Estimated cochlear neural degeneration is associated with loudness hypersensitivity in individuals with normal audiograms

Jahn, Kelly N.; Hancock, Kenneth E.; Maison, Stéphane F.; Polley, Daniel B.

doi:10.1121/10.0011694

Cited by 6 publications

(2 citation statements)

References 34 publications

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“…The additional loss of auditory nerve afferent synapses onto IHCs ( Figure 1D ) would not be expected to affect hearing thresholds, but could have other influences on sound perception ( Chambers et al, 2016a ; Henry and Abrams, 2021 ; Lobarinas et al, 2013 ; Resnik and Polley, 2021 ). For example, we recently reported that human subjects with normal hearing thresholds but asymmetric degeneration of the left and right auditory nerve perceive tones of fixed physical intensity as louder in the ear with poor auditory nerve integrity, particularly for low intensities near sensation level ( Jahn et al, 2022 ). To determine whether mice may be showing evidence of auditory hypersensitivity, we performed a closer inspection of the mouse psychometric detection functions for the spared 8 kHz tone.…”

Section: Resultsmentioning

confidence: 99%

Neural signatures of auditory hypersensitivity following acoustic trauma

McGill

Hight

Watanabe

et al. 2022

eLife

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Neurons in sensory cortex exhibit a remarkable capacity to maintain stable firing rates despite large fluctuations in afferent activity levels. However, sudden peripheral deafferentation in adulthood can trigger an excessive, non-homeostatic cortical compensatory response that may underlie perceptual disorders including sensory hypersensitivity, phantom limb pain, and tinnitus. Here, we show that mice with noise-induced damage of the high-frequency cochlear base were behaviorally hypersensitive to spared mid-frequency tones and to direct optogenetic stimulation of auditory thalamocortical neurons. Chronic two-photon calcium imaging from ACtx pyramidal neurons (PyrNs) revealed an initial stage of spatially diffuse hyperactivity, hyper-correlation, and auditory hyperresponsivity that consolidated around deafferented map regions three or more days after acoustic trauma. Deafferented PyrN ensembles also displayed hypersensitive decoding of spared mid-frequency tones that mirrored behavioral hypersensitivity, suggesting that non-homeostatic regulation of cortical sound intensity coding following sensorineural loss may be an underlying source of auditory hypersensitivity. Excess cortical response gain after acoustic trauma was expressed heterogeneously among individual PyrNs, yet 40% of this variability could be accounted for by each cell’s baseline response properties prior to acoustic trauma. PyrNs with initially high spontaneous activity and gradual monotonic intensity growth functions were more likely to exhibit non-homeostatic excess gain after acoustic trauma. This suggests that while cortical gain changes are triggered by reduced bottom-up afferent input, their subsequent stabilization is also shaped by their local circuit milieu, where indicators of reduced inhibition can presage pathological hyperactivity following sensorineural hearing loss.

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Section: Resultsmentioning

confidence: 99%

Neural signatures of auditory hypersensitivity following acoustic trauma

McGill

Hight

Watanabe

et al. 2022

eLife

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“…We entered the following search terms in Pubmed and found only a single human study of the relationship between physiological indicators of deafferentation and hyperacusis: “hyperacusis synaptopathy,” “hyperacusis hidden hearing loss,” “hyperacusis deafferentation,” and “hyperacusis neural degeneration.” In a small sample of 12 adults with clinically normal hearing and an asymmetric summating potential (SP)/action potential (AP) ratio (a proposed indicator of cochlear deafferentation), Jahn et al (2022) evaluated loudness growth perception in both ears. They found that, on average, the ear with greater estimated cochlear deafferentation (larger SP/AP ratio) showed elevated loudness perception when compared with the contralateral ear of the same participant.…”

Section: Perceptual Consequences Of Cochlear Deafferentation In Human...mentioning

confidence: 99%

Perceptual Consequences of Cochlear Deafferentation in Humans

Bramhall,

McMillan

2024

Trends in Hearing

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Cochlear synaptopathy, a form of cochlear deafferentation, has been demonstrated in a number of animal species, including non-human primates. Both age and noise exposure contribute to synaptopathy in animal models, indicating that it may be a common type of auditory dysfunction in humans. Temporal bone and auditory physiological data suggest that age and occupational/military noise exposure also lead to synaptopathy in humans. The predicted perceptual consequences of synaptopathy include tinnitus, hyperacusis, and difficulty with speech-in-noise perception. However, confirming the perceptual impacts of this form of cochlear deafferentation presents a particular challenge because synaptopathy can only be confirmed through post-mortem temporal bone analysis and auditory perception is difficult to evaluate in animals. Animal data suggest that deafferentation leads to increased central gain, signs of tinnitus and abnormal loudness perception, and deficits in temporal processing and signal-in-noise detection. If equivalent changes occur in humans following deafferentation, this would be expected to increase the likelihood of developing tinnitus, hyperacusis, and difficulty with speech-in-noise perception. Physiological data from humans is consistent with the hypothesis that deafferentation is associated with increased central gain and a greater likelihood of tinnitus perception, while human data on the relationship between deafferentation and hyperacusis is extremely limited. Many human studies have investigated the relationship between physiological correlates of deafferentation and difficulty with speech-in-noise perception, with mixed findings. A non-linear relationship between deafferentation and speech perception may have contributed to the mixed results. When differences in sample characteristics and study measurements are considered, the findings may be more consistent.

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Asymmetric hearing thresholds are associated with hyperacusis in a large clinical population

Jahn

Polley

2023

Hearing Research

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Estimated cochlear neural degeneration is associated with loudness hypersensitivity in individuals with normal audiograms

Cited by 6 publications

References 34 publications

Neural signatures of auditory hypersensitivity following acoustic trauma

Neural signatures of auditory hypersensitivity following acoustic trauma

Perceptual Consequences of Cochlear Deafferentation in Humans

Asymmetric hearing thresholds are associated with hyperacusis in a large clinical population

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