Effects of vestibular neurectomy and neural compensation on head movements in patients undergoing vestibular schwannoma resection

The Journal of Physiology

Ostrander

Roat

et al. 2021

Self Cite

Key points Sensory systems are adapted to the statistical structure of natural stimuli, thereby optimizing neural coding. Head motion during natural activities is first sensed and then processed by central vestibulo‐motor pathways to influence subsequent behaviour, thereby establishing a feedback loop. To investigate the role of this vestibular feedback on the statistical structure of the head movements, we compared head movements in patients with unilateral vestibular loss and healthy controls. We show that the loss of vestibular feedback substantially alters the statistical structure of head motion for activities that require rapid online feedback control and predict this change by modelling the effects of increased movement variability. Our findings suggest that, following peripheral vestibular loss, changes in the reliability of the sensory input to central pathways impact the statistical structure of head motion during voluntary behaviours. Abstract It is widely believed that sensory systems are adapted to optimize neural coding of their natural stimuli. Recent evidence suggests that this is the case for the vestibular system, which senses head movement and contributes to essential functions ranging from the most automatic reflexes to voluntary motor control. During everyday behaviours, head motion is sensed by the vestibular system. In turn, this sensory feedback influences subsequent behaviour, raising the questions of whether and how real‐time feedback provided by the vestibular system alters the statistical structure of head movements. We predicted that a reduction in vestibular feedback would alter head movement statistics, particularly for tasks reliant on rapid vestibular feedback. To test this proposal, we recorded six‐dimensional head motion in patients with variable degrees of unilateral vestibular loss during standard balance and gait tasks, as well as dynamic self‐paced activities. While distributions of linear accelerations and rotational velocities were comparable for patients and age‐matched healthy controls, comparison of power spectra revealed significant differences during more dynamic and challenging activities. Specifically, consistent with our prediction, head movement power spectra were significantly altered in patients during two tasks that required rapid online vestibular feedback: active repetitive jumping and walking on foam. Using computational methods, we analysed concurrently measured torso motion and identified increases in head–torso movement variability. Taken together, our results demonstrate that vestibular loss significantly alters head movement statistics and further suggest that increased variability and impaired feedback to internal models required for accurate motor control contribute to the observed changes.

Section: Vestibular Loss Alters Head Motion Statistics Of Activities Requiring Online Feedbackmentioning

confidence: 89%

Section: Introductionmentioning

confidence: 99%

Loss of peripheral vestibular input alters the statistics of head movement experienced during natural self‐motion

The Journal of Physiology

Ostrander

Roat

et al. 2021

Self Cite

“…Comparisons were also made between the head movement kinematics of preoperative versus postoperative VS subjects. Additionally, we correlated these kinematic data with standard clinical outcome measures [16][17][18][19] to determine whether postoperative head kinematics during balance exercises correlate with preoperative clinical measures. Finally, we addressed whether it was possible to compute a robust "kinematic score" based on head kinematic data obtained from a subset of exercises.…”

Section: Introductionmentioning

confidence: 99%

Head movement kinematics are altered during balance stability exercises in individuals with vestibular schwannoma

J NeuroEngineering Rehabil

Wang

Millar

et al. 2022

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Background Balance stabilization exercises are often prescribed to facilitate compensation in individuals with vestibular schwannoma (VS). However, both the assessment and prescription of these exercises are reliant on clinical observations and expert opinion rather than on quantitative evidence. The aim of this study was to quantify head motion kinematics in individuals with vestibular loss while they performed commonly prescribed balance stability exercises. Methods Using inertial measurement units, head movements of individuals with vestibular schwannoma were measured before and after surgical deafferentation and compared with age-matched controls. Results We found that individuals with vestibular schwannoma experienced more variable head motion compared to healthy controls both pre- and postoperatively, particularly in absence of visual input, but that there was little difference between preoperative and postoperative kinematic measurements for our vestibular schwannoma group. We further found correlations between head motion kinematic measures during balance exercises, performed in the absence of visual input, and multiple clinical measurements for preoperative VS subjects. Subjects with higher head motion variability also had worse DVA scores, moved more slowly during the Timed up and Go and gait speed tests, and had lower scores on the functional gait assessment. In contrast, we did not find strong correlations between clinical measures and postoperative head kinematics for the same VS subjects. Conclusions Our data suggest that further development of such metrics based on the quantification of head motion has merit for the assessment and prescription of balance exercises, as demonstrated by the calculation of a “kinematic score” for identifying the most informative balance exercise (i.e., “Standing on foam eyes closed”).

“…Notably, the dynamics of the head movements generated in both types of exercises (peak head velocities ∼100–300 deg/s, frequency range extending to ∼20 Hz) paralleled those of natural head movement recorded during daily activities. 2,3,25,26 We then compared the head movement patterns of patients to those of healthy controls to reveal patients’ compensatory strategies.…”

Section: Introductionmentioning

confidence: 99%

Continuous Head Motion is a Greater Motor Control Challenge than Transient Head Motion in Patients with Loss of Vestibular Function

Wang

Neurorehabil Neural Repair

Millar

et al. 2021

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Background. The vestibular system is vital for gaze stability via the vestibulo-ocular reflex, which generates compensatory eye motion in the direction opposite to head motion. Consequently, individuals with peripheral vestibular loss demonstrate impaired gaze stability that reduces functional capacity and quality of life. To facilitate patients’ compensatory strategies, two classes of gaze stabilization exercises are often prescribed: (i) transient (eg, ballistic) and (ii) continuous. However, the relative benefits of these two classes of exercises are not well understood. Objective. To quantify head motion kinematics in patients with vestibular loss while they performed both classes of exercises. Methods. Using inertial measurement units, head movements of 18 vestibular schwannoma patients were measured before and after surgical deafferentation and compared with age-matched controls. Results. We found that the head movement during both classes of exercises paralleled those of natural head movement recorded during daily activities. However, head movement patterns were more informative for continuous than transient exercises in distinguishing patients from healthy controls. Specifically, we observed coupling between kinematic measures in control subjects that was absent in patients for continuous but not transient head motion exercises. In addition, kinematic measures (eg, cycle duration) were predictive of standard clinical measures for continuous but not transient head motion exercises. Conclusions. Our data suggest that performing continuous head motion is a greater motor control challenge than transient head motion in patients with less reliable vestibular feedback during the sub-acute stage of recovery, which may also prove to be a reliable measure of progression in vestibular rehabilitation protocols.