Literature DB >> 33177067

Normal Tone-In-Noise Sensitivity in Trained Budgerigars despite Substantial Auditory-Nerve Injury: No Evidence of Hidden Hearing Loss.

Kenneth S Henry1,2,3, Kristina S Abrams3.   

Abstract

Loss of auditory-nerve (AN) afferent cochlear innervation is a prevalent human condition that does not affect audiometric thresholds and therefore remains largely undetectable with standard clinical tests. AN loss is widely expected to cause hearing difficulties in noise, known as "hidden hearing loss," but support for this hypothesis is controversial. Here, we used operant conditioning procedures to examine the perceptual impact of AN loss on behavioral tone-in-noise (TIN) sensitivity in the budgerigar (Melopsittacus undulatus; of either sex), an avian animal model with complex hearing abilities similar to humans. Bilateral kainic acid (KA) infusions depressed compound AN responses by 40-70% without impacting otoacoustic emissions or behavioral tone sensitivity in quiet. Surprisingly, animals with AN damage showed normal thresholds for tone detection in noise (0.1 ± 1.0 dB compared to control animals; mean difference ± SE), even under a challenging roving-level condition with random stimulus variation across trials. Furthermore, decision-variable correlations (DVCs) showed no difference for AN-damaged animals in their use of energy and envelope cues to perform the task. These results show that AN damage has less impact on TIN detection than generally expected, even under a difficult roving-level condition known to impact TIN detection in individuals with sensorineural hearing loss (SNHL). Perceptual deficits could emerge for different perceptual tasks or with greater AN loss but are potentially minor compared with those caused by SNHL.SIGNIFICANCE STATEMENT Loss of auditory-nerve (AN) cochlear innervation is a common problem in humans that does not affect audiometric thresholds on a clinical hearing test. AN loss is widely expected to cause hearing problems in noise, known as "hidden hearing loss," but existing studies are controversial. Here, using an avian animal model with complex hearing abilities similar to humans, we examined for the first time the impact of an experimentally induced AN lesion on behavioral tone sensitivity in noise. Surprisingly, AN-lesioned animals showed no difference in hearing performance in noise or detection strategy compared with controls. These results show that perceptual deficits from AN damage are smaller than generally expected, and potentially minor compared with those caused by sensorineural hearing loss (SNHL).
Copyright © 2021 the authors.

Entities:  

Keywords:  cochlear synaptopathy; decision-variable correlation; hidden hearing loss; operant conditioning; sensorineural hearing loss

Mesh:

Substances:

Year:  2020        PMID: 33177067      PMCID: PMC7786208          DOI: 10.1523/JNEUROSCI.2104-20.2020

Source DB:  PubMed          Journal:  J Neurosci        ISSN: 0270-6474            Impact factor:   6.167


  68 in total

1.  Hearing in the parakeet (Melopsittacus undulatus): absolute thresholds, critical ratios, frequency difference limens, and vocalizations.

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Journal:  J Comp Physiol Psychol       Date:  1975-01

2.  The detectability of a tone added to narrow bands of equal-energy noise.

Authors:  V M Richards
Journal:  J Acoust Soc Am       Date:  1992-06       Impact factor: 1.840

3.  Binaural detection with narrowband and wideband reproducible noise maskers. III. Monaural and diotic detection and model results.

Authors:  Sean A Davidson; Robert H Gilkey; H Steven Colburn; Laurel H Carney
Journal:  J Acoust Soc Am       Date:  2006-04       Impact factor: 1.840

4.  Effects of selective inner hair cell loss on auditory nerve fiber threshold, tuning and spontaneous and driven discharge rate.

Authors:  J Wang; N L Powers; P Hofstetter; P Trautwein; D Ding; R Salvi
Journal:  Hear Res       Date:  1997-05       Impact factor: 3.208

5.  Constrained sampling experiments reveal principles of detection in natural scenes.

Authors:  Stephen Sebastian; Jared Abrams; Wilson S Geisler
Journal:  Proc Natl Acad Sci U S A       Date:  2017-06-26       Impact factor: 11.205

6.  Associations between speech recognition at high levels, the middle ear muscle reflex and noise exposure in individuals with normal audiograms.

Authors:  James Shehorn; Olaf Strelcyk; Pavel Zahorik
Journal:  Hear Res       Date:  2020-05-07       Impact factor: 3.208

7.  Factors inducing retrograde degeneration of the cochlear nerve.

Authors:  H Spoendlin
Journal:  Ann Otol Rhinol Laryngol Suppl       Date:  1984 Jul-Aug

8.  Detection thresholds for amplitude modulations of tones in budgerigar, rabbit, and human.

Authors:  Laurel H Carney; Angela D Ketterer; Kristina S Abrams; Douglas M Schwarz; Fabio Idrobo
Journal:  Adv Exp Med Biol       Date:  2013       Impact factor: 2.622

9.  Morphology of the basilar papilla of the budgerigar, Melopsittacus undulatus.

Authors:  Geoffrey A Manley; Gabriele Schwabedissen; Otto Gleich
Journal:  J Morphol       Date:  1993-11       Impact factor: 1.804

10.  Cochlear neuropathy and the coding of supra-threshold sound.

Authors:  Hari M Bharadwaj; Sarah Verhulst; Luke Shaheen; M Charles Liberman; Barbara G Shinn-Cunningham
Journal:  Front Syst Neurosci       Date:  2014-02-21
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  7 in total

Review 1.  Animal models of hidden hearing loss: Does auditory-nerve-fiber loss cause real-world listening difficulties?

Authors:  Kenneth S Henry
Journal:  Mol Cell Neurosci       Date:  2021-12-07       Impact factor: 4.314

2.  Neural signatures of auditory hypersensitivity following acoustic trauma.

Authors:  Matthew McGill; Ariel E Hight; Yurika L Watanabe; Aravindakshan Parthasarathy; Dongqin Cai; Kameron Clayton; Kenneth E Hancock; Anne Takesian; Sharon G Kujawa; Daniel B Polley
Journal:  Elife       Date:  2022-09-16       Impact factor: 8.713

3.  Auditory-nerve responses in mice with noise-induced cochlear synaptopathy.

Authors:  Kirupa Suthakar; M Charles Liberman
Journal:  J Neurophysiol       Date:  2021-11-17       Impact factor: 2.974

4.  Effects of Noise Exposure and Aging on Behavioral Tone Detection in Quiet and Noise by Mice.

Authors:  Kali Burke; Laurel A Screven; Anastasiya Kobrina; Payton E Charlton; Katrina Schrode; Dillan F Villavisanis; Micheal L Dent; Amanda M Lauer
Journal:  eNeuro       Date:  2022-06-10

Review 5.  Hearing in Complex Environments: Auditory Gain Control, Attention, and Hearing Loss.

Authors:  Benjamin D Auerbach; Howard J Gritton
Journal:  Front Neurosci       Date:  2022-02-10       Impact factor: 4.677

6.  Midbrain-Level Neural Correlates of Behavioral Tone-in-Noise Detection: Dependence on Energy and Envelope Cues.

Authors:  Yingxuan Wang; Kristina S Abrams; Laurel H Carney; Kenneth S Henry
Journal:  J Neurosci       Date:  2021-07-15       Impact factor: 6.167

7.  Cochlear neural degeneration disrupts hearing in background noise by increasing auditory cortex internal noise.

Authors:  Jennifer Resnik; Daniel B Polley
Journal:  Neuron       Date:  2021-02-08       Impact factor: 17.173

  7 in total

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