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Processing of auditory information in forebrain regions after hearing loss in adulthood: Behavioral and electrophysiological studies in a rat model

BACKGROUND: Hearing loss was proposed as a factor affecting development of cognitive impairment in elderly. Deficits cannot be explained primarily by dysfunctional neuronal networks within the central auditory system. We here tested the impact of hearing loss in adult rats on motor, social, and cogn...

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Autores principales: Johne, Marie, Helgers, Simeon O. A., Alam, Mesbah, Jelinek, Jonas, Hubka, Peter, Krauss, Joachim K., Scheper, Verena, Kral, Andrej, Schwabe, Kerstin
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9684731/
https://www.ncbi.nlm.nih.gov/pubmed/36440269
http://dx.doi.org/10.3389/fnins.2022.966568
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author Johne, Marie
Helgers, Simeon O. A.
Alam, Mesbah
Jelinek, Jonas
Hubka, Peter
Krauss, Joachim K.
Scheper, Verena
Kral, Andrej
Schwabe, Kerstin
author_facet Johne, Marie
Helgers, Simeon O. A.
Alam, Mesbah
Jelinek, Jonas
Hubka, Peter
Krauss, Joachim K.
Scheper, Verena
Kral, Andrej
Schwabe, Kerstin
author_sort Johne, Marie
collection PubMed
description BACKGROUND: Hearing loss was proposed as a factor affecting development of cognitive impairment in elderly. Deficits cannot be explained primarily by dysfunctional neuronal networks within the central auditory system. We here tested the impact of hearing loss in adult rats on motor, social, and cognitive function. Furthermore, potential changes in the neuronal activity in the medial prefrontal cortex (mPFC) and the inferior colliculus (IC) were evaluated. MATERIALS AND METHODS: In adult male Sprague Dawley rats hearing loss was induced under general anesthesia with intracochlear injection of neomycin. Sham-operated and naive rats served as controls. Postsurgical acoustically evoked auditory brainstem response (ABR)-measurements verified hearing loss after intracochlear neomycin-injection, respectively, intact hearing in sham-operated and naive controls. In intervals of 8 weeks and up to 12 months after surgery rats were tested for locomotor activity (open field) and coordination (Rotarod), for social interaction and preference, and for learning and memory (4-arms baited 8-arms radial maze test). In a final setting, electrophysiological recordings were performed in the mPFC and the IC. RESULTS: Locomotor activity did not differ between deaf and control rats, whereas motor coordination on the Rotarod was disturbed in deaf rats (P < 0.05). Learning the concept of the radial maze test was initially disturbed in deaf rats (P < 0.05), whereas retesting every 8 weeks did not show long-term memory deficits. Social interaction and preference was also not affected by hearing loss. Final electrophysiological recordings in anesthetized rats revealed reduced firing rates, enhanced irregular firing, and reduced oscillatory theta band activity (4–8 Hz) in the mPFC of deaf rats as compared to controls (P < 0.05). In the IC, reduced oscillatory theta (4–8 Hz) and gamma (30–100 Hz) band activity was found in deaf rats (P < 0.05). CONCLUSION: Minor and transient behavioral deficits do not confirm direct impact of long-term hearing loss on cognitive function in rats. However, the altered neuronal activities in the mPFC and IC after hearing loss indicate effects on neuronal networks in and outside the central auditory system with potential consequences on cognitive function.
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spelling pubmed-96847312022-11-25 Processing of auditory information in forebrain regions after hearing loss in adulthood: Behavioral and electrophysiological studies in a rat model Johne, Marie Helgers, Simeon O. A. Alam, Mesbah Jelinek, Jonas Hubka, Peter Krauss, Joachim K. Scheper, Verena Kral, Andrej Schwabe, Kerstin Front Neurosci Neuroscience BACKGROUND: Hearing loss was proposed as a factor affecting development of cognitive impairment in elderly. Deficits cannot be explained primarily by dysfunctional neuronal networks within the central auditory system. We here tested the impact of hearing loss in adult rats on motor, social, and cognitive function. Furthermore, potential changes in the neuronal activity in the medial prefrontal cortex (mPFC) and the inferior colliculus (IC) were evaluated. MATERIALS AND METHODS: In adult male Sprague Dawley rats hearing loss was induced under general anesthesia with intracochlear injection of neomycin. Sham-operated and naive rats served as controls. Postsurgical acoustically evoked auditory brainstem response (ABR)-measurements verified hearing loss after intracochlear neomycin-injection, respectively, intact hearing in sham-operated and naive controls. In intervals of 8 weeks and up to 12 months after surgery rats were tested for locomotor activity (open field) and coordination (Rotarod), for social interaction and preference, and for learning and memory (4-arms baited 8-arms radial maze test). In a final setting, electrophysiological recordings were performed in the mPFC and the IC. RESULTS: Locomotor activity did not differ between deaf and control rats, whereas motor coordination on the Rotarod was disturbed in deaf rats (P < 0.05). Learning the concept of the radial maze test was initially disturbed in deaf rats (P < 0.05), whereas retesting every 8 weeks did not show long-term memory deficits. Social interaction and preference was also not affected by hearing loss. Final electrophysiological recordings in anesthetized rats revealed reduced firing rates, enhanced irregular firing, and reduced oscillatory theta band activity (4–8 Hz) in the mPFC of deaf rats as compared to controls (P < 0.05). In the IC, reduced oscillatory theta (4–8 Hz) and gamma (30–100 Hz) band activity was found in deaf rats (P < 0.05). CONCLUSION: Minor and transient behavioral deficits do not confirm direct impact of long-term hearing loss on cognitive function in rats. However, the altered neuronal activities in the mPFC and IC after hearing loss indicate effects on neuronal networks in and outside the central auditory system with potential consequences on cognitive function. Frontiers Media S.A. 2022-11-10 /pmc/articles/PMC9684731/ /pubmed/36440269 http://dx.doi.org/10.3389/fnins.2022.966568 Text en Copyright © 2022 Johne, Helgers, Alam, Jelinek, Hubka, Krauss, Scheper, Kral and Schwabe. 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
Johne, Marie
Helgers, Simeon O. A.
Alam, Mesbah
Jelinek, Jonas
Hubka, Peter
Krauss, Joachim K.
Scheper, Verena
Kral, Andrej
Schwabe, Kerstin
Processing of auditory information in forebrain regions after hearing loss in adulthood: Behavioral and electrophysiological studies in a rat model
title Processing of auditory information in forebrain regions after hearing loss in adulthood: Behavioral and electrophysiological studies in a rat model
title_full Processing of auditory information in forebrain regions after hearing loss in adulthood: Behavioral and electrophysiological studies in a rat model
title_fullStr Processing of auditory information in forebrain regions after hearing loss in adulthood: Behavioral and electrophysiological studies in a rat model
title_full_unstemmed Processing of auditory information in forebrain regions after hearing loss in adulthood: Behavioral and electrophysiological studies in a rat model
title_short Processing of auditory information in forebrain regions after hearing loss in adulthood: Behavioral and electrophysiological studies in a rat model
title_sort processing of auditory information in forebrain regions after hearing loss in adulthood: behavioral and electrophysiological studies in a rat model
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9684731/
https://www.ncbi.nlm.nih.gov/pubmed/36440269
http://dx.doi.org/10.3389/fnins.2022.966568
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