Differences in the Structure and Function of the Vestibular Efferent System Among Vertebrates.

Kathleen E Cullen,Rui-Han Wei

doi:10.3389/fnins.2021.684800

Abstract

The role of the mammalian vestibular efferent system in everyday life has been a long-standing mystery. In contrast to what has been reported in lower vertebrate classes, the mammalian vestibular efferent system does not appear to relay inputs from other sensory modalities to the vestibular periphery. Furthermore, to date, the available evidence indicates that the mammalian vestibular efferent system does not relay motor-related signals to the vestibular periphery to modulate sensory coding of the voluntary self-motion generated during natural behaviors. Indeed, our recent neurophysiological studies have provided insight into how the peripheral vestibular system transmits head movement-related information to the brain in a context independent manner. The integration of vestibular and extra-vestibular information instead only occurs at next stage of the mammalian vestibular system, at the level of the vestibular nuclei. The question thus arises: what is the physiological role of the vestibular efferent system in mammals? We suggest that the mammalian vestibular efferent system does not play a significant role in short-term modulation of afferent coding, but instead plays a vital role over a longer time course, for example in calibrating and protecting the functional efficacy of vestibular circuits during development and aging in a role analogous the auditory efferent system.

Highlights

While the function of the mammalian auditory efferent system is well understood, the role of the mammalian vestibular efferent system remains a mystery
The question arises: what is the physiological role of the vestibular efferent system in mammals? We suggest that the mammalian vestibular efferent system does not play a significant role in short-term modulation of afferent coding, but instead plays a vital role over a longer time course, for example in calibrating and protecting the functional efficacy of vestibular circuits during development and aging in a role analogous the auditory efferent system
We focus on how the vestibular efferent systems transmit extra-vestibular sensory and motor information to the vestibular periphery in lower vertebrates

Summary

INTRODUCTION

While the function of the mammalian auditory efferent system is well understood, the role of the mammalian vestibular efferent system remains a mystery. A prevailing hypothesis has been that a key function of the vestibular efferent system is to alter peripheral motion sensing during active movements In this view, the vestibular efferent pathway transmits motor-related signals to the vestibular periphery that modulate the responses of receptor cells within the semicircular canal and otolith sensory organs to effectively extend their head motion coding range during voluntary behaviors (reviewed in Goldberg, 2000; Mathews et al, 2017). Using a semi-isolated in vitro anaesthetized larval Xenopus preparation, showed that motor signals originating in the spinal locomotor circuitry are conveyed to the vestibular periphery to produce an overall reduction in afferent sensitivity to passive vestibular stimulation (Figure 3B; Chagnaud et al, 2015) The results of these studies have led to the common view that motor efference copies (i.e., an internal copy of the motor command) used to generate active behaviors are conveyed by the vestibular efferent system to the periphery to modulate responses in receptor cells and vestibular afferent fibers. This alternate strategy allows pathway-selective modulation of relationships between motor signals and the resultant vestibular feedback during active behaviors

FUTURE DIRECTIONS AND CONCLUSION

SUMMARY