Cargando…

Lack of neural contributions to the summating potential in humans with Meniere’s disease

OBJECTIVE: To investigate the electrophysiology of the cochlear summating potential (SP) in patients with Meniere’s disease (MD). Although long considered a purely hair cell potential, recent studies show a neural contribution to the SP. Patients with MD have an enhanced SP compared to those without...

Descripción completa

Detalles Bibliográficos
Autores principales: Riggs, William J., Fontenot, Tatyana E., Hiss, Meghan M., Varadarajan, Varun, Moberly, Aaron C., Adunka, Oliver F., Fitzpatrick, Douglas C.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9768452/
https://www.ncbi.nlm.nih.gov/pubmed/36570833
http://dx.doi.org/10.3389/fnins.2022.1039986
_version_ 1784854171278639104
author Riggs, William J.
Fontenot, Tatyana E.
Hiss, Meghan M.
Varadarajan, Varun
Moberly, Aaron C.
Adunka, Oliver F.
Fitzpatrick, Douglas C.
author_facet Riggs, William J.
Fontenot, Tatyana E.
Hiss, Meghan M.
Varadarajan, Varun
Moberly, Aaron C.
Adunka, Oliver F.
Fitzpatrick, Douglas C.
author_sort Riggs, William J.
collection PubMed
description OBJECTIVE: To investigate the electrophysiology of the cochlear summating potential (SP) in patients with Meniere’s disease (MD). Although long considered a purely hair cell potential, recent studies show a neural contribution to the SP. Patients with MD have an enhanced SP compared to those without the disease. Consequently, this study was to determine if the enhancement of the SP was in whole or part due to neural dysfunction. DESIGN: Study participants included 41 adults with MD and 53 subjects with auditory neuropathy spectrum disorder (ANSD), undergoing surgery where the round window was accessible. ANSD is a condition with known neural dysfunction, and thus represents a control group for the study. The ANSD subjects and 17 of the MD subjects were undergoing cochlear implantation (CI) surgery; the remaining MD subjects were undergoing either endolymphatic sac decompression or labyrinthectomy to alleviate the symptoms of MD. Electrocochleography was recorded from the round window using high intensity (90 dB nHL) tone bursts. The SP and compound action potential (CAP) were measured to high frequencies (> = 2 kHz) and the SP, cochlear microphonic (CM) and auditory nerve neurophonic (ANN) to low frequencies. Linear mixed models were used to assess differences between MD and ANSD subjects. RESULTS: Across frequencies, the MD subjects had smaller alternating current (AC) response than the ANSD subjects (F = 31.6(1),(534), p < 0.001), but the SP magnitudes were larger (F = 94.3(1),(534), p < 0.001). For frequencies less than 4 kHz the SP magnitude in the MD group was significantly correlated with the magnitude of the CM (p’s < 0.001) but not in the ANSD group (p’s > 0.05). Finally, the relative proportions of both ANN and CAP were greater in MD compared to ANSD subjects. The shapes of the waveforms in the MD subjects showed the presence of multiple components contributing to the SP, including outer and inner hair cells and neural activity. CONCLUSION: The results support the view that the increased negative polarity SP in MD subjects is due to a change in the operating point of hair cells rather than a loss of neural contribution. The steady-state SP to tones in human subjects is a mixture of different sources with different polarities.
format Online
Article
Text
id pubmed-9768452
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher Frontiers Media S.A.
record_format MEDLINE/PubMed
