Neural adaptation at stimulus onset and speed of neural processing as critical contributors to speech comprehension independent of hearing threshold or age

Schirmer, J.; Wolpert, S.; Dapper, K.; Ruehle, M.; Wertz, J.; Wouters, M.; Eldh, T.; Bader, K.; Singer, W.; Gaudrain, E.; Baskent, D.; Verhulst, S.; Braun, C.; Ruettiger, L.; Munk, M. H. J.; Dalhoff, E.; Knipper, M.

doi:10.1101/2023.12.22.573060

bioRxiv · 10.1101/2023.12.22.573060

Neural adaptation at stimulus onset and speed of neural processing as critical contributors to speech comprehension independent of hearing threshold or age

Schirmer, J.·Wolpert, S.·Dapper, K.·Ruehle, M.·Wertz, J.·Wouters, M.·Eldh, T.·Bader, K.·Singer, W.·Gaudrain, E.·Baskent, D.·Verhulst, S.·Braun, C.·Ruettiger, L.·Munk, M. H. J.·Dalhoff, E.·Knipper, M.

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Abstract

Loss of afferent auditory fiber function (cochlear synaptopathy) has been suggested to occur before a clinically measurable deterioration of subjective hearing threshold. This so-called "hidden" hearing loss is characterized by speech comprehension difficulties. We examined young, middle-aged, and older individuals with and without hearing loss using pure-tone (PT) audiometry, short-pulsed distortion-product otoacoustic emissions (DPOAE), auditory brainstem responses (ABR), auditory steady state responses (ASSR), speech comprehension (OLSA), and syllable discrimination in quiet and noise. After normalizing OLSA thresholds for PT thresholds ("PNOT"), differences in speech comprehension still remained and showed no significant dependence on age, allowing us to categorize participants into groups with good, standard, and poor speech comprehension. Listeners with poor speech comprehension in quiet exhibited smaller firing rate adaptions at stimulus onset (as measured by the difference between DPOAE threshold and pure-tone threshold) and delayed supra-threshold ABR waves I-V, suggesting high spontaneous rate low threshold fiber cochlear synaptopathy. In contrast, when speech comprehension was tested in noise, listeners with poor speech comprehension had larger DPOAEs acceptance rate, putatively resulting from altered basilar membrane compression (recruitment). This was linked with higher uncomfortable loudness levels and larger ASSR amplitudes. Moreover, performance in phoneme discrimination was significantly different below (/o/-/u/) and above the phase-locking limit (/i/-/y/), depending on whether vowels were presented in quiet or ipsilateral noise. This suggests that neural firing rate adaptation at stimulus onset is critical for speech comprehension, independent of hearing threshold and age, whereas the recruitment phenomenon counterbalances the loss in speech-in-noise discrimination due to impaired threshold. Significance StatementAge-related hearing loss is the third largest modifiable risk factor for cognitive decline. It has been suggested that the link between hearing loss and cognitive decline is not fully explained by hearing threshold loss. We here suggest that language comprehension deficits may be used as an early indication of future hearing loss and therefore cognitive decline. We found that, independent of age and pure-tone thresholds, speech comprehension in quiet and ipsilateral noise depend on different onset firing-rate adaptations of inner hair cells (measured by DPOAE threshold), along with cochlear synaptopathy of high spontaneous rate auditory nerve fibers and neural spiking synchronicity. These measures may be used as possible future indicators of risk for cognitive decline.

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Schirmer, J., Wolpert, S., Dapper, K., Ruehle, M., Wertz, J., Wouters, M., Eldh, T., Bader, K., Singer, W., Gaudrain, E., Baskent, D., Verhulst, S., Braun, C., Ruettiger, L., Munk, M. H. J., Dalhoff, E., Knipper, M.. 2023-12-23. Neural adaptation at stimulus onset and speed of neural processing as critical contributors to speech comprehension independent of hearing threshold or age. https://doi.org/10.1101/2023.12.22.573060

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