Impact of Electrode Position on the Dynamic Range of a Human Auditory Nerve Fiber

Electrodes of a cochlear implant generate spikes in auditory nerve fibers. While the insertion depth of each of the electrodes is linked to a frequency section of the acoustic signal, the amplitude of the stimulating pulses controls the loudness of the related frequency band. The firing efficiency of an auditory nerve fiber, stimulated by a train of pulses varies between 0 and 100%. 100% firing efficiency means every pulse elicits a spike, 50% defines threshold. The dynamic range of an auditory nerve fiber is the range of stimulus intensities that causes a firing probability between 10 and 90%. This ‘electrical’ dynamic range is quite small in comparison to the variation of spiking rates measured during acoustic stimulation. Consequently, an increased dynamic range may improve the quality of auditory perception for cochlear implant users. Electrodes are often placed as close as possible to the center axis of the cochlea. Analysis of simulated auditory nerve firing showed that this placement is disadvantageous for the dynamic range. Five times larger dynamic ranges are expected for electrodes close to the terminal of the dendrite or at mid-dendritic placement.

Cochlear nucleus small cells use olivocochlear collaterals to encode sounds in noise

Understanding speech, especially in noisy environments, is crucial to social interactions. Yet, as we age, speech processing can be disrupted by cochlear damage and the subsequent auditory nerve fiber degeneration. The most vulnerable-medium and high-threshold-auditory nerve fibers innervate various cell types in the cochlear nucleus, among which, the small cells are unique in receiving this input exclusively. Here, we characterize small cell firing characteristics, demonstrating superior temporal as well as intensity coding. We show that small-cell unique coding properties are facilitated by direct cholinergic input from the medial olivocochlear system. These results highlight the small cell-olivocochlear circuit as a key player in signal processing in noisy environments, which may be selectively degraded in aging or after noise insult.

Distorted tonotopy severely degrades neural representations of natural speech in noise following acoustic trauma

SUMMARYListeners with sensorineural hearing loss (SNHL) struggle to understand speech, especially in noise, despite audibility compensation. These real-world suprathreshold deficits are hypothesized to arise from degraded frequency tuning and reduced temporal-coding precision; however, peripheral neurophysiological studies testing these hypotheses have been largely limited to in-quiet artificial vowels. Here, we measured single auditory-nerve-fiber responses to a natural speech sentence in noise from anesthetized chinchillas with normal hearing (NH) or noise-induced hearing loss (NIHL). Our results demonstrate that temporal precision was not degraded, and broader tuning was not the major factor affecting peripheral coding of natural speech in noise. Rather, the loss of cochlear tonotopy, a hallmark of normal hearing, had the most significant effects (both on vowels and consonants). Because distorted tonotopy varies in degree across etiologies (e.g., noise exposure, age), these results have important implications for understanding and treating individual differences in speech perception for people suffering from SNHL.

Simple transformations capture auditory input to cortex

Sounds are processed by the ear and central auditory pathway. These processing steps are biologically complex, and many aspects of the transformation from sound waveforms to cortical response remain unclear. To understand this transformation, we combined models of the auditory periphery with various encoding models to predict auditory cortical responses to natural sounds. The cochlear models ranged from detailed biophysical simulations of the cochlea and auditory nerve to simple spectrogram-like approximations of the information processing in these structures. For three different stimulus sets, we tested the capacity of these models to predict the time course of single-unit neural responses recorded in ferret primary auditory cortex. We found that simple models based on a log-spaced spectrogram with approximately logarithmic compression perform similarly to the best-performing biophysically detailed models of the auditory periphery, and more consistently well over diverse natural and synthetic sounds. Furthermore, we demonstrated that including approximations of the three categories of auditory nerve fiber in these simple models can substantially improve prediction, particularly when combined with a network encoding model. Our findings imply that the properties of the auditory periphery and central pathway may together result in a simpler than expected functional transformation from ear to cortex. Thus, much of the detailed biological complexity seen in the auditory periphery does not appear to be important for understanding the cortical representation of sound.

Envelope Following Response Measurements in Young Veterans Are Consistent With Noise-Induced Cochlear Synaptopathy

Animal studies have demonstrated that noise exposure can lead to the loss of the synapses between the inner hair cells and their afferent auditory nerve fiber targets without impacting auditory thresholds. Although several non-invasive physiological measures appear to be sensitive to cochlear synaptopathy in animal models, including auditory brainstem response (ABR) wave I amplitude, the envelope following response (EFR), and the middle ear muscle reflex (MEMR), human studies of these measures in samples that are expected to vary in terms of the degree of noise-induced synaptopathy have resulted in mixed findings. One possible explanation for the differing results is that synaptopathy risk is lower for recreational noise exposure than for occupational or military noise exposure. The goal of this analysis was to determine if EFR magnitude and ABR wave I amplitude are reduced among young Veterans with a history of military noise exposure compared with non-Veteran controls with minimal noise exposure. EFRs and ABRs were obtained in a sample of young (19-35 years) Veterans and non-Veterans with normal audiograms and robust distortion product otoacoustic emissions (DPOAEs). Mean EFR magnitudes and ABR wave I amplitudes were reduced for Veterans compared with non-Veteran controls. These findings replicate previous ABR wave I amplitude results in young Veterans and are consistent with animal models of noise-induced cochlear synaptopathy.

