The development of a novel pitch-side concussion balance assessment: a comparison between a virtual reality based balance tool and the modified balance error scoring system

Background: Balance deficits are a key measurable marker of concussion injuries. An objective pitch-side concussion balance assessment needs to replace current subjective, insensitive, unportable tests. A novel pitch-side dual-task VR test has been developed to evoke perturbations, and measure COP path length changes, via a WBB. Aims: To establish whether a VR WBB system is effectively able to assess postural stability, by evoking perturbations, and to measure subsequent changes in COP path length. To establish whether mBESS error scores, or objective mBESS COP path lengths correlate with changes in COP path length post-perturbation. Methods: 14 female University of Birmingham hockey players aged 18-21 performed both the mBESS and the VR WBB assessment at the pitch-side. Results: The mean COP path length post-perturbation was significantly greater than pre- perturbation, as the tilt induced a compensatory sway response. SL error scores significantly correlated with SL COP path length, and COP path length percentage change from pre to post-perturbation. Conclusion: The dual-task VR WBB system effectively assesses postural stability by measuring subsequent changes in COP path length. The objective nature and plethora of information provided by the VR WBB system, heightens its appeal over the mBESS, as an assessment of postural stability

Phase Dynamics in Human Visuomotor Control - Health & Disease

In this thesis, comprised of four publications, I investigated phase dynamics of visuomotor control in humans during upright stance in response to an oscillatory visual drive. For this purpose, I applied different versions of a ‘moving room’ paradigm in virtual reality while stimulating human participants with anterior-posterior motion of their visual surround and analyzed their bodily responses. Human balance control constitutes a complex interplay of interdependent processes. The main sensory contributors include vision, vestibular input, and proprioception, with a dominant role attributed to vision. The purpose of the balance control system is to keep the body’s center of mass (COM) within a certain spatial range around the current base of support. Ever-changing environmental circumstances along with sensory noise cause the body to permanently sway around its point of equilibrium. Considering this sway, the human body can be modelled as a (multi-link) inverted pendulum. To maintain balance while being exposed to perturbations of the visual environment, humans adjust their sway to counteract the perceived motion of their bodies. Neurodegenerative diseases like Parkinson’s impair balance control and thus are likely to affect these mechanisms. Hence, investigation of bodily responses to a visual drive gives insight into visuomotor control in health and disease. In my first study, I introduced inter-trial phase coherence (ITPC) as a novel method to investigate postural responses to periodical visual stimulation. I found that human participants phase-locked the motion of their center of pressure (COP) to a 3-D dot cloud which oscillated in the anterior-posterior direction. This effect was equally strong for a low frequency of visual stimulation at 0.2 Hz and a high frequency of 1.5 Hz, the latter exceeding the previously assumed frequency range associated with coherent postural sway responses to periodical oscillations of the visual environment (moving room). Moreover, I was able to show that ITPC reliably captured responses in almost all participants, thereby addressing the common problem of inter-subject variability in body sway research. Based on the results of my first study, I concluded phase locking to be an essential feature in human postural control. For the second study, I introduced a mobile and cost-effective setup to apply a visual paradigm consisting of a virtual tunnel which stretched in the anterior-posterior direction and oscillated back and forth at three distinct frequencies (0.2 Hz, 0.8 Hz, and 1.2 Hz). Because tracking of the COP alone neglects crucial information about how COM shifts are arranged across the body, I included additional full-body motion tracking here to evaluate sway of individual body segments. Using a modified measure of phase locking, the phase locking value (PLV), allowed me to find participants phase-locking not only their COP, but also additional segments of their body to the visual drive. While their COP exhibited a strong phase locking to all frequencies of visual stimulation, distribution of phase locking across the body underwent a shift as the frequency of the visual stimulation increased. For the lowest frequency of 0.2 Hz, participants phase-locked almost their entire body to the stimulus. At higher frequencies, this phase locking shifted towards the lower torso and hip, with subjects almost exclusively phase-locking their hip to the visual drive at the highest frequency of 1.2 Hz. Having introduced a novel and reliable measurement along with a mobile setup, these results allowed me to empirically confirm shifts in postural strategies previously proposed in the literature. In the third study, a collaboration with the neurology department of the Universitätsklinikum Gießen und Marburg (UKGM), I used the same setup and paradigm as in the previous study and additionally derived the trajectory of the COM from a weighted combination of certain body segments. The aim was to investigate phase locking of body sway in a group of patients suffering from Parkinson’s disease (PD) to find potential means for an early diagnosis of the illness. For this purpose, I recruited a group of PD patients, an age-matched control group, and a group of young healthy adults. Even though the sway amplitude of PD patients was significantly larger than that of both other groups, they phase-locked their COP and COM in a similar manner as the control groups. However, considering individual body segments, the shift in PLV distribution differed between groups. While young healthy adults, analogous to the participants in the second study, exhibited a shift towards exclusive phase locking of their hips as frequency of the stimulation increased, both PD patients and age-matched controls maintained a rather homogeneous phase locking across their body. This suggested increased body stiffness, although being an effect of age rather than disease. Overall, I concluded that patients of early-to-mid stage PD exhibit impaired motor control, reflected in their increased sway amplitude, but intact visuomotor processing, indicated by their ability to phase-lock the motion of their body to a visual drive. The fourth study, to which I contributed as second author, used experimental data collected from an additional visual condition in the course of the third study. This condition consisted of unpredictable back and forward motion of the simulated tunnel. Here, we investigated the velocity profiles of the COP and COM in response to the unpredictable visual motion and a baseline condition at which the tunnel remained static. We found PD patients to exhibit larger velocities of their COP and COM under both conditions when compared to the control groups. When examining the net increase that unpredictable motion had on the velocity of both parameters, we found a significantly higher increase in COP velocity for both PD patients and age-matched controls, but no increase in COM velocity in any of the groups. These results suggested that all groups successfully maintained their balance under unpredictable visual perturbations, but that PD patients and older adults required more effort to accomplish this task, as reflected by the increased velocity of their COP. Again, these results indicated an effect of age rather than disease on the observed postural responses. In summary, using innovative phase-locking techniques and simultaneously tracking multiple body sway parameters, I was able to provide novel insight into visuomotor control in humans. First, I overcame previous issues of inconsistent sway parameters in groups of participants; Second, I found phase-locking to be an essential feature of visuomotor processing, which also allowed me to empirically confirm previously established theories of postural control; Third, through studies in collaboration with the neurology department of the UKGM, I was able to uncover new aspects of visuomotor processing in Parkinson’s, contributing to a better understanding of the sensorimotor aspects of the disease

