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Schematic of turn movement. Initiation of the turn movement was referenced from the ipsilateral foot contact prior to the turn (IFC1). Turn completion was referenced from the ipsilateral foot contact following the turn (IFC2). Lead foot distances were calculated as the distance between IFC1 and a defined center point (indicated) of the turn movement space
Source publication
Walking and turning is a movement that places individuals with Parkinson's disease (PD) at increased risk for fall-related injury. However, turning is an essential movement in activities of daily living, making up to 45 % of the total steps taken in a given day. Hypotheses regarding how turning is controlled suggest an essential role of anticipator...
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Citations
... One way to objectify this deviation of the saccades is to compare the eye positions between the end positions of the two fast phases and determine a deviation (Fig. 1d). We argue that the evaluation of the fast component of VORS deficit-related saccades, in particular, has excellent potential to improve our understanding of the interaction of VORS deficit and mobility impairment as changes in saccade latency have already been demonstrated in PD patients with increased risk of falling, which have an increased latency of saccades, compared to PD patients without increased fall risk [34], and in PD patients, compared to healthy adults, during turns [35]. ...
Background
Visual acuity and image stability are crucial for daily activities, particularly during head motion. The vestibulo-ocular reflex (VOR) and its suppression (VORS) support stable fixation of objects of interest. The VOR drives a reflexive eye movement to counter retinal slip of a stable target during head motion. In contrast, VORS inhibits this countermovement when the target stimulus is in motion. The VORS allows for object fixation when it aligns with the direction of the head’s movement, or when an object within or outside the peripheral vision needs to be focused upon.
Summary
Deficits of the VORS have been linked to age-related diseases such as balance deficits associated with an increased fall risk. Therefore, the accurate assessment of the VORS is of particular clinical relevance. However, current clinical assessment methods for VORS are mainly qualitative and not sufficiently standardised. Recent advances in digital health technology, such as smartphone-based videooculography, offer a promising alternative for assessing VORS in a more accessible, efficient, and quantitative manner. Moreover, integrating mobile eye-tracking technology with virtual reality environments allows for the implementation of controlled VORS assessments with different visual inputs. These assessment approaches allow the extraction of novel parameters with potential pathomechanistic and clinical relevance.
Key Messages
We argue that researchers and clinicians can obtain a more nuanced understanding of this ocular stabilisation reflex and its associated pathologies by harnessing digital health technology for VORS assessment. Further research is warranted to explore the technologies’ full potential and utility in clinical practice.
... In addition, there was a main effect of turn speed on the number of fast phases, showing that the longer the turn duration the more eye movements they made. Eye movement and turning kinematics have been reported to be altered significantly in clinical populations with turning problems, and a causal link between oculomotor deficits and turning dysfunction has been suggested 12,28,30 . However, the effect of turn speed on the spatiotemporal fast phase characteristics in individuals without PD is unknown, therefore it is not possible to determine whether differences between groups are due to pathology caused by PD or simply alteration in behaviour by turn speed. ...
... The oculomotor system has access to information from the visual cues and visual systems in obtaining spatial and egocentric information that is passed to the motor system 12,29 . The central nervous system (CNS) uses visual information to plan the postural adjustments and to coordinate whole-body responses [30][31][32] . Furthermore, the anticipatory eye and head movements is involved in the synergy of movement during turning 30,32,33 . ...
... The central nervous system (CNS) uses visual information to plan the postural adjustments and to coordinate whole-body responses [30][31][32] . Furthermore, the anticipatory eye and head movements is involved in the synergy of movement during turning 30,32,33 . Taking these together, it is likely that the motor symptom of PD such as bradykinesia and rigidity may limit head movement resulting in both anticipatory head and eye movement. ...
