Sound-Evoked Responses in the Vestibulo-Ocular Reflex Pathways of Rats

Vestibular evoked myogenic potentials (VEMP) have been used to assess otolith function in clinics worldwide. However, there are accumulating evidence suggesting that the clinically used sound stimuli activate not only the otolith afferents, but also the canal afferents, indicating canal contribution...

Full description

Bibliographic Details
Main Authors: Tianwen Chen, Jun Huang, Yue Yu, Xuehui Tang, Chunming Zhang, Youguo Xu, Alberto Arteaga, Jerome Allison, William Mustain, Matthew C. Donald, Tracy Rappai, Michael Zhang, Wu Zhou, Hong Zhu
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-10-01
Series:Frontiers in Neuroscience
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fnins.2021.741571/full
_version_ 1818885356311805952
author Tianwen Chen
Jun Huang
Yue Yu
Xuehui Tang
Chunming Zhang
Youguo Xu
Alberto Arteaga
Jerome Allison
Jerome Allison
William Mustain
Matthew C. Donald
Tracy Rappai
Michael Zhang
Wu Zhou
Wu Zhou
Wu Zhou
Hong Zhu
Hong Zhu
author_facet Tianwen Chen
Jun Huang
Yue Yu
Xuehui Tang
Chunming Zhang
Youguo Xu
Alberto Arteaga
Jerome Allison
Jerome Allison
William Mustain
Matthew C. Donald
Tracy Rappai
Michael Zhang
Wu Zhou
Wu Zhou
Wu Zhou
Hong Zhu
Hong Zhu
author_sort Tianwen Chen
collection DOAJ
description Vestibular evoked myogenic potentials (VEMP) have been used to assess otolith function in clinics worldwide. However, there are accumulating evidence suggesting that the clinically used sound stimuli activate not only the otolith afferents, but also the canal afferents, indicating canal contributions to the VEMPs. To better understand the neural mechanisms underlying the VEMPs and develop discriminative VEMP protocols, we further examined sound-evoked responses of the vestibular nucleus neurons and the abducens neurons, which have the interneurons and motoneurons of the vestibulo-ocular reflex (VOR) pathways. Air-conducted clicks (50–80 dB SL re ABR threshold, 0.1 ms duration) or tone bursts (60–80 dB SL, 125–4,000 Hz, 8 ms plateau, 1 ms rise/fall) were delivered to the ears of Sprague-Dawley or Long-Evans rats. Among 425 vestibular nucleus neurons recorded in anesthetized rats and 18 abducens neurons recorded in awake rats, sound activated 35.9% of the vestibular neurons that increased discharge rates for ipsilateral head rotation (Type I neuron), 15.7% of the vestibular neurons that increased discharge rates for contralateral head rotation (Type II neuron), 57.2% of the vestibular neurons that did not change discharge rates during head rotation (non-canal neuron), and 38.9% of the abducens neurons. Sound sensitive vestibular nucleus neurons and abducens neurons exhibited characteristic tuning curves that reflected convergence of canal and otolith inputs in the VOR pathways. Tone bursts also evoked well-defined eye movements that increased with tone intensity and duration and exhibited peak frequency of ∼1,500 Hz. For the left eye, tone bursts evoked upward/rightward eye movements for ipsilateral stimulation, and downward/leftward eye movements for contralateral stimulation. These results demonstrate that sound stimulation results in activation of the canal and otolith VOR pathways that can be measured by eye tracking devices to develop discriminative tests of vestibular function in animal models and in humans.
