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Cross-species experiments reveal widespread cochlear neural damage in normal hearing.

ABSTRACT: Animal models suggest that cochlear afferent nerve endings may be more vulnerable than sensory hair cells to damage from acoustic overexposure and aging. Because neural degeneration without hair-cell loss cannot be detected in standard clinical audiometry, whether such damage occurs in humans is hotly debated. Here, we address this debate through co-ordinated experiments in at-risk humans and a wild-type chinchilla model. Cochlear neuropathy leads to large and sustained reductions of the wideband middle-ear muscle reflex in chinchillas. Analogously, human wideband reflex measures revealed distinct damage patterns in middle age, and in young individuals with histories of high acoustic exposure. Analysis of an independent large public dataset and additional measurements using clinical equipment corroborated the patterns revealed by our targeted cross-species experiments. Taken together, our results suggest that cochlear neural damage is widespread even in populations with clinically normal hearing.

SUBMITTER: Bharadwaj HM

PROVIDER: S-EPMC9307777 | biostudies-literature | 2022 Jul

REPOSITORIES: biostudies-literature

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Cross-species experiments reveal widespread cochlear neural damage in normal hearing.

Bharadwaj Hari M HM Hustedt-Mai Alexandra R AR Ginsberg Hannah M HM Dougherty Kelsey M KM Muthaiah Vijaya Prakash Krishnan VPK Hagedorn Anna A Simpson Jennifer M JM Heinz Michael G MG

Communications biology 20220722 1

Animal models suggest that cochlear afferent nerve endings may be more vulnerable than sensory hair cells to damage from acoustic overexposure and aging. Because neural degeneration without hair-cell loss cannot be detected in standard clinical audiometry, whether such damage occurs in humans is hotly debated. Here, we address this debate through co-ordinated experiments in at-risk humans and a wild-type chinchilla model. Cochlear neuropathy leads to large and sustained reductions of the wideban ...[more]

PMID: 35869142

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Project description:ObjectivesBinaural pitch fusion is the perceptual integration of stimuli that evoke different pitches between the ears into a single auditory image. Adults who use hearing aids (HAs) or cochlear implants (CIs) often experience abnormally broad binaural pitch fusion, such that sounds differing in pitch by as much as 3 to 4 octaves are fused across ears, leading to spectral averaging and speech perception interference. The main goal of this study was to measure binaural pitch fusion in children with different hearing device combinations and compare results across groups and with adults. A second goal was to examine the relationship of binaural pitch fusion to interaural pitch differences or pitch match range, a measure of sequential pitch discriminability.DesignBinaural pitch fusion was measured in children between the ages of 6.1 and 11.1 years with bilateral HAs (n = 9), bimodal CI (n = 10), bilateral CIs (n = 17), as well as normal-hearing (NH) children (n = 21). Depending on device combination, stimuli were pure tones or electric pulse trains delivered to individual electrodes. Fusion ranges were measured using simultaneous, dichotic presentation of reference and comparison stimuli in opposite ears, and varying the comparison stimulus to find the range that fused with the reference stimulus. Interaural pitch match functions were measured using sequential presentation of reference and comparison stimuli, and varying the comparison stimulus to find the pitch match center and range.ResultsChildren with bilateral HAs had significantly broader binaural pitch fusion than children with NH, bimodal CI, or bilateral CIs. Children with NH and bilateral HAs, but not children with bimodal or bilateral CIs, had significantly broader fusion than adults with the same hearing status and device configuration. In children with bilateral CIs, fusion range was correlated with several variables that were also correlated with each other: pure-tone average in the second implanted ear before CI, and duration of prior bilateral HA, bimodal CI, or bilateral CI experience. No relationship was observed between fusion range and pitch match differences or range.ConclusionsThe findings suggest that binaural pitch fusion is still developing in this age range and depends on hearing device combination but not on interaural pitch differences or discriminability.

Project description:PurposeThe breadth of binaural pitch fusion, the integration of sounds differing in frequency across the two ears, can limit the ability to segregate and understand speech in background noise. Binaural pitch fusion is one type of central auditory processing that may still be developing in the pre-adolescent age range. In addition, children with hearing loss potentially have different trajectories of development of central auditory processing compared to their normal-hearing (NH) peers, due to disruption of auditory input and/or abnormal stimulation from hearing devices. The goal of this study was to measure and compare binaural pitch fusion changes during development in children with NH versus hearing loss and different hearing device combinations. Interaural pitch discrimination abilities were also measured to control for pitch discrimination as a potential limiting factor for fusion that may also change during development.MethodsBaseline measurements of binaural pitch fusion and interaural pitch discrimination were conducted in a total of 62 (22 female) children with NH (n = 25), bilateral hearing aids (HA; n = 10, bimodal cochlear implants (CI; n = 9), and bilateral CIs (n = 18), with longitudinal follow-up for a subset of participants (18 NH, 9 HA, 8 bimodal CI, and 15 bilateral CI). Age at the start of testing ranged from 6 to 10 years old, with a goal of repeated measurements over 3-6 years. Binaural pitch fusion ranges were measured as the range of acoustic frequencies (electrodes) presented to one ear that was perceptually fused with a single reference frequency (electrode) presented simultaneously to the other ear. Similarly, interaural pitch discrimination was measured as the range of frequencies (electrodes) that could not be consistently ranked in pitch compared to a single reference frequency (electrode) under sequential presentation to opposite ears.ResultsChildren with NH and HAs initially had broad binaural pitch fusion ranges compared to adults. With increasing age, the binaural fusion range narrowed by 1-3 octaves for children with NH, bilateral HAs, and bimodal CIs, but not for children with bilateral CIs. Interaural pitch discrimination showed no changes with age, though differences in discrimination ability were seen across groups.ConclusionBinaural fusion sharpens significantly on the scale of octaves in the age range from 6 to 14 years. The lack of change in interaural pitch discrimination with increasing age rules out discrimination changes as an explanation for the binaural fusion range changes. The differences in the trajectory of binaural fusion changes across groups indicate the importance of hearing device combination for the development of binaural processing abilities in children with hearing loss, with implications for addressing challenges with speech perception in noise. Together, the results suggest that pruning of binaural connections is still occurring and likely guided by hearing experience during childhood development.

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Cross-species experiments reveal widespread cochlear neural damage in normal hearing.

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Cross-species experiments reveal widespread cochlear neural damage in normal hearing.

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