Issues around turning can impair daily tasks and trigger episodes of freezing of gait in individuals with Parkinson's disease (PD). Slow speeds associated with aging produce a more en-bloc movement strategy which have been linked with falls while turning. However, the influence of speed of turning on the complex whole-body coordination considering eye movements, turning kinematics, and stepping characteristics during turning has not been examined. The aim of this study was to investigate if individuals with PD have a different response to changes in turning speed compared to healthy older adults during 180° standing turns. 20 individuals with PD and 20 healthy age matched adults participated in this study. Data were collected during clockwise and counter-clockwise turns at three self-selected speeds in a randomised order: (a) normal; (b) faster than normal; and (c) slower than normal. Eye movement and turning kinematics were investigated using electrooculography and Inertial Measurement Units. Mixed Model Analysis of Variance (MM ANOVA) tests with post hoc pairwise comparisons were performed to assess the differences between groups and turning speed. In addition, further post hoc Repeated Measures ANOVA (RM ANOVA) tests were performed if any significant interactions were seen between groups and turning speed. Significant interaction effects were found in eye movement and turning kinematics, and the RM ANOVA showed significant main effects for turning speeds within the PD and the control groups. Turning slowly resulted in similar alterations in eye movement, turning kinematics and stepping characteristics in the PD group and the healthy controls. However, individuals with PD showed a different response to the healthy controls, with a greater delay in eye movement and onset latency of segments in turning kinematics and step variables between the different speeds. These findings help our understanding regarding the turning strategies in individuals with PD. The incorporation of guidance with regard to faster turning speeds may be useful in the management of individuals with PD. Clinical training using different turn directions and speeds may improve coordination, increase confidence and reduce the risk of falling.
... It would be of benefit to examine gait performance in more complex situations. Finally, the findings of visuospatial recognition were not evaluated during walking; 3DGA analysis using a wearable eye tracker that monitors eye movements during walking will lead to a better understanding of them (Ambati et al. 2016). ...
Williams syndrome (WS) is a genetically based neurodevelopmental disorder characterized by intellectual disability and impaired visuospatial recognition. The aim of this study was to analyze the gait characteristics of WS children with impaired visuospatial recognition using a three-dimensional gait analysis (3DGA) to clarify the gait adaptation needed to compensate for it. 3DGA was performed in 8 WS children with impaired visuospatial recognition (mean age, 11.8 years) and 9 age-, sex-, height-, and weight-matched controls. Clinical data, fundamental motor tests, and gait variables while walking on a flat surface and walking up a mat were compared between the two groups, and the correlations between variables were analyzed in the WS children. WS children showed impairment of balance function without muscle weakness. In walking on a flat surface, the WS group showed reduced walking speed, short step length, increased variability of step length, increased knee flexion throughout the stance phase, increased horizontal pelvic range of motion (ROM), and a low Gait Deviation Index and a high Gait Profile Score, which are indices of gait quality. In walking up a mat, the WS group showed further reduced walking speed and decreased sagittal hip flexion and ankle dorsiflexion ROM in the swing phase. Impaired balance function was significantly correlated with increased variability of step length and decreased sagittal ankle dorsiflexion ROM in the swing phase. The detailed gait pattern of WS children with impaired visuospatial recognition was presented. These findings show that impaired visuospatial recognition and balance function contribute to gait adaptation.
... Turning while walking is defined as having a robust cranio-caudal segment sequence resulting in a head first turning strategy (Spildooren et al., 2017) or steering synergy (Patla et al., 1999;Ambati et al., 2016). This strategy requires independent control of the segments, increasing the complexity of control by the CNS, but also allows individuals to respond to perturbations (Assaiante and Amblard, 1995). ...
... However, individuals with Parkinson's disease, unlike neurotypical young adults, do not anticipate a turn by moving their eyes and head in the direction of the turn. Instead, individuals with PD maintain the eyes straight ahead until the onset of the turn and use an "enbloc" turning strategy (Ambati et al., 2016). These observations suggest that en-bloc segment coordination may result from a lack of anticipatory redirection of the eyes. ...
... The turn movement was defined by the ipsilateral foot contact (IFC1) prior to change in direction (onset) to the ipsilateral foot contact (IFC2) following the change in direction (completion), as used in previous work (Patla et al., 1999;Ambati et al., 2016). Refer to Supplementary Figure 1 in supplementary files for further definition. ...
