‘Normal’ hearing thresholds and fundamental auditory grouping processes predict difficulties with speech-in-noise perception

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Abstract

Understanding speech when background noise is present is a critical everyday task that varies widely among people. A key challenge is to understand why some people struggle with speech-in-noise perception, despite having clinically normal hearing. Here, we developed new figure-ground tests that require participants to extract a coherent tone pattern from a stochastic background of tones. These tests dissociated variability in speech-in-noise perception related to mechanisms for detecting static (same-frequency) patterns and those for tracking patterns that change frequency over time. In addition, elevated hearing thresholds that are widely considered to be ‘normal’ explained significant variance in speech-in-noise perception, independent of figure-ground perception. Overall, our results demonstrate that successful speech-in-noise perception is related to audiometric thresholds, fundamental grouping of static acoustic patterns, and tracking of acoustic sources that change in frequency. Crucially, speech-in-noise deficits are better assessed by measuring central (grouping) processes alongside audiometric thresholds.

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Most cited references 43

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Age-related cochlear synaptopathy: an early-onset contributor to auditory functional decline.

Yevgeniya Sergeyenko, Kumud Lall, M. Liberman … (2013)

Aging listeners experience greater difficulty understanding speech in adverse listening conditions and exhibit degraded temporal resolution, even when audiometric thresholds are normal. When threshold evidence for peripheral involvement is lacking, central and cognitive factors are often cited as underlying performance declines. However, previous work has uncovered widespread loss of cochlear afferent synapses and progressive cochlear nerve degeneration in noise-exposed ears with recovered thresholds and no hair cell loss (Kujawa and Liberman 2009). Here, we characterize age-related cochlear synaptic and neural degeneration in CBA/CaJ mice never exposed to high-level noise. Cochlear hair cell and neuronal function was assessed via distortion product otoacoustic emissions and auditory brainstem responses, respectively. Immunostained cochlear whole mounts and plastic-embedded sections were studied by confocal and conventional light microscopy to quantify hair cells, cochlear neurons, and synaptic structures, i.e., presynaptic ribbons and postsynaptic glutamate receptors. Cochlear synaptic loss progresses from youth (4 weeks) to old age (144 weeks) and is seen throughout the cochlea long before age-related changes in thresholds or hair cell counts. Cochlear nerve loss parallels the synaptic loss, after a delay of several months. Key functional clues to the synaptopathy are available in the neural response; these can be accessed noninvasively, enhancing the possibilities for translation to human clinical characterization.

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Noise-induced cochlear neuropathy is selective for fibers with low spontaneous rates.

Adam C Furman, Sharon G Kujawa, M Charles Liberman (2013)

Acoustic overexposure can cause a permanent loss of auditory nerve fibers without destroying cochlear sensory cells, despite complete recovery of cochlear thresholds (Kujawa and Liberman 2009), as measured by gross neural potentials such as the auditory brainstem response (ABR). To address this nominal paradox, we recorded responses from single auditory nerve fibers in guinea pigs exposed to this type of neuropathic noise (4- to 8-kHz octave band at 106 dB SPL for 2 h). Two weeks postexposure, ABR thresholds had recovered to normal, while suprathreshold ABR amplitudes were reduced. Both thresholds and amplitudes of distortion-product otoacoustic emissions fully recovered, suggesting recovery of hair cell function. Loss of up to 30% of auditory-nerve synapses on inner hair cells was confirmed by confocal analysis of the cochlear sensory epithelium immunostained for pre- and postsynaptic markers. In single fiber recordings, at 2 wk postexposure, frequency tuning, dynamic range, postonset adaptation, first-spike latency and its variance, and other basic properties of auditory nerve response were all completely normal in the remaining fibers. The only physiological abnormality was a change in population statistics suggesting a selective loss of fibers with low- and medium-spontaneous rates. Selective loss of these high-threshold fibers would explain how ABR thresholds can recover despite such significant noise-induced neuropathy. A selective loss of high-threshold fibers may contribute to the problems of hearing in noisy environments that characterize the aging auditory system.

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Are individual differences in speech reception related to individual differences in cognitive ability? A survey of twenty experimental studies with normal and hearing-impaired adults.

Michael A Akeroyd (2008)

This paper summarizes twenty studies, published since 1989, that have measured experimentally the relationship between speech recognition in noise and some aspect of cognition, using statistical techniques such as correlation or factor analysis. The results demonstrate that there is a link, but it is secondary to the predictive effects of hearing loss, and it is somewhat mixed across study. No one cognitive test always gave a significant result, but measures of working memory (especially reading span) were mostly effective, whereas measures of general ability, such as IQ, were mostly ineffective. Some of the studies included aided listening, and two reported the benefits from aided listening: again mixed results were found, and in some circumstances cognition was a useful predictor of hearing-aid benefit.

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Author and article information

Contributors

Emma Holmes: emma.holmes@ucl.ac.uk

Journal

Journal ID (nlm-ta): Sci Rep

Journal ID (iso-abbrev): Sci Rep

Title: Scientific Reports

Publisher: Nature Publishing Group UK (London )

ISSN (Electronic): 2045-2322

Publication date (Electronic): 14 November 2019

Publication date PMC-release: 14 November 2019

Publication date Collection: 2019

Volume: 9

Electronic Location Identifier: 16771

Affiliations

[1 ]ISNI 0000 0004 0611 8165, GRID grid.450002.3, Wellcome Centre for Human Neuroimaging, UCL, ; London, UK

[2 ]ISNI 0000 0001 0462 7212, GRID grid.1006.7, Institute of Neuroscience, Newcastle University, ; Newcastle upon Tyne, UK

Article

Publisher ID: 53353

DOI: 10.1038/s41598-019-53353-5

PMC ID: 6856372

PubMed ID: 31728002

SO-VID: 9ca08b93-15ce-4971-81fa-b3e17f02966a

License:

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

History

Date received : 29 April 2019

Date accepted : 18 October 2019

Funding

Funded by: FundRef https://doi.org/10.13039/100004440, Wellcome Trust (Wellcome);

Award ID: WT091681MA

Award Recipient : Timothy D. Griffiths

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ScienceOpen disciplines: Uncategorized

Keywords: auditory system,human behaviour

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ScienceOpen disciplines: Uncategorized

Keywords: auditory system, human behaviour

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‘Normal’ hearing thresholds and fundamental auditory grouping processes predict difficulties with speech-in-noise perception

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Most cited references 43

Age-related cochlear synaptopathy: an early-onset contributor to auditory functional decline.

Noise-induced cochlear neuropathy is selective for fibers with low spontaneous rates.

Are individual differences in speech reception related to individual differences in cognitive ability? A survey of twenty experimental studies with normal and hearing-impaired adults.

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