Abstract
Speech intelligibility declines with age and sensorineural hearing damage (SNHL). However, it remains unclear whether cochlear synaptopathy (CS), a recently discovered form of SNHL, significantly contributes to this issue. CS refers to damaged auditory-nerve synapses that innervate the inner hair cells and there is currently no go-to diagnostic test available. Furthermore, age-related hearing damage can comprise various aspects (e.g., hair cell damage, CS) that each can play a role in impaired sound perception. To explore the link between cochlear damage and speech intelligibility deficits, this study examines the role of CS for word recognition among older listeners. We first validated an envelope-following response (EFR) marker for CS using a Budgerigar model. We then applied this marker in human experiments, while restricting the speech material’s frequency content to ensure that both the EFR and the behavioral tasks engaged similar cochlear frequency regions. Following this approach, we identified the relative contribution of hearing sensitivity and CS to speech intelligibility in two age-matched (65-year-old) groups with clinically normal (n=15, 8 females) or impaired audiograms (n=13, 8 females). Compared to a young normal-hearing control group (n = 13, 7 females), the older groups demonstrated lower EFR responses and impaired speech reception thresholds. We conclude that age-related CS reduces supra-threshold temporal envelope coding with subsequent speech coding deficits in noise that cannot be explained based on hearing sensitivity alone.
Significance Statement Temporal bone histology reveals that cochlear synaptopathy (CS), characterized by damage to inner hair cell auditory nerve fiber synapses, precedes sensory cell damage and hearing sensitivity decline. Despite this, clinical practice primarily evaluates hearing status based on audiometric thresholds, potentially overlooking a prevalent aspect of sensorineural hearing damage due to aging, noise exposure, or ototoxic drugs—all of which can lead to CS. To address this gap, we employ a novel and sensitive EEG-based marker of CS to investigate its relationship with speech intelligibility. This study addresses a crucial unresolved issue in hearing science: whether CS significantly contributes to degraded speech intelligibility as individuals age. Our study-outcomes are pivotal for identifying the appropriate target for treatments aimed at improving impaired speech perception.
Footnotes
Ghent University owns a patent (US Patent App. 17/791,985) related to the RAM-EFR methods adopted in this paper. Sarah Verhulst and Viacheslav Vasilkov are inventors.
This work was supported by the DFG Cluster of Excellence EXC 1077/1 ”Hearing4all” (MG, MM, SV), the European Research Council (ERC) under the Horizon 2020 Research and Innovation Programme (grant agreement No 678120 RobSpear; VV, SV) and European Innovation Council (EIC Transition EarDiTech 101058278; SV), National Institutes of Health grant R01 DC017519 (KH) and a National Institutes of Health Predoctoral National Research Service Award Fellowship (TL1 TR002000) administered by the University of Rochester Clinical and Translational Science Institute (JW). The authors would like to thank the study participants as well as the Hörzentrum Oldenburg for helping with participant recruitment. Lastly, we thank Sarineh Keshishzadeh for help with the analysis scripts and data storage and labelling throughout the project and Attila Fráter for help with the reanalysis of the Encina-llamas data.
↵*These authors contributed equally to the work
This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
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