Anticipatory eye movement promotes cranio-caudal sequencing during walking turns. Clinical groups, such as Parkinson's disease (PD), do not produce anticipatory eye movements, leading to increased risk of falls. Visual cues may promote anticipatory eye movement by guiding the eyes into the turn. This study examined if visual cues could train anticipatory eye movement. Ten neurotypical young adults and 6 adults with PD completed three blocks of walking trials. Trials were blocked by visual condition: non-cued baseline turns (5 trials), visually cued turns (10 trials), and non-cued post turns (5 trials). A Delsys Trigno (Delsys, Boston, MA) recorded horizontal saccades at 1024 Hz via electrooculography (EOG). Two Optotrak cameras (Northern Digital Inc., ON, Canada) captured body segment kinematics at 120 Hz. Initiation of segment rotation with respect to ipsilateral foot contact (IFC1) prior to the turn was calculated. Neurotypical young adults (NYA) produced typical cranio-caudal rotation sequences during walking turns. Eyes led (407 ms prior to IFC1), followed by the head (50 ms prior to IFC1), then trunk and pelvis. In contrast, PD produced no anticipatory eye or segment movement at baseline. During pre-trials the eyes moved 96 ms after IFC1 and segment movement was initiated by the pelvis followed by trunk and head segments. After visual cue training however, PD produced anticipatory eye movements 161 ms prior to IFC1, followed by the head 88 ms following IFC1 but ahead of trunk and pelvis onset. These results suggest visual cues assist in producing cranio-caudal control during walking turns in PD.
... Persons with PD exhibit lower saccade amplitude, higher saccadic latencies, and longer durations to achieve targets (Mosimann et al., 2005;Terao et al., 2011). Deficits in voluntary saccade control contribute to mobility impairments related to turning during navigation (Ambati et al., 2016;Nemanich and Earhart, 2016). It has been noted that turning during navigation in persons with PD increases instability and risk of falling (Stack and Ashburn, 1999). ...
... Other treatments include the anti-saccade paradigm, which requires the suppression of a saccade to a stimulus and voluntary saccade to a location of equal eccentricity in the opposite direction (Jamadar et al., 2015). However, such studies focus on accuracy and error rate and do not address hypometria as is needed for navigation (Jamadar et al., 2015;Ambati et al., 2016). ...
... Physical mobility is of the utmost importance for the quality of life in the general population. Furthermore, recent PD literature indicates that abnormal saccade behavior is associated with the freezing of gait and difficulty in navigation (Lohnes and Earhart, 2011;Ambati et al., 2016;Nemanich and Earhart, 2016;Stuart et al., 2017). Improving abnormal saccade behavior may affect freezing of gait and other motor-related PD symptoms. ...
Background: Voluntary saccade function gradually decreases during both the progression of Parkinson’s disease (PD) and neurologically healthy adult aging. Voluntary saccades display decreased length and increased saccade latency, duration, and the number of compensatory saccades in aging and PD. Saccades serve as the key eye movement for maintaining salient features of the visual environment on the high visual acuity fovea of the retina. Abnormal saccade behavior has been associated with freezing of gait in PD. We have not identified any studies that have investigated improvement in voluntary saccade function using voluntary saccade training.
Objective: We report an experimental protocol that tests a training paradigm following the principle of specificity to improve voluntary saccade velocity and amplitude, while decreasing latency and the number of compensatory saccades.
Methods: Persons with PD (n = 22) and persons with no known neurological disorders (n = 22) between the ages of 40 and 65 years will be recruited. In a randomized-block study design, all participants will perform voluntary saccades to targets in eight cardinal and intercardinal directions. In each of the eight sessions during the four-week intervention period, participants will train at three target amplitudes. Participants will perform 40 trials for each amplitude block, consisting of five randomly presented repetitions for each direction. Voluntary and reflexive saccades will be recorded pre- and post-intervention, along with clinical mobility assessment using the Movement Disorder Society Unified Parkinson’s Disease Rating Scale. Mobility scores, the amplitude, latency, and duration of the first saccade, and the number of saccades to reach the fixation target will be analyzed using an ANOVA of mixed effects.
Discussion: This protocol holds promise as a potential method to improve voluntary saccade function in persons with PD. Should persons with PD not improve on any outcome following the intervention, this lack of response may support the use of saccade assessment as a response biomarker for the diagnosis of PD.
Trial Registration: This protocol was retrospectively registered at ISRCTN (ISRCTN.com) since July 25, 2018. The first participant was recruited March 12, 2016. The protocol identifier is 17784042.
Descriptive Title: A two-arm, pre/post-protocol to compare the effects of a four-week voluntary saccade training intervention in persons with Parkinson’s disease and healthy adults aged forty years or older.
... More than that, there is evidence that the disorder of body movement system leads to the constraining eye movement in patients with Parkinson's disease (Ambati et al., 2016), which implies a common or interactive system to control eye and body movement simultaneously (Srivastava et al., 2018). The current study may also shed lights on the potential clinical anchor points of the disorders in locomotion-eye coordination with zebrafish model (Huang and Neuhauss, 2008). ...
