstrate any potential effect on outcomes such as balance and gait in clinical populations [42]. The strobe glasses themselves are lightweight and portable and therefore have the potential to be used, with supervision, in a variety of different settings, which has significant implications for clinical practice as rehabilitation becomes more community based [68]. However, “buy in” to the strobe glasses by health professionals is likely to be affected by the current lack of evidence to support their effectiveness in clinical populations as well as the need to provide one-to-one supervision to individuals while using them [69]. “Buy in” from patient populations may be limited by the fact that the strobe effect could be disorientating for people with existing visual or balance deficits and because of the extra challenge they add to performance. Conclusions and recommendations for future research The purpose of this paper has been to review the scientific literature that has tested the impact of SVT on visual and motor performance in different populations. The functional implications of SVT beyond sport-specific skill performance remain unclear, and the lack of standardised approach to studying the effects of SVT limits understanding and application to clinical practice. Despite these limitations, our review informs this emerging field. Future trials involving SVT should be adequately powered to ensure that statistically significant effects can be detected and preregistered prior to data collection to provide transparency about the research methods used and improve credibility of findings. Fig 3 outlines our recommendations for future research in this field. PPT PowerPoint slide PNG larger image TIFF original image Download: Fig 3. Recommendations for future research in clinical populations. https://doi.org/10.1371/journal.pdig.0000335.g003 [END] --- [1] Url: https://journals.plos.org/digitalhealth/article?id=10.1371/journal.pdig.0000335 Published and (C) by PLOS One Content appears here under this condition or license: Creative Commons - Attribution BY 4.0. via Magical.Fish Gopher News Feeds: gopher://magical.fish/1/feeds/news/plosone/