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A primal role for the vestibular sense in the development of coordinated locomotion.

ABSTRACT: Mature locomotion requires that animal nervous systems coordinate distinct groups of muscles. The pressures that guide the development of coordination are not well understood. To understand how and why coordination might emerge, we measured the kinematics of spontaneous vertical locomotion across early development in zebrafish (Danio rerio) . We found that zebrafish used their pectoral fins and bodies synergistically during upwards swims. As larvae developed, they changed the way they coordinated fin and body movements, allowing them to climb with increasingly stable postures. This fin-body synergy was absent in vestibular mutants, suggesting sensed imbalance promotes coordinated movements. Similarly, synergies were systematically altered following cerebellar lesions, identifying a neural substrate regulating fin-body coordination. Together these findings link the vestibular sense to the maturation of coordinated locomotion. Developing zebrafish improve postural stability by changing fin-body coordination. We therefore propose that the development of coordinated locomotion is regulated by vestibular sensation.

SUBMITTER: Ehrlich DE

PROVIDER: S-EPMC6783269 | biostudies-literature | 2019 Oct

REPOSITORIES: biostudies-literature

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A primal role for the vestibular sense in the development of coordinated locomotion.

Ehrlich David E DE Schoppik David D

eLife 20191008

Mature locomotion requires that animal nervous systems coordinate distinct groups of muscles. The pressures that guide the development of coordination are not well understood. To understand how and why coordination might emerge, we measured the kinematics of spontaneous vertical locomotion across early development in zebrafish (<i>Danio rerio</i>) . We found that zebrafish used their pectoral fins and bodies synergistically during upwards swims. As larvae developed, they changed the way they coo ...[more]

PMID: 31591962

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Project description:To evaluate vestibular function in the clinic, current assessments are applied under static conditions, such as with the subject in a sitting or supine position. Considering the complexities of daily activities, the combination of dynamic activities, dynamic visual acuity (DVA) and postural control could produce an evaluation that better reflects vestibular function in daily activities. Objective: To develop a novel sensor-based system to investigate DVA, walking trajectory, head and trunk movements and the chest-pelvis rotation ratio during forward and backward overground walking in both healthy individuals and patients with vestibular hypofunction. Methods: Fifteen healthy subjects and 7 patients with bilateral vestibular hypofunction (BVH) were recruited for this study. Inertial measurement units were placed on each subject's head and torso. Each subject walked forward and backward for 5 m twice with 2 Hz head yaw. Our experiment comprised 2 stages. In stage 1, we measured forward (FW), backward (BW), and medial-lateral (MLW) walking trajectories; head and trunk movements; and the chest-pelvis rotation ratio. In stage 2, we measured standing and locomotion DVA (loDVA). Using Mann-Whitney U-test, we compared the abovementioned parameters between the 2 groups. Results: Patients exhibited an in-phase chest/pelvis reciprocal rotation ratio only in FW. The walking trajectory deviation, calculated by normalizing the summation of medial-lateral swaying with 1/2 body height (%), was significantly larger (FW mean ± standard deviation: 20.4 ± 7.1% (median (M)/interquartile range (IQR): 19.3/14.4-25.2)in healthy vs. 43.9 ± 27. 3% (M/IQR: 36.9/21.3-56.9) in patients, p = 0.020)/(BW mean ± standard deviation: 19.2 ± 11.5% (M/IQR: 13.6/10.4-25.3) in healthy vs. 29.3 ± 6.4% (M/IQR: 27.7/26.5-34.4) in patients, p = 0.026), and the walking DVA was also significantly higher (LogMAR score in the patient group [FW LogMAR: rightDVA: mean ± standard deviation:0.127 ± 0.081 (M/IQR: 0.127/0.036-0.159) in healthy vs. 0.243 ± 0.101 (M/IQR: 0.247/0.143-0.337) in patients (p = 0.013) and leftDVA: 0.136 ± 0.096 (M/IQR: 0.127/0.036-0.176) in healthy vs. 0.258 ± 0.092 (M/IQR: 0.247/0.176-0.301) in patients (p = 0.016); BW LogMAR: rightDVA: mean ± standard deviation: 0.162 ± 0.097 (M/IQR: 0.159/0.097-0.273) in healthy vs. 0.281 ± 0.130 (M/IQR: 0.273/0.176-0.418) in patients(p = 0.047) and leftDVA: 0.156 ± 0.101 (M/IQR: 0.159/0.097-0.198) in healthy vs. 0.298 ± 0.153 (M/IQR: 0.2730/0.159-0.484) in patients (p = 0.038)]. Conclusions: Our sensor-based vestibular evaluation system provided a more functionally relevant assessment for the identification of BVH patients.