Vestibular rehabilitation for peripheral vestibular hypofunction: An updated clinical practice guideline from the Academy of Neurologic Physical Therapy of the American Physical Therapy Association

BACKGROUND: Uncompensated vestibular hypofunction can result in symptoms of dizziness, imbalance, and/or oscillopsia, gaze and gait instability, and impaired navigation and spatial orientation; thus, may negatively impact an individual\u27s quality of life, ability to perform activities of daily living, drive, and work. It is estimated that one-third of adults in the United States have vestibular dysfunction and the incidence increases with age. There is strong evidence supporting vestibular physical therapy for reducing symptoms, improving gaze and postural stability, and improving function in individuals with vestibular hypofunction. The purpose of this revised clinical practice guideline is to improve quality of care and outcomes for individuals with acute, subacute, and chronic unilateral and bilateral vestibular hypofunction by providing evidence-based recommendations regarding appropriate exercises. METHODS: These guidelines are a revision of the 2016 guidelines and involved a systematic review of the literature published since 2015 through June 2020 across 6 databases. Article types included meta-analyses, systematic reviews, randomized controlled trials, cohort studies, case-control series, and case series for human subjects, published in English. Sixty-seven articles were identified as relevant to this clinical practice guideline and critically appraised for level of evidence. RESULTS: Based on strong evidence, clinicians should offer vestibular rehabilitation to adults with unilateral and bilateral vestibular hypofunction who present with impairments, activity limitations, and participation restrictions related to the vestibular deficit. Based on strong evidence and a preponderance of harm over benefit, clinicians should not include voluntary saccadic or smooth-pursuit eye movements in isolation (ie, without head movement) to promote gaze stability. Based on moderate to strong evidence, clinicians may offer specific exercise techniques to target identified activity limitations and participation restrictions, including virtual reality or augmented sensory feedback. Based on strong evidence and in consideration of patient preference, clinicians should offer supervised vestibular rehabilitation. Based on moderate to weak evidence, clinicians may prescribe weekly clinic visits plus a home exercise program of gaze stabilization exercises consisting of a minimum of: (1) 3 times per day for a total of at least 12 minutes daily for individuals with acute/subacute unilateral vestibular hypofunction; (2) 3 to 5 times per day for a total of at least 20 minutes daily for 4 to 6 weeks for individuals with chronic unilateral vestibular hypofunction; (3) 3 to 5 times per day for a total of 20 to 40 minutes daily for approximately 5 to 7 weeks for individuals with bilateral vestibular hypofunction. Based on moderate evidence, clinicians may prescribe static and dynamic balance exercises for a minimum of 20 minutes daily for at least 4 to 6 weeks for individuals with chronic unilateral vestibular hypofunction and, based on expert opinion, for a minimum of 6 to 9 weeks for individuals with bilateral vestibular hypofunction. Based on moderate evidence, clinicians may use achievement of primary goals, resolution of symptoms, normalized balance and vestibular function, or plateau in progress as reasons for stopping therapy. Based on moderate to strong evidence, clinicians may evaluate factors, including time from onset of symptoms, comorbidities, cognitive function, and use of medication that could modify rehabilitation outcomes. DISCUSSION: Recent evidence supports the original recommendations from the 2016 guidelines. There is strong evidence that vestibular physical therapy provides a clear and substantial benefit to individuals with unilateral and bilateral vestibular hypofunction. LIMITATIONS: The focus of the guideline was on peripheral vestibular hypofunction; thus, the recommendations of the guideline may not apply to individuals with central vestibular disorders. One criterion for study inclusion was that vestibular hypofunction