The healthy auditory system enables communication in challenging situations with high levels of background noise. Yet, despite normal sensitivity to pure tones, many listeners complain about having difficulties in such situations. Recent animal studies demonstrated that noise overexposure that produces temporary threshold shifts can cause the loss of auditory nerve (AN) fiber synapses (i.e., cochlear synaptopathy, CS), which appears to predominantly affect medium- and low-spontaneous rate (SR) fibers. In the present study, envelope following response (EFR) magnitude-level functions were recorded in normal hearing (NH) threshold and mildly hearing-impaired (HI) listeners with thresholds elevated above 2 kHz. EFRs were elicited by sinusoidally amplitude modulated (SAM) tones presented in quiet with a carrier frequency of 2 kHz, modulated at 93 Hz, and modulation depths of 0.85 (deep) and 0.25 (shallow). While EFR magnitude-level functions for deeply modulated tones were similar for all listeners, EFR magnitudes for shallowly modulated tones were reduced at medium stimulation levels in some NH threshold listeners and saturated in all HI listeners for the whole level range. A phenomenological model of the AN was used to investigate the extent to which hair-cell dysfunction and/or CS could explain the trends observed in the EFR data. Hair-cell dysfunction alone, including postulated elevated hearing thresholds at extended high frequencies (EHF) beyond 8 kHz, could not account for the recorded EFR data. Postulated CS led to simulations generally consistent with the recorded data, but a loss of all types of AN fibers was required within the model framework. The effects of off-frequency contributions (i.e., away from the characteristic place of the stimulus) and the differential loss of different AN fiber types on EFR magnitude-level functions were analyzed. When using SAM tones in quiet as the stimulus, model simulations suggested that (1) EFRs are dominated by the activity of high-SR fibers at all stimulus intensities, and (2) EFRs at medium-to-high stimulus levels are dominated by off-frequency contributions. Electronic supplementary material The online version of this article (10.1007/s10162-019-00721-7) contains supplementary material, which is available to authorized users.
Individual estimates of cochlear compression may provide complementary information to traditional audiometric hearing thresholds in disentangling different types of peripheral cochlear damage. Here we investigated the use of the slope of envelope following response (EFR) magnitude-level functions obtained from four simultaneously presented amplitude modulated tones with modulation frequencies of 80–100 Hz as a proxy of peripheral level compression. Compression estimates in individual normal hearing (NH) listeners were consistent with previously reported group-averaged compression estimates based on psychoacoustical and distortion-product oto-acoustic emission (DPOAE) measures in human listeners. They were also similar to basilar membrane (BM) compression values measured invasively in non-human mammals. EFR-based compression estimates in hearing-impaired listeners were less compressive than those for the NH listeners, consistent with a reduction of BM compression. Cochlear compression was also estimated using DPOAEs in the same NH listeners. DPOAE estimates were larger (less compressive) than EFRs estimates, showing no correlation. Despite the numerical concordance between EFR-based compression estimates and group-averaged estimates from other methods, simulations using an auditory nerve (AN) model revealed that compression estimates based on EFRs might be highly influenced by contributions from off-characteristic frequency (CF) neural populations. This compromises the possibility to estimate on-CF (i.e., frequency-specific or “local”) peripheral level compression with EFRs.
The ability to compress the large level range of incoming sounds into a smaller range of vibration amplitudes on the basilar membrane (BM) is an important property of the healthy auditory system. Sensorineural hearing impairment typically leads to a decrease in sensitivity to sound and a reduction of the amount of compression observed in BM input-output functions. While sensitivity loss can be measured efficiently via audiometry, no measure has yet been provided that represents fast and reliable compression estimates in the individual listener. In the present study, magnitude-level functions obtained from envelope following responses (EFR) to four simultaneously presented amplitude modulated tones were measured in normal-hearing (NH) and sensorineural hearing-impaired (HI) listeners. The slope of part of the EFR magnitude-level function was used to estimate level compression. The median values of the compression estimates in the group of NH listeners were found to be consistent with previously reported group-averaged compression estimates based on psychoacoustical measures and group-averaged distortion-product otoacoustic emission magnitude-level functions in human listeners, and similar to BM compression values measured invasively in non-human mammals. The EFR magnitude-level functions for the HI listeners were less compressive than those for the NH listeners, consistent with a reduction of BM compression in HI listeners. A computer model of the auditory nerve (AN) was used to simulate EFR magnitude-level functions at the level of the AN. The recorded EFRs at the chosen amplitude modulation rates (81-98 Hz) were considered to represent neural activity originating from the auditory brainstem and midbrain rather than a direct measure of AN activity. Nonetheless, the AN model simulations could account for the main trends observed in the recorded data. The model simulations suggested that the growth of the EFR magnitude-level function is highly influenced by contributions from off-frequency neural populations, which compromises the possibility to estimate local (i.e., frequency specific) compression with EFRs. Furthermore, the model showed that while the slope of the EFR magnitude-level function is sensitive to the loss of compression observed in HI listeners due to outer hair cell dysfunction, it is also sensitive to inner hair cell dysfunction. Overall, it is concluded that EFR magnitude-level functions do not represent frequency specific level compression in the auditory system.
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