spelling pubmed-97684522022-12-22 Lack of neural contributions to the summating potential in humans with Meniere’s disease Riggs, William J. Fontenot, Tatyana E. Hiss, Meghan M. Varadarajan, Varun Moberly, Aaron C. Adunka, Oliver F. Fitzpatrick, Douglas C. Front Neurosci Neuroscience OBJECTIVE: To investigate the electrophysiology of the cochlear summating potential (SP) in patients with Meniere’s disease (MD). Although long considered a purely hair cell potential, recent studies show a neural contribution to the SP. Patients with MD have an enhanced SP compared to those without the disease. Consequently, this study was to determine if the enhancement of the SP was in whole or part due to neural dysfunction. DESIGN: Study participants included 41 adults with MD and 53 subjects with auditory neuropathy spectrum disorder (ANSD), undergoing surgery where the round window was accessible. ANSD is a condition with known neural dysfunction, and thus represents a control group for the study. The ANSD subjects and 17 of the MD subjects were undergoing cochlear implantation (CI) surgery; the remaining MD subjects were undergoing either endolymphatic sac decompression or labyrinthectomy to alleviate the symptoms of MD. Electrocochleography was recorded from the round window using high intensity (90 dB nHL) tone bursts. The SP and compound action potential (CAP) were measured to high frequencies (> = 2 kHz) and the SP, cochlear microphonic (CM) and auditory nerve neurophonic (ANN) to low frequencies. Linear mixed models were used to assess differences between MD and ANSD subjects. RESULTS: Across frequencies, the MD subjects had smaller alternating current (AC) response than the ANSD subjects (F = 31.6(1),(534), p < 0.001), but the SP magnitudes were larger (F = 94.3(1),(534), p < 0.001). For frequencies less than 4 kHz the SP magnitude in the MD group was significantly correlated with the magnitude of the CM (p’s < 0.001) but not in the ANSD group (p’s > 0.05). Finally, the relative proportions of both ANN and CAP were greater in MD compared to ANSD subjects. The shapes of the waveforms in the MD subjects showed the presence of multiple components contributing to the SP, including outer and inner hair cells and neural activity. CONCLUSION: The results support the view that the increased negative polarity SP in MD subjects is due to a change in the operating point of hair cells rather than a loss of neural contribution. The steady-state SP to tones in human subjects is a mixture of different sources with different polarities. Frontiers Media S.A. 2022-12-07 /pmc/articles/PMC9768452/ /pubmed/36570833 http://dx.doi.org/10.3389/fnins.2022.1039986 Text en Copyright © 2022 Riggs, Fontenot, Hiss, Varadarajan, Moberly, Adunka and Fitzpatrick. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Neuroscience
Riggs, William J.
Fontenot, Tatyana E.
Hiss, Meghan M.
Varadarajan, Varun
Moberly, Aaron C.
Adunka, Oliver F.
Fitzpatrick, Douglas C.
Lack of neural contributions to the summating potential in humans with Meniere’s disease
title Lack of neural contributions to the summating potential in humans with Meniere’s disease
title_full Lack of neural contributions to the summating potential in humans with Meniere’s disease
title_fullStr Lack of neural contributions to the summating potential in humans with Meniere’s disease
title_full_unstemmed Lack of neural contributions to the summating potential in humans with Meniere’s disease
title_short Lack of neural contributions to the summating potential in humans with Meniere’s disease
title_sort lack of neural contributions to the summating potential in humans with meniere’s disease
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9768452/
https://www.ncbi.nlm.nih.gov/pubmed/36570833
http://dx.doi.org/10.3389/fnins.2022.1039986
work_keys_str_mv AT riggswilliamj lackofneuralcontributionstothesummatingpotentialinhumanswithmenieresdisease
AT fontenottatyanae lackofneuralcontributionstothesummatingpotentialinhumanswithmenieresdisease
AT hissmeghanm lackofneuralcontributionstothesummatingpotentialinhumanswithmenieresdisease
AT varadarajanvarun lackofneuralcontributionstothesummatingpotentialinhumanswithmenieresdisease
AT moberlyaaronc lackofneuralcontributionstothesummatingpotentialinhumanswithmenieresdisease
AT adunkaoliverf lackofneuralcontributionstothesummatingpotentialinhumanswithmenieresdisease
AT fitzpatrickdouglasc lackofneuralcontributionstothesummatingpotentialinhumanswithmenieresdisease