Subtle alterations of vestibulomotor functioning in conductive hearing loss
IntroductionConductive hearing loss (CHL) attenuates the ability to transmit air conducted sounds to the ear. In humans, severe hearing loss is often accompanied by alterations to other neural systems, such as the vestibular system; however, the inter-relations are not well understood. The overall g...
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Frontiers Media S.A.
2023-08-01
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| Series: | Frontiers in Neuroscience |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fnins.2023.1057551/full |
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| author | Francis A. M. Manno Francis A. M. Manno Francis A. M. Manno Francis A. M. Manno Pikting Cheung Vardhan Basnet Muhammad Shehzad Khan Yuqi Mao Leilei Pan Victor Ma William C. Cho Shile Tian Ziqi An Yanqiu Feng Yanqiu Feng Yanqiu Feng Yi-Ling Cai Martin Pienkowski Condon Lau Condon Lau |
| author_facet | Francis A. M. Manno Francis A. M. Manno Francis A. M. Manno Francis A. M. Manno Pikting Cheung Vardhan Basnet Muhammad Shehzad Khan Yuqi Mao Leilei Pan Victor Ma William C. Cho Shile Tian Ziqi An Yanqiu Feng Yanqiu Feng Yanqiu Feng Yi-Ling Cai Martin Pienkowski Condon Lau Condon Lau |
| author_sort | Francis A. M. Manno |
| collection | DOAJ |
| description | IntroductionConductive hearing loss (CHL) attenuates the ability to transmit air conducted sounds to the ear. In humans, severe hearing loss is often accompanied by alterations to other neural systems, such as the vestibular system; however, the inter-relations are not well understood. The overall goal of this study was to assess vestibular-related functioning proxies in a rat CHL model.MethodsMale Sprague–Dawley rats (N=134, 250g, 2months old) were used in a CHL model which produced a >20dB threshold shift induced by tympanic membrane puncture. Auditory brainstem response (ABRs) recordings were used to determine threshold depth at different times before and after CHL. ABR threshold depths were assessed both manually and by an automated ABR machine learning algorithm. Vestibular-related functioning proxy assessment was performed using the rotarod, balance beam, elevator vertical motion (EVM) and Ferris-wheel rotation (FWR) assays.ResultsThe Pre-CHL (control) threshold depth was 27.92dB±11.58dB compared to the Post-CHL threshold depth of 50.69dB±13.98dB (mean±SD) across the frequencies tested. The automated ABR machine learning algorithm determined the following threshold depths: Pre-CHL=24.3dB, Post-CHL same day=56dB, Post-CHL 7 days=41.16dB, and Post-CHL 1 month=32.5dB across the frequencies assessed (1, 2, 4, 8, 16, and 32kHz). Rotarod assessment of motor function was not significantly different between pre and post-CHL (~1week) rats for time duration (sec) or speed (RPM), albeit the former had a small effect size difference. Balance beam time to transverse was significantly longer for post-CHL rats, likely indicating a change in motor coordination. Further, failure to cross was only noted for CHL rats. The defection count was significantly reduced for CHL rats compared to control rats following FWR, but not EVM. The total distance traveled during open-field examination after EVM was significantly different between control and CHL rats, but not for FWR. The EVM is associated with linear acceleration (acting in the vertical plane: up-down) stimulating the saccule, while the FWR is associated with angular acceleration (centrifugal rotation about a circular axis) stimulating both otolith organs and semicircular canals; therefore, the difference in results could reflect the specific vestibular-organ functional role.DiscussionLess movement (EVM) and increase time to transverse (balance beam) may be associated with anxiety and alterations to defecation patterns (FWR) may result from autonomic disturbances due to the impact of hearing loss. In this regard, vestibulomotor deficits resulting in changes in balance and motion could be attributed to comodulation of auditory and vestibular functioning. Future studies should manipulate vestibular functioning directly in rats with CHL. |
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| last_indexed | 2024-03-12T12:28:47Z |
| publishDate | 2023-08-01 |
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| series | Frontiers in Neuroscience |
| spelling | doaj.art-84a45dd41a034fd5a7caa6fac28f63092023-08-29T17:47:38ZengFrontiers Media S.A.Frontiers in Neuroscience1662-453X2023-08-011710.3389/fnins.2023.10575511057551Subtle alterations of vestibulomotor functioning in conductive hearing lossFrancis A. M. Manno0Francis A. M. Manno1Francis A. M. Manno2Francis A. M. Manno3Pikting Cheung4Vardhan Basnet5Muhammad Shehzad Khan6Yuqi Mao7Leilei Pan8Victor Ma9William C. Cho10Shile Tian11Ziqi An12Yanqiu Feng13Yanqiu Feng14Yanqiu Feng15Yi-Ling Cai16Martin Pienkowski17Condon Lau18Condon Lau19Department of Physics, East Carolina University, Greenville, NC, United StatesDepartment of Biomedical Engineering, Center for Imaging Science, Whiting School of Engineering, Johns Hopkins University, Baltimore, MD, United StatesCenter for Advanced Nuclear Safety and Sustainable Development, City University of Hong Kong, Kowloon, Hong Kong SAR, ChinaDepartment of Physics, City University of Hong Kong, Kowloon, Hong Kong SAR, ChinaDepartment of Physics, City University of Hong Kong, Kowloon, Hong Kong SAR, ChinaDepartment of Physics, City University of Hong Kong, Kowloon, Hong Kong SAR, ChinaDepartment of Physics, City University of Hong Kong, Kowloon, Hong Kong SAR, ChinaDepartment of Nautical Injury Prevention, Faculty of Navy Medicine, Second Military Medical