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 ...

Applicability of subcortical EEG metrics of synaptopathy to older listeners with impaired audiograms

“…14 15 1) Reduced EFR amplitudes: 16 On the basis of animal-synaptopathy findings (Parthasarathy and Kujawa, 2018; Shaheen et al, 17 2015) and reduced temporal envelop encoding ability (Bharadwaj et al, 2014) we expect that 18 the EFR strength is reduced in the oHI group. Because biophysical EFR-model predictions 19 support the idea that OHC loss does not strongly influence the EFR metric (Verhulst et al, 20 2018a, 2018b, 2016), we predict that reduced EFR amplitudes in the oHI group predominantly 21 reflect their individual degree of synaptopathy. In line with this, individual differences in oHI- 22 EFRs should not relate to hearing threshold differences in this group.…”

“…Second, the ratio between the hair-cell- 17 generated summating potential (SP) and the cochlear-neuron generated action potential (AP or 18 ABR Wave I) was also suggested as a marker of synaptopathy in humans. It predicted the poorer 19 word-recognition-in-noise performance of participants with higher doses of self-reported noise 20 exposure . Further studies have related the ABR Wave-I amplitude to the 21 amount of life time noise exposure (Bramhall et al, 2017;Valderrama et al, 2018) and tinnitus 22 (Schaette and McAlpine, 2011) in accordance with noise-induced synaptopathy observations in 23 rodents (Furman et al, 2013;Kujawa and Liberman, 2009;Möhrle et al, 2016).…”

“…Research in mice has shown that an 17 overexposure to noise can lead to a loss of up to 50% of the synapses and cochlear nerve 18 terminals innervating the inner hair cells (IHC) while hearing thresholds are normal (Kujawa and 19 Liberman, 2009). Cochlear synaptopathy is hypothesised to be induced by glutamate 20 excitotoxicity in the post-synaptic terminals of IHCs and the consequences are swelling, bursting 21 and finally the withdrawal of the terminal dendrite (Liberman and Kujawa, 2017). Because each 22 neuron communicates only with one IHC per tonotopic location along the basilar membrane 23 (Stamataki et al, 2006), even a partial deafferentation leads to a loss of information in the chain 24 of information transfer that could eventually lead to neurodegeneration of the spiral ganglion 25 cells (SGC; Liberman and Kujawa, 2017).…”

“…Low-spontaneous rate (low-SR) fibres with high firing 26 thresholds are relatively more affected by noise exposure (Furman et al, 2013) or aging 27 (Schmiedt et al, 1996) than those with low thresholds and high-spontaneous firing rates (high- 28 SR fibres). Given its expression, synaptopathy is thought to degrade the robust encoding of 29 suprathreshold temporal envelopes (Bharadwaj et al, 2014; Parthasarathy and Kujawa, 2018; 30 Verhulst et al, 2018b), or results in the loss of spectral contrast important for speech-in-noise 1 decoding (Carney, 2018). 2 In animal studies, it is possible to study and relate histological findings of synaptopathy directly 3 to non-invasive subcortical electrophysiological measures such as the auditory brainstem 4 response (ABR) and the envelope following response (EFR).…”

“…17 Despite a range of positive findings, there is also a considerable body of research that did not 18 find links between sound perception and electrophysiological measures of synaptopathy. For 19 example, a study which investigated the relationship between noise exposure history, 20 suprathreshold functional hearing tests and the ABR Wave-I amplitude did not find any 21 significant relation between the metrics (Fulbright et al, 2017). Guest and colleagues (2017) 22 followed a similar approach and did not find any links between noise exposure history and the 23 ABR Wave-I amplitude, or EFR measures, in young adults with and without tinnitus.…”