Distorted Tonotopy Severely Degrades Neural Representations of Connected Speech in Noise following Acoustic Trauma

Abstract

Listeners 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 connected speech sentence in noise from anesthetized male chinchillas with normal hearing (NH) or noise-induced hearing loss (NIHL). Our results demonstrated that temporal precision was not degraded following acoustic trauma, and furthermore that sharpness of cochlear frequency tuning was not the major factor affecting impaired peripheral coding of connected speech in noise. Rather, the loss of cochlear tonotopy, a hallmark of NH, contributed the most to both consonant-coding and vowel-coding degradations. 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.

Cell-type-specific roles of inhibitory interneurons in the rehabilitation of auditory cortex after peripheral damage

“…Compensatory plasticity in the A1 after peripheral damage supports the recovery of the perceptual sound-detection threshold but does not support sound processing encoded by precise spike timing, such as modulated noise or speech and restricts hearing in a noisy environment 10,11,15,84,85 . Interestingly, A1 SOM neurons, which are critically important for sound processing encoded by precise spike timing of neuronal firing 43,44,86,87 , showed reduced sound-evoked activity after NIHL (Fig.…”

“…Compensatory plasticity in the A1 after peripheral damage supports the recovery of the perceptual sound-detection threshold but does not support sound processing encoded by precise spike timing, such as modulated noise or speech and restricts hearing in a noisy environment 10,11,15,84,85 .…”

Enhanced envelope coding following acoustic trauma is detrimental to neural coding of speech in noise

“…Local 10-dB quality factor or 𝑄𝑄 10 was estimated as the 10-dB bandwidth relative to the threshold at CF. For W-shaped FTCs, the narrowest 10-dB bandwidth near CF was considered for local 𝑄𝑄 10 , which is similar to psychoacoustic approaches for estimating tuning 27 and disentangles broadened bandwidth effects from distorted tonotopy 20 .…”

“…S1d). Alternatively, our recent studies show that disruption in cochlear tonotopy, the functional connectivity between sound frequency and cochlear place, which occurs following NIHL can play a key role in speech-in-noise coding 20–22 . To evaluate the relative contributions of these two factors (i.e., bandwidth and tonotopy), a toy model was created.…”

“…Because distorted tonotopy, the degree of which varies across hearing-loss etiologies 21 , is the dominant contributor to these degradations in speech-in-noise coding following NIHL, this understudied suprathreshold deficit likely contributes to individual differences in speech perception among listeners with sensorineural hearing loss. Further studies are warranted to establish the relation between speech perception and noninvasive assays of distorted tonotopy 22 , especially in real-world listening conditions since environmental noises have substantial low-frequency 108 energy, which can exacerbate the effects of distorted tonotopy 20,22 . 109…”