University, Shanghai, ChinaDepartment of Nautical Injury Prevention, Faculty of Navy Medicine, Second Military Medical University, Shanghai, ChinaDepartment of Clinical Oncology, Queen Elizabeth Hospital, Kowloon, Hong Kong SAR, ChinaDepartment of Clinical Oncology, Queen Elizabeth Hospital, Kowloon, Hong Kong SAR, ChinaSchool of Biomedical Engineering, Southern Medical University, Guangzhou, ChinaSchool of Biomedical Engineering, Southern Medical University, Guangzhou, ChinaSchool of Biomedical Engineering, Southern Medical University, Guangzhou, ChinaGuangdong Provincial Key Laboratory of Medical Image Processing and Guangdong Province Engineering Laboratory for Medical Imaging and Diagnostic Technology, Southern Medical University, Guangzhou, ChinaKey Laboratory of Mental Health of the Ministry of Education, Guangdong-Hong Kong-Macao Greater Bay Area Center for Brain Science and Brain-Inspired Intelligence, Guangdong Province Key Laboratory of Psychiatric Disorders, Department of Neurobiology, School of Basic Medical Sciences, Southern Medical University, Guangzhou, ChinaDepartment of Physics, City University of Hong Kong, Kowloon, Hong Kong SAR, China0Osborne College of Audiology, Salus University, Elkins Park, PA, United StatesCenter for Advanced Nuclear Safety and Sustainable Development, City University of Hong Kong, Kowloon, Hong Kong SAR, ChinaDepartment of Physics, City University of Hong Kong, Kowloon, Hong Kong SAR, ChinaIntroductionConductive hearing loss (CHL) attenuates the ability to transmit air conducted sounds to the ear. In humans, severe hearing loss is often accompanied by alterations to other neural systems, such as the vestibular system; however, the inter-relations are not well understood. The overall goal of this study was to assess vestibular-related functioning proxies in a rat CHL model.MethodsMale Sprague–Dawley rats (N=134, 250g, 2months old) were used in a CHL model which produced a >20dB threshold shift induced by tympanic membrane puncture. Auditory brainstem response (ABRs) recordings were used to determine threshold depth at different times before and after CHL. ABR threshold depths were assessed both manually and by an automated ABR machine learning algorithm. Vestibular-related functioning proxy assessment was performed using the rotarod, balance beam, elevator vertical motion (EVM) and Ferris-wheel rotation (FWR) assays.ResultsThe Pre-CHL (control) threshold depth was 27.92dB±11.58dB compared to the Post-CHL threshold depth of 50.69dB±13.98dB (mean±SD) across the frequencies tested. The automated ABR machine learning algorithm determined the following threshold depths: Pre-CHL=24.3dB, Post-CHL same day=56dB, Post-CHL 7 days=41.16dB, and Post-CHL 1 month=32.5dB across the frequencies assessed (1, 2, 4, 8, 16, and 32kHz). Rotarod assessment of motor function was not significantly different between pre and post-CHL (~1week) rats for time duration (sec) or speed (RPM), albeit the former had a small effect size difference. Balance beam time to transverse was significantly longer for post-CHL rats, likely indicating a change in motor coordination. Further, failure to cross was only noted for CHL rats. The defection count was significantly reduced for CHL rats compared to control rats following FWR, but not EVM. The total distance traveled during open-field examination after EVM was significantly different between control and CHL rats, but not for FWR. The EVM is associated with linear acceleration (acting in the vertical plane: up-down) stimulating the saccule, while the FWR is associated with angular acceleration (centrifugal rotation about a circular axis) stimulating both otolith organs and semicircular canals; therefore, the difference in results could reflect the specific vestibular-organ functional role.DiscussionLess movement (EVM) and increase time to transverse (balance beam) may be associated with anxiety and alterations to defecation patterns (FWR) may result from autonomic disturbances due to the impact of hearing loss. In this regard, vestibulomotor deficits resulting in changes in balance and motion could be attributed to comodulation of auditory and vestibular functioning. Future studies should manipulate vestibular functioning directly in rats with CHL.https://www.frontiersin.org/articles/10.3389/fnins.2023.1057551/fullvestibular dysfunctioneighth cranial nervevestibulocochlearvestibularmotionpsychomotor |
| spellingShingle | Francis A. M. Manno Francis A. M. Manno Francis A. M. Manno Francis A. M. Manno Pikting Cheung Vardhan Basnet Muhammad Shehzad Khan Yuqi Mao Leilei Pan Victor Ma William C. Cho Shile Tian Ziqi An Yanqiu Feng Yanqiu Feng Yanqiu Feng Yi-Ling Cai Martin Pienkowski Condon Lau Condon Lau Subtle alterations of vestibulomotor functioning in conductive hearing loss Frontiers in Neuroscience vestibular dysfunction eighth cranial nerve vestibulocochlear vestibular motion psychomotor |
| title | Subtle alterations of vestibulomotor functioning in conductive hearing loss |
| title_full | Subtle alterations of vestibulomotor functioning in conductive hearing loss |
| title_fullStr | Subtle alterations of vestibulomotor functioning in conductive hearing loss |
| title_full_unstemmed | Subtle alterations of vestibulomotor functioning in conductive hearing loss |
| title_short | Subtle alterations of vestibulomotor functioning in conductive hearing loss |
| title_sort | subtle alterations of vestibulomotor functioning in conductive hearing loss |
| topic | vestibular dysfunction eighth cranial nerve vestibulocochlear vestibular motion psychomotor |
| url | https://www.frontiersin.org/articles/10.3389/fnins.2023.1057551/full |
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