Auditory sensory deprivation induced by noise exposure exacerbates cognitive decline in a mouse model of Alzheimer’s disease

Although association between hearing impairment and dementia has been widely documented by epidemiological studies, the role of auditory sensory deprivation in cognitive decline remains to be fully understood. To address this issue we investigated the impact of hearing loss on the onset and time-cou...

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Main Authors: Fabiola Paciello, Marco Rinaudo, Valentina Longo, Sara Cocco, Giulia Conforto, Anna Pisani, Maria Vittoria Podda, Anna Rita Fetoni, Gaetano Paludetti, Claudio Grassi
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2021-10-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/70908
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author Fabiola Paciello
Marco Rinaudo
Valentina Longo
Sara Cocco
Giulia Conforto
Anna Pisani
Maria Vittoria Podda
Anna Rita Fetoni
Gaetano Paludetti
Claudio Grassi
author_facet Fabiola Paciello
Marco Rinaudo
Valentina Longo
Sara Cocco
Giulia Conforto
Anna Pisani
Maria Vittoria Podda
Anna Rita Fetoni
Gaetano Paludetti
Claudio Grassi
author_sort Fabiola Paciello
collection DOAJ
description Although association between hearing impairment and dementia has been widely documented by epidemiological studies, the role of auditory sensory deprivation in cognitive decline remains to be fully understood. To address this issue we investigated the impact of hearing loss on the onset and time-course of cognitive decline in an animal model of Alzheimer’s disease (AD), that is the 3×Tg-AD mice and the underlying mechanisms. We found that hearing loss induced by noise exposure in the 3×Tg-AD mice before the phenotype is manifested caused persistent synaptic and morphological alterations in the auditory cortex. This was associated with earlier hippocampal dysfunction, increased tau phosphorylation, neuroinflammation, and redox imbalance, along with anticipated memory deficits compared to the expected time-course of the neurodegenerative phenotype. Our data suggest that a mouse model of AD is more vulnerable to central damage induced by hearing loss and shows reduced ability to counteract noise-induced detrimental effects, which accelerates the neurodegenerative disease onset.
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spelling doaj.art-5de695750b7644e4971a558fe8ee81992022-12-22T03:52:26ZengeLife Sciences Publications LtdeLife2050-084X2021-10-011010.7554/eLife.70908Auditory sensory deprivation induced by noise exposure exacerbates cognitive decline in a mouse model of Alzheimer’s diseaseFabiola Paciello0https://orcid.org/0000-0002-8473-8074Marco Rinaudo1Valentina Longo2https://orcid.org/0000-0002-5763-8879Sara Cocco3Giulia Conforto4Anna Pisani5https://orcid.org/0000-0003-0661-5017Maria Vittoria Podda6https://orcid.org/0000-0002-2779-8417Anna Rita Fetoni7https://orcid.org/0000-0002-6955-7603Gaetano Paludetti8Claudio Grassi9https://orcid.org/0000-0001-7253-1685Fondazione Policlinico Universitario A. Gemelli IRCCS, Rome, Italy; Department of Neuroscience, Università Cattolica del Sacro Cuore, Rome, ItalyDepartment of Neuroscience, Università Cattolica del Sacro Cuore, Rome, ItalyDepartment of Neuroscience, Università Cattolica del Sacro Cuore, Rome, ItalyDepartment of Neuroscience, Università Cattolica del Sacro Cuore, Rome, ItalyDepartment of Neuroscience, Università Cattolica del Sacro Cuore, Rome, ItalyDepartment of Otolaryngology Head and Neck Surgery, Università Cattolica del Sacro Cuore, Rome, ItalyFondazione Policlinico Universitario A. Gemelli IRCCS, Rome, Italy; Department of Neuroscience, Università Cattolica del Sacro Cuore, Rome, ItalyFondazione Policlinico Universitario A. Gemelli IRCCS, Rome, Italy; Department of Otolaryngology Head and Neck Surgery, Università Cattolica del Sacro Cuore, Rome, ItalyFondazione Policlinico Universitario A. Gemelli IRCCS, Rome, Italy; Department of Otolaryngology Head and Neck Surgery, Università Cattolica del Sacro Cuore, Rome, ItalyFondazione Policlinico Universitario A. Gemelli IRCCS, Rome, Italy; Department of Neuroscience, Università Cattolica del Sacro Cuore, Rome, ItalyAlthough association between hearing impairment and dementia has been widely documented by epidemiological studies, the role of auditory sensory deprivation in cognitive decline remains to be fully understood. To address this issue we investigated the impact of hearing loss on the onset and time-course of cognitive decline in an animal model of Alzheimer’s disease (AD), that is the 3×Tg-AD mice and the underlying mechanisms. We found that hearing loss induced by noise exposure in the 3×Tg-AD mice before the phenotype is manifested caused persistent synaptic and morphological alterations in the auditory cortex. This was associated with earlier hippocampal dysfunction, increased tau phosphorylation, neuroinflammation, and redox imbalance, along with anticipated memory deficits compared to the expected time-course of the neurodegenerative phenotype. Our data suggest that a mouse model of AD is more vulnerable to central damage induced by hearing loss and shows reduced ability to counteract noise-induced detrimental effects, which accelerates the neurodegenerative disease onset.https://elifesciences.org/articles/70908hearing lossdementiaoxidative stresstau phosphorylationneuroinflammation
spellingShingle Fabiola Paciello
Marco Rinaudo
Valentina Longo
Sara Cocco
Giulia Conforto
Anna Pisani
Maria Vittoria Podda
Anna Rita Fetoni
Gaetano Paludetti
Claudio Grassi
Auditory sensory deprivation induced by noise exposure exacerbates cognitive decline in a mouse model of Alzheimer’s disease
eLife
hearing loss
dementia
oxidative stress
tau phosphorylation
neuroinflammation
title Auditory sensory deprivation induced by noise exposure exacerbates cognitive decline in a mouse model of Alzheimer’s disease
title_full Auditory sensory deprivation induced by noise exposure exacerbates cognitive decline in a mouse model of Alzheimer’s disease
title_fullStr Auditory sensory deprivation induced by noise exposure exacerbates cognitive decline in a mouse model of Alzheimer’s disease
title_full_unstemmed Auditory sensory deprivation induced by noise exposure exacerbates cognitive decline in a mouse model of Alzheimer’s disease
title_short Auditory sensory deprivation induced by noise exposure exacerbates cognitive decline in a mouse model of Alzheimer’s disease
title_sort auditory sensory deprivation induced by noise exposure exacerbates cognitive decline in a mouse model of alzheimer s disease
topic hearing loss
dementia
oxidative stress
tau phosphorylation
neuroinflammation
url https://elifesciences.org/articles/70908
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