Visual stabilization is an inevitable requirement for animals during active motion interaction with the environment. Visual motion cues of the surroundings or induced by self-generated behaviors are perceived then trigger proper motor responses mediated by neural representations conceptualized as the internal model: one part of it predicts the consequences of sensory dynamics as a forward model, another part generates proper motor control as a reverse model. However, the neural circuits between the two models remain mostly unknown. Here, we demonstrate that an internal component, the efference copy, coordinated the two models in a push-pull manner by generating extra reset saccades during active motion processing in larval zebrafish. Calcium imaging indicated that the saccade preparation circuit is enhanced while the velocity integration circuit is inhibited during the interaction, balancing the internal representations from both directions. This is the first model of efference copy on visual stabilization beyond the sensorimotor stage.
... Decreased gait velocity [165][166][167] Disordered regulation of footstep timing; reduced stride length 168 Cerebellar ataxia Square-wave jerks, saccadic dysmetria, and reduced saccadic velocity [169][170][171] Decreased step length, stride length, and gait speed [172][173][174] PD: Parkinson disease, PSP: progressive supranuclear palsy other study, saccadic frequency was found to increase in both patients with PD and their age-matched controls when approaching a turn, but the PD patients made fewer preparatory saccades than the controls before the turn. 178,179 During the turn, the PD patients made more saccades, and the saccadic velocity was slower than that of the controls. 180 The likely neural components affecting both saccades and locomotion in PD include the STN, the SNr, and the MLR/MFR. ...
Human locomotion involves a complex interplay among multiple brain regions and depends on constant feedback from the visual system. We summarize here the current understanding of the relationship among fixations, saccades, and gait as observed in studies sampling eye movements during locomotion, through a review of the literature and a synthesis of the relevant knowledge on the topic. A significant overlap in locomotor and saccadic neural circuitry exists that may support this relationship. Several animal studies have identified potential integration nodes between these overlapping circuitries. Behavioral studies that explored the relationship of saccadic and gait-related impairments in normal conditions and in various disease states are also discussed. Eye movements and locomotion share many underlying neural circuits, and further studies can leverage this interplay for diagnostic and therapeutic purposes.
... The requirement to adjust the CoM trajectory from time-to-time during walking with OC increased variability of spatial-temporal parameters in the PDG, which may be interpreted as deficits in the internal rhythmicity [25], causing inconsistency in stepping patterns and balance impairments [17]. In addition, previous studies have demonstrated visual sampling impairment in PDG [26,27], which requires visual identification of obstacles. The greater dependency on visual obstacle information may be explained due to working memory and/or executive function deficits caused by the disease. ...
The aim of this study was to analyze the motor and visual strategies used when walking around (circumvention) an obstacle in patients with Parkinson's disease (PD), in addition to the effects of dopaminergic medication on these strategies. To answer the study question, people with PD (15) and neurologically healthy individuals (15 - CG) performed the task of obstacle circumvention during walking (5 trials of unobstructed walking and obstacle circumvention). The following parameters were analyzed: body clearance (longer mediolateral distance during obstacle circumvention of the center of mass -CoM- to the obstacle), horizontal distance (distance of the CoM at the beginning of obstacle circumvention to the obstacle), circumvention strategy ("lead-out" or "lead-in" strategy), spatial-temporal of each step, and number of fixations, the mean duration of the fixations and time of fixations according to areas of interest. In addition, the variability of each parameter was calculated. The results indicated that people with PD and the CG presented similar obstacle circumvention strategies (no differences between groups for body clearance, horizontal distance to obstacle, or obstacle circumvention strategy), but the groups used different adjustments to perform these strategies (people with PD performed adjustments during both the approach and circumvention steps and presented greater visual dependence on the obstacle; the CG adjusted only the final step before obstacle circumvention). Moreover, without dopaminergic medication, people with PD reduced body clearance and increased the use of a "lead-out" strategy, variability in spatial-temporal parameters, and dependency on obstacle information, increasing the risk of contact with the obstacle during circumvention.
Objectives
To describe changes in balance, walking speed, functional mobility, and eye movements following an activity-oriented physiotherapy (AOPT) or its combination with eye movement training (AOPT-E) in patients with Parkinson’s disease (PD). To explore the feasibility of a full-scale randomised controlled trial (RCT).