Speech-in-noise intelligibility difficulties with age: the role of cochlear synaptopathy

Damage to auditory-nerve-fiber synapses (i.e. cochlear synaptopathy) degrades the neural coding of sound and is predicted to impair sound perception in noisy listening environments. However, establishing a causal relationship between synaptopathy and speech intelligibility is difficult because we have no direct access to synapse counts in humans. Hence, we rely on the quality of noninvasive auditory-evoked potential (AEP) markers developed in rodent studies of histologically-verified synaptopathy. However, there are a number of reasons which render the interpretation of these markers in humans difficult. To bridge this translational gap, we apply a multi-method approach to enable a meaningful interpretation of the relationship between the histopathology of sensorineural hearing loss (SNHL) and speech perception. We first selected a synaptopathy-sensitive AEP marker and verified its sensitivity (i) in an animal model using a Kainic-acid induced synaptopathy, and (ii), via auditory model simulations which connect the histopathology of SNHL to the source generators of AEPs. Secondly, we restricted the frequency content of the speech-material to ensure that both AEP and speech metrics targeted similar cochlear frequency regions and associated auditory coding mechanisms. Following this approach, we studied the relative contribution of AEP markers of synaptopathy and hearing sensitivity to speech recognition thresholds in 44 listeners (24 women) of different ages and SNHL profiles. Our analysis shows that synaptopathy plays an important role for speech intelligibility in noise, but that outer-hair-cell integrity predicts performance in the absence of noise. Our results corroborate conclusions from animal studies regarding the prevalence of age-related synaptopathy, and its occurrence before outer-hair-cell loss damage.Significance StatementTemporal-bone histology demonstrates that cochlear synaptopathy, i.e. damage to inner-hair-cell auditory-nerve fiber synapses, sets in before sensory cell damage and associated hearing threshold elevation. Clinical practice assesses hearing status on the basis of audiometric thresholds, and is hence overlooking a -likely prevalent-aspect of sensorineural hearing damage given that ageing, noise exposure or ototoxic drugs can cause synaptopathy. We present a multi-method approach to study the relationship between synaptopathy and speech intelligibility and address an important unresolved issue in hearing science, namely why speech-intelligibility-in-noise degrades as we age, even when hearing sensitivity remains normal. Our study outcomes have important implications for hearing diagnostics and treatment.

Evoked Potentials Reveal Noise Exposure–Related Central Auditory Changes Despite Normal Audiograms

Purpose Complaints of auditory perceptual deficits, such as tinnitus and difficulty understanding speech in background noise, among individuals with clinically normal audiograms present a perplexing problem for audiologists. One potential explanation for these “hidden” auditory deficits is loss of the synaptic connections between the inner hair cells and their afferent auditory nerve fiber targets, a condition that has been termed cochlear synaptopathy . In animal models, cochlear synaptopathy can occur due to aging or exposure to noise or ototoxic drugs and is associated with reduced auditory brainstem response (ABR) wave I amplitudes. Decreased ABR wave I amplitudes have been demonstrated among young military Veterans and non-Veterans with a history of firearm use, suggesting that humans may also experience noise-induced synaptopathy. However, the downstream consequences of synaptopathy are unclear. Method To investigate how noise-induced reductions in wave I amplitude impact the central auditory system, the ABR, the middle latency response (MLR), and the late latency response (LLR) were measured in 65 young Veterans and non-Veterans with normal audiograms. Results In response to a click stimulus, the MLR was weaker for Veterans compared to non-Veterans, but the LLR was not reduced. In addition, low ABR wave I amplitudes were associated with a reduced MLR, but with an increased LLR. Notably, Veterans reporting tinnitus showed the largest mean LLRs. Conclusions These findings indicate that decreased peripheral auditory input leads to compensatory gain in the central auditory system, even among individuals with normal audiograms, and may impact auditory perception. This pattern of reduced MLR, but not LLR, was observed among Veterans even after statistical adjustment for sex and distortion product otoacoustic emission differences, suggesting that synaptic loss plays a role in the observed central gain. Supplemental Material https://doi.org/10.23641/asha.11977854