Sensorimotor Rehabilitation Promotes Vestibular Compensation in a Rodent Model of Acute Peripheral Vestibulopathy by Promoting Microgliogenesis in the Deafferented Vestibular Nuclei.

Emna Marouane,Alain Tonetto,Nada El Mahmoudi,Guillaume Rastoldo,Christian Chabbert,Frédéric Xavier,Agnès Lapôtre,David Péricat,Vincent Artzner,Olivier Dumas,Isabelle Watabe,Brahim Tighilet

doi:10.3390/cells10123377

Abstract

Acute peripheral vestibulopathy leads to a cascade of symptoms involving balance and gait disorders that are particularly disabling for vestibular patients. Vestibular rehabilitation protocols have proven to be effective in improving vestibular compensation in clinical practice. Yet, the underlying neurobiological correlates remain unknown. The aim of this study was to highlight the behavioural and cellular consequences of a vestibular rehabilitation protocol adapted to a rat model of unilateral vestibular neurectomy. We developed a progressive sensory-motor rehabilitation task, and the behavioural consequences were quantified using a weight-distribution device. This analysis method provides a precise and ecological analysis of posturolocomotor vestibular deficits. At the cellular level, we focused on the analysis of plasticity mechanisms expressed in the vestibular nuclei. The results obtained show that vestibular rehabilitation induces a faster recovery of posturolocomotor deficits during vestibular compensation associated with a decrease in neurogenesis and an increase in microgliogenesis in the deafferented medial vestibular nucleus. This study reveals for the first time a part of the underlying adaptative neuroplasticity mechanisms of vestibular rehabilitation. These original data incite further investigation of the impact of rehabilitation on animal models of vestibulopathy. This new line of research should improve the management of vestibular patients.

Highlights

At rest and during displacements, postural adaptations must be made in real time to manage one’s balance in the face of environmental disturbances
We show that vestibular rehabilitation induces a faster recovery of posturolocomotor deficits during vestibular compensation associated with a decrease in neurogenesis and an increase in microgliogenesis in the deafferented medial vestibular nucleus
We have shown in the unilateral vestibular neurectomy (UVN) feline model that treatment with BDNF considerably increases the level of cell proliferation and survival in all deafferented vestibular nuclei (VN) [11]

Summary

Introduction

At rest and during displacements, postural adaptations must be made in real time to manage one’s balance in the face of environmental disturbances. The vestibular nuclei (VN) located in the brain stem receive afferences from all these sensory modalities Integration of these information by the VN allows to provide posturolocomotor responses adapted to the external environment [1]. The return to electrophysiological homeostasis, considered the key parameter for vestibular functional recovery, takes place via a mosaic of neuroplasticity mechanisms occurring within the deafferented VN [8]. Among these mechanisms, reactive neurogliogenesis has been observed in numerous studies in rat and feline unilateral vestibular neurectomy (UVN) models [9,10,11,12,13] and favour vestibular function recovery [13]. Numerous studies highlighted the beneficial effects of physical exercise on neurogenesis and brain plasticity in numerous models of brain pathologies [25,26,27]

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