Methods
Using an assessor-blinded pilot RCT, 25 patients with PD were allocated to either AOPT or AOPT-E. Supervised interventions were performed 30 minutes, 4x/weekly, for 4 weeks, alongside inpatient rehabilitation. Outcomes were assessed at baseline and post-intervention, including dynamic balance, walking speed, functional and dual-task mobility, ability to safely balance, health-related quality of life (HRQoL), depression, and eye movements (number/duration of fixations) using a mobile eye tracker. Freezing of gait (FOG), and falls-related self-efficacy were assessed at baseline, post-intervention, and 4-week follow-up. Effect sizes of 0.10 were considered weak, 0.30 moderate, and ≥0.50 strong. Feasibility was assessed using predefined criteria: recruitment, retention and adherence rates, adverse events, falls, and post-intervention acceptability using qualitative interviews.
Results
Improvements were observed in dynamic balance (effect size r = 0.216–0.427), walking speed (r = 0.165), functional and dual-task mobility (r = 0.306–0.413), ability to safely balance (r = 0.247), HRQoL (r = 0.024–0.650), and depression (r = 0.403). Falls-related self-efficacy (r = 0.621) and FOG (r = 0.248) showed varied improvements, partly sustained at follow-up. Eye movement improvements were observed after AOPT-E only. Feasibility analysis revealed that recruitment was below target, with less than two patients recruited per month due to COVID-19 restrictions. Feasibility targets were met, with a retention rate of 96% (95% confidence interval [CI]: 77.68–99.79) and a 98.18% (95% CI: 96.12–99.20) adherence rate, exceeding the targets of 80% and 75%, respectively. One adverse event unrelated to the study intervention confirmed intervention safety, and interview data indicated high intervention acceptability.
Conclusions
AOPT-E and AOPT appeared to be effective in patients with PD. Feasibility of a larger RCT was confirmed and is needed to validate results.
Turning during ambulation has a frequent occurrence during activities of daily living. Yet, little is known about turning gait while most previous investigations have focused on straight line walking, although gait analysis methods have made great progress recently. Gait analysis of normal turning while walking will provide greater insight into the body reorientation, and help identify and manage pathological gait, guide rehabilitation programs and design assistance devices. Therefore, the aim of this thesis was to quantitatively analyze turning gait of healthy young adults regarding dynamic stability, kinematics and kinetics. Specific purpose was to quantify the gait adaptability during transient turns in comparison with straight gait, and the gait differences between the two turning strategies by comparing step turn and spin turn.
Fifteen healthy young adults were instructed to perform straight walking, 45° step turn to the left and 45° spin turn to the right at natural speed, where the turning limb was right leg (also the dominant leg). Marker position data and ground reaction data were collected simultaneously using a motion capture system and force plates. Turning gait was separated into approach, turn, and depart phases, and time normalization was employed. For gait parameters, a one-way repeated measures analysis of variance was run to test for significant differences between matching phases of different tasks and between different phases of the same task. For gait variables, bootstrap confidence bands were applied to detect differences between different tasks.
First dynamic stability analysis was achieved with margin of stability as a key measure. Results revealed that the poorest anterior stability occurred at middle of swing phase while the posterior at heel strike during straight and turning gait; and the poorest lateral stability appeared at contralateral heel strike during straight, in turn phase of step turn whereas depart of spin.
Then kinematic analysis was conducted with spatiotemporal parameters and lower limb joint angles as key measures. For spin turn, gait speed was slightly faster, the step and stride length larger than those of straight walking and step turn, and step width the smallest in turn phase. For step turn, speed was slightly slower than straight walking, and step width the smallest in depart. Long swing phases were observed in turns. For joint angles of turning limb between tasks, the same pattern was found in the sagittal plane, but quite differences during turn phases in the coronal and the horizontal.
Finally, kinetic analysis was executed with ground reaction force (GRF) and lower limb joint moments as key measures. For GRF under the turning limb during turn phase, the medial force increased in step turn; while the lateral existed and the braking rose in spin. For joint moments of turning limb during turn phase, the hip abduction moment and the ankle dorsiflexion and internal rotation were large for step turn; whereas the hip extension and adduction, the knee extension and internal rotation and the ankle plantar flexion and external rotation for spin.
This work quantified the gait adaptability during transient turns and the gait differences between the two turning strategies in healthy young adults, and could provide theoretical basis and data support for rehabilitation evaluation of gait function, development of gait assistive aids and gait planning of biped robot.
KEY WORDS: Gait analysis, Turning gait, Dynamic stability, Kinematics, Kinetics
