Supra-Threshold Hearing and Fluctuation Profiles: Implications for Sensorineural and Hidden Hearing Loss

Abstract

An important topic in contemporary auditory science is supra-threshold hearing. Difficulty hearing at conversational speech levels in background noise has long been recognized as a problem of sensorineural hearing loss, including that associated with aging (presbyacusis). Such difficulty in listeners with normal thresholds has received more attention recently, especially associated with descriptions of synaptopathy, the loss of auditory nerve (AN) fibers as a result of noise exposure or aging. Synaptopathy has been reported to cause a disproportionate loss of low- and medium-spontaneous rate (L/MSR) AN fibers. Several studies of synaptopathy have assumed that the wide dynamic ranges of L/MSR AN fiber rates are critical for coding supra-threshold sounds. First, this review will present data from the literature that argues against a direct role for average discharge rates of L/MSR AN fibers in coding sounds at moderate to high sound levels. Second, the encoding of sounds at supra-threshold levels is examined. A key assumption in many studies is that saturation of AN fiber discharge rates limits neural encoding, even though the majority of AN fibers, high-spontaneous rate (HSR) fibers, have saturated average rates at conversational sound levels. It is argued here that the cross-frequency profile of low-frequency neural fluctuation amplitudes, not average rates, encodes complex sounds. As described below, this fluctuation-profile coding mechanism benefits from both saturation of inner hair cell (IHC) transduction and average rate saturation associated with the IHC-AN synapse. Third, the role of the auditory efferent system, which receives inputs from L/MSR fibers, is revisited in the context of fluctuation-profile coding. The auditory efferent system is hypothesized to maintain and enhance neural fluctuation profiles. Lastly, central mechanisms sensitive to neural fluctuations are reviewed. Low-frequency fluctuations in AN responses are accentuated by cochlear nucleus neurons which, either directly or via other brainstem nuclei, relay fluctuation profiles to the inferior colliculus (IC). IC neurons are sensitive to the frequency and amplitude of low-frequency fluctuations and convert fluctuation profiles from the periphery into a phase-locked rate profile that is robust across a wide range of sound levels and in background noise. The descending projection from the midbrain (IC) to the efferent system completes a functional loop that, combined with inputs from the L/MSR pathway, is hypothesized to maintain "sharp" supra-threshold hearing, reminiscent of visual mechanisms that regulate optical accommodation. Examples from speech coding and detection in noise are reviewed. Implications for the effects of synaptopathy on control mechanisms hypothesized to influence supra-threshold hearing are discussed. This framework for understanding neural coding and control mechanisms for supra-threshold hearing suggests strategies for the design of novel hearing aid signal-processing and electrical stimulation patterns for cochlear implants.

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