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Context-independent encoding of passive and active self-motion in vestibular afferent fibers during locomotion in primates.

ABSTRACT: The vestibular system detects head motion to coordinate vital reflexes and provide our sense of balance and spatial orientation. A long-standing hypothesis has been that projections from the central vestibular system back to the vestibular sensory organs (i.e., the efferent vestibular system) mediate adaptive sensory coding during voluntary locomotion. However, direct proof for this idea has been lacking. Here we recorded from individual semicircular canal and otolith afferents during walking and running in monkeys. Using a combination of mathematical modeling and nonlinear analysis, we show that afferent encoding is actually identical across passive and active conditions, irrespective of context. Thus, taken together our results are instead consistent with the view that the vestibular periphery relays robust information to the brain during primate locomotion, suggesting that context-dependent modulation instead occurs centrally to ensure that coding is consistent with behavioral goals during locomotion.

SUBMITTER: Mackrous I

PROVIDER: S-EPMC8748921 | biostudies-literature | 2022 Jan

REPOSITORIES: biostudies-literature

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Context-independent encoding of passive and active self-motion in vestibular afferent fibers during locomotion in primates.

Mackrous Isabelle I Carriot Jérome J Cullen Kathleen E KE

Nature communications 20220110 1

The vestibular system detects head motion to coordinate vital reflexes and provide our sense of balance and spatial orientation. A long-standing hypothesis has been that projections from the central vestibular system back to the vestibular sensory organs (i.e., the efferent vestibular system) mediate adaptive sensory coding during voluntary locomotion. However, direct proof for this idea has been lacking. Here we recorded from individual semicircular canal and otolith afferents during walking an ...[more]

PMID: 35013266

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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.

Dataset Information

Context-independent encoding of passive and active self-motion in vestibular afferent fibers during locomotion in primates.

Publications

Context-independent encoding of passive and active self-motion in vestibular afferent fibers during locomotion in primates.

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