Project description:IntroductionThe vestibular system, which encodes our head movement in space, plays an important role in maintaining our balance as we navigate the environment. While in-laboratory research demonstrates that the vestibular system exerts a context-dependent influence on the control of balance during locomotion, differences in whole-body and head kinematics between indoor treadmill and real-world locomotion challenge the generalizability of these findings. Thus, the goal of this study was to characterize vestibular-evoked balance responses in the real world using a fully portable system.MethodsWhile experiencing stochastic electrical vestibular stimulation (0-20 Hz, amplitude peak ± 4.5 mA, root mean square 1.25 mA) and wearing inertial measurement units (IMUs) on the head, low back, and ankles, 10 participants walked outside at 52 steps/minute (∼0.4 m/s) and 78 steps/minute (∼0.8 m/s). We calculated time-dependent coherence (a measure of correlation in the frequency domain) between the applied stimulus and the mediolateral back, right ankle, and left ankle linear accelerations to infer the vestibular control of balance during locomotion.ResultsIn all participants, we observed vestibular-evoked balance responses. These responses exhibited phasic modulation across the stride cycle, peaking during the middle of the single-leg stance in the back and during the stance phase for the ankles. Coherence decreased with increasing locomotor cadence and speed, as observed in both bootstrapped coherence differences (p < 0.01) and peak coherence (low back: 0.23 ± 0.07 vs. 0.16 ± 0.14, p = 0.021; right ankle: 0.38 ± 0.12 vs. 0.25 ± 0.10, p < 0.001; left ankle: 0.33 ± 0.09 vs. 0.21 ± 0.09, p < 0.001).DiscussionThese results replicate previous in-laboratory studies, thus providing further insight into the vestibular control of balance during naturalistic movements and validating the use of this portable system as a method to characterize real-world vestibular responses. This study will help support future work that seeks to better understand how the vestibular system contributes to balance in variable real-world environments.

Project description:Lower-limb exoskeletons have demonstrated great potential for gait rehabilitation in individuals with motor impairments; however, maintaining human-exoskeleton coordination remains a challenge. The coordination problem, referred to as any mismatch or asynchrony between the user's intended trajectories and exoskeleton desired trajectories, leads to sub-optimal gait performance, particularly for individuals with residual motor ability. Here, we investigate the virtual energy regulator (VER)'s ability to generate coordinated locomotion in lower limb exoskeleton. Contribution: (1) In this paper, we experimented VER on a group of nine healthy individuals at different speeds (0.6m/s - 0.85m/s) to study the resultant gait coordination and naturalness on a large group of users. (2) The resultant assisted gait is compared to the natural and passive (zero-torque exoskeleton) walking conditions in terms of muscle activities, kinematic, spatiotemporal and kinetic measures, and questionnaires. (3) Moreover, we presented the VER's convergence proof considering the user contribution to the gait and introduced a metric to measure the user's contribution to gait. (4) We also compared VER performance with the phase-based path controller in terms of muscle effort reduction and joint kinematics using three able-bodied individuals. Results: (1) The results from the VER demonstrate the emergence of natural, coordinated locomotion, resulting in an average muscle effort reduction ranging from 13.1% to 17.7% at different speeds compared to passive walking. (2) The results from VER revealed improvements in all indicators towards natural gait when compared to walking with a zero-torque exoskeleton, for instance, an enhancement in average knee extension ranging from 3.9 to 4.1 degrees. All indicators suggest that the VER preserves natural gait variability and user engagement in locomotion control. (3) Using VER also yields in 13.9%, 15.1%, and 7.0% average muscle effort reduction when compared to the phase-based path controller. (4) Finally, using our proposed metric, we demonstrated that the resultant locomotion limit cycle is a linear combination of human-intended limit cycle and the VER's limit cycle. These findings may have implications for understanding how the central nervous system controls our locomotion.

Project description:BackgroundUni- or bilateral peripheralvestibular impairment causes objective spatial orientation deficits, which can be measured using pen-and-paper-tests or sensorimotor tasks (navigation or pointing). For patients' subjective orientation abilities, questionnaires are commonly used (e.g., Santa Barbara sense of direction scale [SBSODS]). However, the relationship between subjective assessment of spatial skills and objective vestibular function has only been scarcely investigated.MethodsA total of 177 patients (mean age 57.86 ± 17.53 years, 90 females) who presented in our tertiary Center for Vertigo and Balance Disorders underwent neuro-otological examinations, including bithermal water calorics, video head impulse test (vHIT), and testing of the subjective visual vertical (SVV), and filled out the SBSODS (German version). Correlation analyses and linear multiple regression model analyses were performed between vestibular test results and self-assessment scores. Additionally, groupwise vestibular function for patients with low, average, and high self-report scores was analyzed.ResultsForty-two patients fulfilled the diagnostic criteria for bilateral vestibulopathy, 93 for chronic unilateral vestibulopathy (68 unilateral caloric hypofunction and 25 isolated horizontal vestibulo-ocular reflex deficits), and 42 patients had normal vestibular test results. SBSODS scores showed clear sex differences with higher subjective skill levels in males (mean score males: 4.94 ± 0.99, females 4.40 ± 0.94; Student's t-test: t-3.78, p < .001***). No stable correlation between objective vestibular function and subjective sense of spatial orientation was found. A multiple linear regression model could not reliably explain the self-reported variance. The three patient groups with low, average, and high self-assessment-scores showed no significant differences of vestibular function.ConclusionSelf-reported assessment of spatial orientation does not robustly correlate with objective peripheral vestibular function. Therefore, other methods of measuring spatial skills in real-world and virtual environments are required to disclose orientation deficits due to vestibular hypofunction.

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A primal role for the vestibular sense in the development of coordinated locomotion.

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A primal role for the vestibular sense in the development of coordinated locomotion.

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