was determined based on objective vestibular function tests. This guideline may not apply to individuals who report symptoms of dizziness, imbalance, and/or oscillopsia without a diagnosis of vestibular hypofunction. DISCLAIMER: These recommendations are intended as a guide to optimize rehabilitation outcomes for individuals undergoing vestibular physical therapy. The contents of this guideline were developed with support from the American Physical Therapy Association and the Academy of Neurologic Physical Therapy using a rigorous review process. The authors declared no conflict of interest and maintained editorial independence.Video Abstract available for more insights from the authors (see the Video, Supplemental Digital Content 1, available at: http://links.lww.com/JNPT/A369)

Training functional mobility using a dynamic virtual reality obstacle course

Falling poses a significant risk of injury for older adults, thus decreasing quality of life. Major risk factors for falling include decrements in gait and balance, and adverse patient-reported health and well-being. Virtual Reality (VR) can be a cost-effective, resource-efficient, and highly engaging training tool, and previous research has utilized VR to reduce fall-risk factors in a variety of populations with aging and pathology. However, there are barriers to implementing VR as a training tool to improve functional mobility in older adults that include the manner in which healthy older adults perform in VR relative to younger adults, the effect of extended duration training, and the relation of fall-risk clinical metrics to performance in VR. The purpose of this dissertation is threefold: (1) to compare performance between older and younger adults in VR and in real-world gait and balance tests as a result of a single bout of VR training; (2) to compare performance in VR and gait and balance within younger adults as a result of extended training duration; and (3) to evaluate clinical tests as prerequisite measures for performance within the VR environment. Thirty-five healthy adults participated in this study and were placed into either the older adult training group (n=8; 67.0±4.4yrs), younger training (n=13; 22.1±2.5yrs), or younger control (n=13; 21.7±1.0yrs). All participants completed an online patient-reported survey of balance confidence and health and well-being, as well as a pre-test of clinical assessments and walking and balance tests. The training groups then completed 15 trials of a VR obstacle course, while the controls walked overground for 15 minutes. The VR obstacle course included a series of gait and dynamic balance tasks, such as stepping on irregularly placed virtual stepping stones and walking a virtual balance beam. All participants repeated the walking and balance tests at post-test. The younger training group also completed 3 weeks of training in the same VR obstacle course and a second post-test. Analyses of variance were completed to determine the extent to which participants improved within VR and the walking and balance tests both as a result of a single bout of training, and for the younger adults – three weeks of extended training. Multiple regressions were run to determine the extent to which patient-reports and clinical assessments may predict performance within VR. The results reported in Manuscript I show that although younger adults completed the VR course quicker, their learning rate was not different from older adults; and as a result of extended training, younger adults continued to improve their time to complete the course. For gait and balance tests, age related differences were observed. Both groups showed better performance on some post-tests, indicating that VR training may have had a positive effect on neuromotor control. The results reported in Manuscript II suggest the RAND-1 pain subscale and simple reaction time (SRT) may predict time to complete the VR course, and SRT and BBS Q14 may additionally predict obstacle contact. These data suggest a VR obstacle course may be effective in improving gait and balance in both younger and older adults. It is recommended that future work enroll older adults in the extended training portion of the study and to increase the VR obstacle course difficulty when benchmarks are met

