Lack of neural contributions to the summating potential in humans with Meniere’s disease
ObjectiveTo 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 t...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2022-12-01
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| Series: | Frontiers in Neuroscience |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fnins.2022.1039986/full |
| _version_ | 1811310370499854336 |
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| author | William J. Riggs William J. Riggs Tatyana E. Fontenot Meghan M. Hiss Varun Varadarajan Aaron C. Moberly Oliver F. Adunka Oliver F. Adunka Douglas C. Fitzpatrick |
| author_facet | William J. Riggs William J. Riggs Tatyana E. Fontenot Meghan M. Hiss Varun Varadarajan Aaron C. Moberly Oliver F. Adunka Oliver F. Adunka Douglas C. Fitzpatrick |
| author_sort | William J. Riggs |
| collection | DOAJ |
| description | ObjectiveTo 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.DesignStudy 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.ResultsAcross frequencies, the MD subjects had smaller alternating current (AC) response than the ANSD subjects (F = 31.61,534, p < 0.001), but the SP magnitudes were larger (F = 94.31,534, 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.ConclusionThe 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. |
| first_indexed | 2024-04-13T09:57:46Z |
| format | Article |
| id | doaj.art-a492eab72ae74ff9a08f68a2310d5d86 |
| institution | Directory Open Access Journal |
| issn | 1662-453X |
| language | English |
| last_indexed | 2024-04-13T09:57:46Z |
| publishDate | 2022-12-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Neuroscience |
| spelling | doaj.art-a492eab72ae74ff9a08f68a2310d5d862022-12-22T02:51:19ZengFrontiers Media S.A.Frontiers in Neuroscience1662-453X2022-12-011610.3389/fnins.2022.10399861039986Lack of neural contributions to the summating potential in humans with Meniere’s diseaseWilliam J. Riggs0William J. Riggs1Tatyana E. Fontenot2Meghan M. Hiss3Varun Varadarajan4Aaron C. Moberly5Oliver F. Adunka6Oliver F. Adunka7Douglas C. Fitzpatrick8Department of Otolaryngology-Head and Neck Surgery, The Ohio State University, Columbus, OH, United StatesDepartment of Audiology, Nationwide Children’s Hospital, Columbus, OH, United StatesDepartment of Otolaryngology-Head and Neck Surgery, University of North Carolina at Chapel Hill, Chapel Hill, NC, United StatesDepartment of Otolaryngology-Head and Neck Surgery, The Ohio State University, Columbus, OH, United StatesDepartment of Otolaryngology-Head and Neck Surgery, The Ohio State University, Columbus, OH, United StatesDepartment of Otolaryngology-Head and Neck Surgery, The Ohio State University, Columbus, OH, United StatesDepartment of Otolaryngology-Head and Neck Surgery, The Ohio State University, Columbus, OH, United StatesDepartment of Audiology, Nationwide Children’s Hospital, Columbus, OH, United StatesDepartment of Otolaryngology-Head and Neck Surgery, University of North Carolina at Chapel Hill, Chapel Hill, NC, United StatesObjectiveTo 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.DesignStudy 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.ResultsAcross frequencies, the MD subjects had smaller alternating current (AC) response than the ANSD subjects (F = 31.61,534, p < 0.001), but the SP magnitudes were larger (F = 94.31,534, 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.ConclusionThe 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.https://www.frontiersin.org/articles/10.3389/fnins.2022.1039986/fullelectrocochleographysummating potentialMeniere’s diseaseauditory nerveinner hair cellsouter hair cells |
| spellingShingle | William J. Riggs William J. Riggs Tatyana E. Fontenot Meghan M. Hiss Varun Varadarajan Aaron C. Moberly Oliver F. Adunka Oliver F. Adunka Douglas C. Fitzpatrick Lack of neural contributions to the summating potential in humans with Meniere’s disease Frontiers in Neuroscience electrocochleography summating potential Meniere’s disease auditory nerve inner hair cells outer hair cells |
| 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 | electrocochleography summating potential Meniere’s disease auditory nerve inner hair cells outer hair cells |
| url | https://www.frontiersin.org/articles/10.3389/fnins.2022.1039986/full |
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