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

Kathleen E Cullen,Jérome Carriot,Isabelle Mackrous

doi:10.1038/s41467-021-27753-z

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.

Highlights

The vestibular system detects head motion to coordinate vital reflexes and provide our sense of balance and spatial orientation
Regardless of their organ of origin (Fig. 1a), vestibular afferents display a wide range of resting discharge in the absence of movement (CV*, see Methods)
Our results indicate that the observed increase in the mean firing rate of irregular otolith afferents during running was due to nonlinear responses evoked by the higher amplitude vestibular stimulation

Summary

Introduction

The vestibular system detects head motion to coordinate vital reflexes and provide our sense of balance and spatial orientation. The proposal that the EVS plays a role in adaptive coding during voluntary head movements is at odds with the results of neurophysiological studies in primates showing no difference in vestibular afferent encoding of active orienting head movements and comparable passive head movements[15,16,17]. These prior studies did not record afferent responses during active locomotion. We speculate that context-dependent modulation occurs centrally, in a pathway-specific manner, to ensure that coding is consistent with behavioral goals during locomotion

Methods

Results

Conclusion