The development of a novel balance platform for concussion assessment

Balance dysfunction has been recognised as a key marker of concussion for many years. Whilst this measure has been exploited within concussion assessments, current balance procedures are expensive, and laboratory-constrained or inexpensive, but subjective. The present study focused on developing an objective, inexpensive tool to assess balance utilizing Virtual Reality (VR) to induce a perturbation and a Wii Balance Board (WBB) to measure the response. The first part of this thesis focused on constructing a VR-WBB system to determine its validity when assessing balance. Notably, piloting confined the VR component of the system was effective in inducing perturbation and further, the WBB could adequately quantify the response by obtaining sensitive centre of pressure (COP) data. The second prut of this thesis focused on refining this prototype, assessing how an individual's balance would be affected by speed-manipulated and axismanipulated perturbations. Current studies highlighted that manipulating axes and speed of perturbation significantly affected the COP response, which has profound implications when developing the optimal VR-WBB tool. Overall this thesis confirms that the VR- WBB prototype is an effective system to induce a perturbation and obtain quantifiable balance responses. With further parameter refinement, this tool could be revolutionary for pitchside assessment of concussion

Effects of Sensorimotor Perturbations on Balance Performance and Electrocortical Dynamics

Humans must frequently adapt their posture to prevent loss of balance. Such balance control requires complex, precisely-timed coordination among sensory input, neural processing, and motor output. Despite its importance, our current understanding of cortical involvement during balance control remains limited by traditional neuroimaging methods, which are stationary and have poor time resolution. High-density electroencephalography (EEG), combined with independent component analysis, has become a promising tool for recording cortical dynamics during balance perturbations due to its portability and high temporal resolution. Additionally, recent improvements in immersive virtual reality headsets may provide new rehabilitative paradigms, but the effects of virtual reality on balance and cortical function remain poorly understood. In my first study, I recorded high-density EEG from healthy, young adult subjects as they walked along a beam with and without virtual reality high heights exposure. While virtual high heights did induce stress, the use of virtual reality during the task increased performance errors and EEG measures of cognitive loading compared to real-world viewing without a headset. In my second study, I collected high-density EEG from healthy young adults as they walked along a treadmill-mounted balance beam to determine the effect of a transient visual perturbation on training in virtual reality. Subjects in the perturbations group improved comparably to those that trained without virtual reality, indicating that the perturbation helped subjects overcome the negative effects of virtual reality on motor learning. The perturbation primarily elicited a cognitive change. In my third study, healthy, young adult EEG was recorded during physical pull and visual rotation perturbations to tandem walking and tandem standing. I found similar electrocortical patterns for both perturbation types, but different cortical areas were involved for each. In my fourth study, I used a phantom head to validate EEG connectivity methods based on Granger causality in a real-world environment. In general, connectivity measures could determine the underlying connections, but many were susceptible to high-frequency false positives. Using data from my third study, my fifth study analyzed corticomuscular connectivity patterns following sensorimotor balance perturbations. I found strong occipito-parietal connections regardless of perturbation type, along with evidence of direct muscular control from the supplementary motor area during the standing perturbation response. Taken together, the work presented in this dissertation greatly expands upon the current knowledge of cortical processing during sensorimotor balance perturbations and the effect of such perturbations on short-term motor learning, providing multiple avenues for future exploration.PHDBiomedical EngineeringUniversity of Michigan, Horace H. Rackham School of Graduate Studieshttps://deepblue.lib.umich.edu/bitstream/2027.42/147615/1/stepeter_1.pd

