Increased listening effort and cochlear neural degeneration underlie speech-in-noise deficits in normal-hearing middle-aged adults

Middle age represents a critical period of accelerated brain changes and provides a window for early detection and intervention in age-related neurological decline. Hearing loss is a key early marker of such decline and is linked to numerous comorbidities in older adults. Yet, ~10% of middle-aged in...

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Main Authors: Maggie E Zink, Leslie Zhen, Jacie R McHaney, Jennifer Klara, Kimberly Yurasits, Victoria E Cancel, Olivia Flemm, Claire Mitchell, Jyotishka Datta, Bharath Chandresekaran, Aravindakshan Parthasarathy
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Language:English
Published: eLife Sciences Publications Ltd 2025-07-01
Series:eLife
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Online Access:https://elifesciences.org/articles/102823
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author Maggie E Zink
Leslie Zhen
Jacie R McHaney
Jennifer Klara
Kimberly Yurasits
Victoria E Cancel
Olivia Flemm
Claire Mitchell
Jyotishka Datta
Bharath Chandresekaran
Aravindakshan Parthasarathy
author_facet Maggie E Zink
Leslie Zhen
Jacie R McHaney
Jennifer Klara
Kimberly Yurasits
Victoria E Cancel
Olivia Flemm
Claire Mitchell
Jyotishka Datta
Bharath Chandresekaran
Aravindakshan Parthasarathy
author_sort Maggie E Zink
collection DOAJ
description Middle age represents a critical period of accelerated brain changes and provides a window for early detection and intervention in age-related neurological decline. Hearing loss is a key early marker of such decline and is linked to numerous comorbidities in older adults. Yet, ~10% of middle-aged individuals who report hearing difficulties show normal audiograms. Cochlear neural degeneration (CND) could contribute to these hidden hearing deficits, though its role remains unclear due to a lack of objective diagnostics and uncertainty regarding its perceptual outcomes. Here, we employed a cross-species design to examine neural and behavioral signatures of CND. We measured envelope following responses (EFRs) – neural ensemble responses to sound originating from the peripheral auditory pathway – in young and middle-aged adults with normal audiograms and compared these responses to young and middle-aged Mongolian gerbils, where CND was histologically confirmed. We observed near-identical changes in EFRs across species that were associated with CND. Behavioral assessments revealed age-related speech-in-noise deficits under challenging conditions, while pupil-indexed listening effort increased with age even when behavioral performance was matched. Together, these results demonstrate that CND contributes to speech perception difficulties and elevated listening effort in midlife, which may ultimately lead to listening fatigue and social withdrawal.
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spelling doaj-art-2dfc1e192279421eaa1abf930266d9cd2025-08-20T03:31:27ZengeLife Sciences Publications LtdeLife2050-084X2025-07-011310.7554/eLife.102823Increased listening effort and cochlear neural degeneration underlie speech-in-noise deficits in normal-hearing middle-aged adultsMaggie E Zink0https://orcid.org/0000-0003-2018-2772Leslie Zhen1Jacie R McHaney2Jennifer Klara3Kimberly Yurasits4Victoria E Cancel5Olivia Flemm6Claire Mitchell7Jyotishka Datta8Bharath Chandresekaran9Aravindakshan Parthasarathy10https://orcid.org/0000-0002-4573-8004Department of Communication Science and Disorders, School of Health and Rehabilitation Sciences, University of Pittsburgh, Pittsburgh, United StatesDepartment of Communication Science and Disorders, School of Health and Rehabilitation Sciences, University of Pittsburgh, Pittsburgh, United StatesDepartment of Communication Science and Disorders, School of Health and Rehabilitation Sciences, University of Pittsburgh, Pittsburgh, United StatesDepartment of Communication Science and Disorders, School of Health and Rehabilitation Sciences, University of Pittsburgh, Pittsburgh, United StatesDepartment of Communication Science and Disorders, School of Health and Rehabilitation Sciences, University of Pittsburgh, Pittsburgh, United StatesDepartment of Communication Science and Disorders, School of Health and Rehabilitation Sciences, University of Pittsburgh, Pittsburgh, United StatesDepartment of Communication Science and Disorders, School of Health and Rehabilitation Sciences, University of Pittsburgh, Pittsburgh, United StatesDepartment of Communication Science and Disorders, School of Health and Rehabilitation Sciences, University of Pittsburgh, Pittsburgh, United StatesDepartment of Statistics, Virginia Polytechnic Institute and State University, Blacksburg, United StatesDepartment of Communication Science and Disorders, School of Health and Rehabilitation Sciences, University of Pittsburgh, Pittsburgh, United StatesDepartment of Communication Science and Disorders, School of Health and Rehabilitation Sciences, University of Pittsburgh, Pittsburgh, United States; Department of Bioengineering, Swanson School of Engineering, University of Pittsburgh, Pittsburgh, United States; Department of Otolaryngology, School of Medicine, University of Pittsburgh, Pittsburgh, United StatesMiddle age represents a critical period of accelerated brain changes and provides a window for early detection and intervention in age-related neurological decline. Hearing loss is a key early marker of such decline and is linked to numerous comorbidities in older adults. Yet, ~10% of middle-aged individuals who report hearing difficulties show normal audiograms. Cochlear neural degeneration (CND) could contribute to these hidden hearing deficits, though its role remains unclear due to a lack of objective diagnostics and uncertainty regarding its perceptual outcomes. Here, we employed a cross-species design to examine neural and behavioral signatures of CND. We measured envelope following responses (EFRs) – neural ensemble responses to sound originating from the peripheral auditory pathway – in young and middle-aged adults with normal audiograms and compared these responses to young and middle-aged Mongolian gerbils, where CND was histologically confirmed. We observed near-identical changes in EFRs across species that were associated with CND. Behavioral assessments revealed age-related speech-in-noise deficits under challenging conditions, while pupil-indexed listening effort increased with age even when behavioral performance was matched. Together, these results demonstrate that CND contributes to speech perception difficulties and elevated listening effort in midlife, which may ultimately lead to listening fatigue and social withdrawal.https://elifesciences.org/articles/102823cochlear synaptopathylistening effortcross-speciesEFRshidden hearing lossMongolian gerbil
spellingShingle Maggie E Zink
Leslie Zhen
Jacie R McHaney
Jennifer Klara
Kimberly Yurasits
Victoria E Cancel
Olivia Flemm
Claire Mitchell
Jyotishka Datta
Bharath Chandresekaran
Aravindakshan Parthasarathy
Increased listening effort and cochlear neural degeneration underlie speech-in-noise deficits in normal-hearing middle-aged adults
eLife
cochlear synaptopathy
listening effort
cross-species
EFRs
hidden hearing loss
Mongolian gerbil
title Increased listening effort and cochlear neural degeneration underlie speech-in-noise deficits in normal-hearing middle-aged adults
title_full Increased listening effort and cochlear neural degeneration underlie speech-in-noise deficits in normal-hearing middle-aged adults
title_fullStr Increased listening effort and cochlear neural degeneration underlie speech-in-noise deficits in normal-hearing middle-aged adults
title_full_unstemmed Increased listening effort and cochlear neural degeneration underlie speech-in-noise deficits in normal-hearing middle-aged adults
title_short Increased listening effort and cochlear neural degeneration underlie speech-in-noise deficits in normal-hearing middle-aged adults
title_sort increased listening effort and cochlear neural degeneration underlie speech in noise deficits in normal hearing middle aged adults
topic cochlear synaptopathy
listening effort
cross-species
EFRs
hidden hearing loss
Mongolian gerbil
url https://elifesciences.org/articles/102823
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