first_indexed 2024-12-19T16:04:08Z
format Article
id doaj.art-40f53332e527439591ead6a0431a97cb
institution Directory Open Access Journal
issn 1662-453X
language English
last_indexed 2024-12-19T16:04:08Z
publishDate 2021-10-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Neuroscience
spelling doaj.art-40f53332e527439591ead6a0431a97cb2022-12-21T20:14:52ZengFrontiers Media S.A.Frontiers in Neuroscience1662-453X2021-10-011510.3389/fnins.2021.741571741571Sound-Evoked Responses in the Vestibulo-Ocular Reflex Pathways of RatsTianwen Chen0Jun Huang1Yue Yu2Xuehui Tang3Chunming Zhang4Youguo Xu5Alberto Arteaga6Jerome Allison7Jerome Allison8William Mustain9Matthew C. Donald10Tracy Rappai11Michael Zhang12Wu Zhou13Wu Zhou14Wu Zhou15Hong Zhu16Hong Zhu17Department of Otolaryngology-Head and Neck Surgery, University of Mississippi Medical Center, Jackson, MS, United StatesDepartment of Otolaryngology-Head and Neck Surgery, University of Mississippi Medical Center, Jackson, MS, United StatesDepartment of Otolaryngology-Head and Neck Surgery, University of Mississippi Medical Center, Jackson, MS, United StatesDepartment of Otolaryngology-Head and Neck Surgery, University of Mississippi Medical Center, Jackson, MS, United StatesDepartment of Otolaryngology, First Affiliated Hospital, Shanxi Medical University, Taiyuan, ChinaDepartment of Otolaryngology-Head and Neck Surgery, University of Mississippi Medical Center, Jackson, MS, United StatesDepartment of Otolaryngology-Head and Neck Surgery, University of Mississippi Medical Center, Jackson, MS, United StatesDepartment of Otolaryngology-Head and Neck Surgery, University of Mississippi Medical Center, Jackson, MS, United StatesDepartment of Neurobiology and Anatomical Sciences, University of Mississippi Medical Center, Jackson, MS, United StatesDepartment of Otolaryngology-Head and Neck Surgery, University of Mississippi Medical Center, Jackson, MS, United StatesSchool of Medicine, University of Mississippi Medical Center, Jackson, MS, United StatesSchool of Medicine, University of Mississippi Medical Center, Jackson, MS, United StatesSummer Undergraduate Research Program, University of Mississippi Medical Center, Jackson, MS, United StatesDepartment of Otolaryngology-Head and Neck Surgery, University of Mississippi Medical Center, Jackson, MS, United StatesDepartment of Neurobiology and Anatomical Sciences, University of Mississippi Medical Center, Jackson, MS, United StatesDepartment of Neurology, University of Mississippi Medical Center, Jackson, MS, United StatesDepartment of Otolaryngology-Head and Neck Surgery, University of Mississippi Medical Center, Jackson, MS, United StatesDepartment of Neurobiology and Anatomical Sciences, University of Mississippi Medical Center, Jackson, MS, United StatesVestibular evoked myogenic potentials (VEMP) have been used to assess otolith function in clinics worldwide. However, there are accumulating evidence suggesting that the clinically used sound stimuli activate not only the otolith afferents, but also the canal afferents, indicating canal contributions to the VEMPs. To better understand the neural mechanisms underlying the VEMPs and develop discriminative VEMP protocols, we further examined sound-evoked responses of the vestibular nucleus neurons and the abducens neurons, which have the interneurons and motoneurons of the vestibulo-ocular reflex (VOR) pathways. Air-conducted clicks (50–80 dB SL re ABR threshold, 0.1 ms duration) or tone bursts (60–80 dB SL, 125–4,000 Hz, 8 ms plateau, 1 ms rise/fall) were delivered to the ears of Sprague-Dawley or Long-Evans rats. Among 425 vestibular nucleus neurons recorded in anesthetized rats and 18 abducens neurons recorded in awake rats, sound activated 35.9% of the