I-BaR: Integrated Balance Rehabilitation Framework

Neurological diseases are observed in approximately one billion people worldwide. A further increase is foreseen at the global level as a result of population growth and aging. Individuals with neurological disorders often experience cognitive, motor, sensory, and lower extremity dysfunctions. Thus, the possibility of falling and balance problems arise due to the postural control deficiencies that occur as a result of the deterioration in the integration of multi-sensory information. We propose a novel rehabilitation framework, Integrated Balance Rehabilitation (I-BaR), to improve the effectiveness of the rehabilitation with objective assessment, individualized therapy, convenience with different disability levels and adoption of an assist-as-needed paradigm and, with an integrated rehabilitation process as a whole, i.e., ankle-foot preparation, balance, and stepping phases, respectively. Integrated Balance Rehabilitation allows patients to improve their balance ability by providing multi-modal feedback: visual via utilization of Virtual Reality; vestibular via anteroposterior and mediolateral perturbations with the robotic platform; proprioceptive via haptic feedback.Comment: 37 pages, 2 figures, journal pape

Virtual reality obstacle crossing: adaptation, retention and transfer to the physical world

Virtual reality (VR) paradigms are increasingly being used in movement and exercise sciences with the aim to enhance motor function and stimulate motor adaptation in healthy and pathological conditions. Locomotor training based in VR may be promising for motor skill learning, with transfer of VR skills to the physical world in turn required to benefit functional activities of daily life. This PhD project aims to examine locomotor adaptations to repeated VR obstacle crossing in healthy young adults as well as transfers to the untrained limb and the physical world, and retention potential of the learned skills. For these reasons, the current thesis comprises three studies using controlled VR obstacle crossing interventions during treadmill walking. In the first and second studies we investigated adaptation to crossing unexpectedly appearing virtual obstacles, with and without feedback about crossing performance, and its transfer to the untrained leg. In the third study we investigated transfer of virtual obstacle crossing to physical obstacles of similar size to the virtual ones, that appeared at the same time point within the gait cycle. We also investigated whether the learned skills can be retained in each of the environments over one week. In all studies participants were asked to walk on a treadmill while wearing a VR headset that represented their body as an avatar via real-time synchronised optical motion capture. Participants had to cross virtual and/or physical obstacles with and without feedback about their crossing performance. If applicable, feedback was provided based on motion capture immediately after virtual obstacle crossing. Toe clearance, margin of stability, and lower extremity joint angles in the sagittal plane were calculated for the crossing legs to analyse adaptation, transfer, and retention of obstacle crossing performance. The main outcomes of the first and second studies were that crossing multiple virtual obstacles increased participants’ dynamic stability and led to a nonlinear adaptation of toe clearance that was enhanced by visual feedback about crossing performance. However, independent of the use of feedback, no transfer to the untrained leg was detected. Moreover, despite significant and rapid adaptive changes in locomotor kinematics with repeated VR obstacle crossing, results of the third study revealed limited transfer of learned skills from virtual to physical obstacles. Lastly, despite full retention over one week in the virtual environment we found only partial retention when crossing a physical obstacle while walking on the treadmill. In summary, the findings of this PhD project confirmed that repeated VR obstacle perturbations can effectively stimulate locomotor skill adaptations. However, these are not transferable to the untrained limb irrespective of enhanced awareness and feedback. Moreover, the current data provide evidence that, despite significant adaptive changes in locomotion kinematics with repeated practice of obstacle crossing under VR conditions, transfer to and retention in the physical environment is limited. It may be that perception-action coupling in the virtual environment, and thus sensorimotor coordination, differs from the physical world, potentially inhibiting retained transfer between those two conditions. Accordingly, VR-based locomotor skill training paradigms need to be considered carefully if they are to replace training in the physical world

Trunk Rehabilitation Using Cable-Driven Robotic Systems

Upper body control is required to complete many daily tasks. One needs to stabilize the head and trunk over the pelvis, as one shifts the center of mass to interact with the world. While healthy individuals can perform activities that require leaning, reaching, and grasping readily, those with neurological and musculoskeletal disorders present with control deficits. These deficits can lead to difficulty in shifting the body center of mass away from the stable midline, leading to functional limitations and a decline in the quality of activity. Often these patient groups use canes, walkers, and wheelchairs for support, leading to occasional strapping or joint locking of the body for trunk stabilization. Current rehabilitation strategies focus on isolated components of stability. This includes strengthening, isometric exercises, hand-eye coordination tasks, isolated movement, and proprioceptive training. Although all these components are evidence based and directly correlate to better stability, motor learning theories such as those by Nikolai Bernstein, suggest that task and context specific training can lead to better outcomes. In specific, based on our experimentation, we believe functional postural exploration, while encompassing aspects of strengthening, hand-eye coordination, and proprioceptive feedback can provide better results. In this work, we present two novel cable robotic platforms for seated and standing posture training. The Trunk Support Trainer (TruST) is a platform for seated posture rehabilitation that provides controlled external wrench on the human trunk in any direction in real-time. The Stand Trainer is a platform for standing posture rehabilitation that can control the trunk, pelvis, and knees, simultaneously. The system works through the use of novel force-field algorithms that are modular and user-specific. The control uses an assist-as-needed strategy to apply forces on the user during regions of postural instability. The device also allows perturbations for postural reactive training. We have conducted several studies using healthy adult populations and pilot studies on patient groups including cerebral palsy, cerebellar ataxia, and spinal cord injury. We propose new training methods that incorporate motor learning theory and objective interventions for improving posture control. We identify novel methods to characterize posture in form of the “8-point star test”. This is to assess the postural workspace. We also demonstrate novel methods for functional training of posture and balance. Our results show that training with our robotic platforms can change the trunk kinematics. Specifically, healthy adults are able to translate the trunk further and rotate the trunk more anteriorly in the seated position. In the standing position, they can alter their reach strategy to maintain the upper trunk more vertically while reaching. Similarly, Cerebral Palsy patients improve their trunk translations, reaching workspace, and maintain a more vertical posture after training, in the seated position. Our results also showed that an Ataxia patient was able to improve their reaching workspace and trunk translations in the standing position. Finally, our results show that the robotic platforms can successfully reduce trunk and pelvis sway in spinal cord injury patients. The results of the pilot studies suggest that training with our robotic platforms and methods is beneficial in improving trunk control

Visual determinants of postural control and perception during physical and visual motion

The control of balance and posture is a critical task of daily life to limit the risk of falls and potential injury. In order to be successful in the control of balance the central nervous system utilizes sensory feedback from the visual, proprioceptive/somtatosensory and vestibular systems. It is through the detection, processing and perception of these sensory cues that allow us to form an accurate representation of postural events and respond accordingly. In this dissertation I investigate how we perceive postural events, how this perception can change with altered visual cues introduced through virtual reality and how virtual visual motion with differing context can alter postural responses. This dissertation aims to determine the following: (1) to determine if methodological changes effect an individuals perception of postural instability onset, (2) to investigate if visual information can alter our perception of instability onset, (3) to investigate if visual motion with differing visual characteristics can alter postural responses. Results indicate that the methodology utilized during a temporal order judgement task has an effect on the perception of postural instability onset. Additionally, it was observed that virtual visual height impacts the precision of perceptual responses to postural instability onset. Finally, virtual visual motion with differing visual context appeared to only be affected by visual motion duration. However, there were also strong individual differences in postural responses to visual motion, which has not been broadly addressed in the literature. As a whole this thesis can exemplify the importance of visual information on both perceptual and behavioural responses related to posture and balance