vestibular neurons that increased discharge rates for ipsilateral head rotation (Type I neuron), 15.7% of the vestibular neurons that increased discharge rates for contralateral head rotation (Type II neuron), 57.2% of the vestibular neurons that did not change discharge rates during head rotation (non-canal neuron), and 38.9% of the abducens neurons. Sound sensitive vestibular nucleus neurons and abducens neurons exhibited characteristic tuning curves that reflected convergence of canal and otolith inputs in the VOR pathways. Tone bursts also evoked well-defined eye movements that increased with tone intensity and duration and exhibited peak frequency of ∼1,500 Hz. For the left eye, tone bursts evoked upward/rightward eye movements for ipsilateral stimulation, and downward/leftward eye movements for contralateral stimulation. These results demonstrate that sound stimulation results in activation of the canal and otolith VOR pathways that can be measured by eye tracking devices to develop discriminative tests of vestibular function in animal models and in humans.https://www.frontiersin.org/articles/10.3389/fnins.2021.741571/fullvestibular-evoked myogenic potential (VEMP)single unit recordingvestibulo ocular reflexotolithcanaleye movement
spellingShingle Tianwen Chen
Jun Huang
Yue Yu
Xuehui Tang
Chunming Zhang
Youguo Xu
Alberto Arteaga
Jerome Allison
Jerome Allison
William Mustain
Matthew C. Donald
Tracy Rappai
Michael Zhang
Wu Zhou
Wu Zhou
Wu Zhou
Hong Zhu
Hong Zhu
Sound-Evoked Responses in the Vestibulo-Ocular Reflex Pathways of Rats
Frontiers in Neuroscience
vestibular-evoked myogenic potential (VEMP)
single unit recording
vestibulo ocular reflex
otolith
canal
eye movement
title Sound-Evoked Responses in the Vestibulo-Ocular Reflex Pathways of Rats
title_full Sound-Evoked Responses in the Vestibulo-Ocular Reflex Pathways of Rats
title_fullStr Sound-Evoked Responses in the Vestibulo-Ocular Reflex Pathways of Rats
title_full_unstemmed Sound-Evoked Responses in the Vestibulo-Ocular Reflex Pathways of Rats
title_short Sound-Evoked Responses in the Vestibulo-Ocular Reflex Pathways of Rats
title_sort sound evoked responses in the vestibulo ocular reflex pathways of rats
topic vestibular-evoked myogenic potential (VEMP)
single unit recording
vestibulo ocular reflex
otolith
canal
eye movement
url https://www.frontiersin.org/articles/10.3389/fnins.2021.741571/full
work_keys_str_mv AT tianwenchen soundevokedresponsesinthevestibuloocularreflexpathwaysofrats
AT junhuang soundevokedresponsesinthevestibuloocularreflexpathwaysofrats
AT yueyu soundevokedresponsesinthevestibuloocularreflexpathwaysofrats
AT xuehuitang soundevokedresponsesinthevestibuloocularreflexpathwaysofrats
AT chunmingzhang soundevokedresponsesinthevestibuloocularreflexpathwaysofrats
AT youguoxu soundevokedresponsesinthevestibuloocularreflexpathwaysofrats
AT albertoarteaga soundevokedresponsesinthevestibuloocularreflexpathwaysofrats
AT jeromeallison soundevokedresponsesinthevestibuloocularreflexpathwaysofrats
AT jeromeallison soundevokedresponsesinthevestibuloocularreflexpathwaysofrats
AT williammustain soundevokedresponsesinthevestibuloocularreflexpathwaysofrats
AT matthewcdonald soundevokedresponsesinthevestibuloocularreflexpathwaysofrats
AT tracyrappai soundevokedresponsesinthevestibuloocularreflexpathwaysofrats
AT michaelzhang soundevokedresponsesinthevestibuloocularreflexpathwaysofrats
AT wuzhou soundevokedresponsesinthevestibuloocularreflexpathwaysofrats
AT wuzhou soundevokedresponsesinthevestibuloocularreflexpathwaysofrats
AT wuzhou soundevokedresponsesinthevestibuloocularreflexpathwaysofrats
AT hongzhu soundevokedresponsesinthevestibuloocularreflexpathwaysofrats
AT hongzhu soundevokedresponsesinthevestibuloocularreflexpathwaysofrats