The association between subcortical and cortical fMRI and lifetime noise exposure in listeners with normal hearing thresholds

Rebecca S Dewey,Susan T Francis,Hannah Guest,Garreth Prendergast,Rebecca E Millman,Christopher J Plack,Deborah A Hall

doi:10.1016/j.neuroimage.2019.116239

Abstract

In animal models, exposure to high noise levels can cause permanent damage to hair-cell synapses (cochlear synaptopathy) for high-threshold auditory nerve fibers without affecting sensitivity to quiet sounds. This has been confirmed in several mammalian species, but the hypothesis that lifetime noise exposure affects auditory function in humans with normal audiometric thresholds remains unconfirmed and current evidence from human electrophysiology is contradictory. Here we report the auditory brainstem response (ABR), and both transient (stimulus onset and offset) and sustained functional magnetic resonance imaging (fMRI) responses throughout the human central auditory pathway across lifetime noise exposure. Healthy young individuals aged 25–40 years were recruited into high (n = 32) and low (n = 30) lifetime noise exposure groups, stratified for age, and balanced for audiometric threshold up to 16 kHz fMRI demonstrated robust broadband noise-related activity throughout the auditory pathway (cochlear nucleus, superior olivary complex, nucleus of the lateral lemniscus, inferior colliculus, medial geniculate body and auditory cortex). fMRI responses in the auditory pathway to broadband noise onset were significantly enhanced in the high noise exposure group relative to the low exposure group, differences in sustained fMRI responses did not reach significance, and no significant group differences were found in the click-evoked ABR. Exploratory analyses found no significant relationships between the neural responses and self-reported tinnitus or reduced sound-level tolerance (symptoms associated with synaptopathy). In summary, although a small effect, these fMRI results suggest that lifetime noise exposure may be associated with central hyperactivity in young adults with normal hearing thresholds.

Highlights

Noise exposure is the main cause of preventable hearing loss (World Health Organization, 1997)
Our primary hypothesis, informed by (Gu et al, 2010) and as pre-registered in Dewey et al (2018a) was that higher lifetime noise exposure would lead to increased functional magnetic resonance imaging (fMRI) and auditory brainstem response (ABR) responses in central auditory regions compared to lower noise exposure, consistent with central gain enhancement (Gu et al, 2010; Gu et al, 2012; Auerbach et al, 2014) as a consequence of cochlear synaptopathy
A correlation analysis was run between the magnitude of the fMRI onset response in bilateral Nucleus of the Lateral Lemniscus (NLL) and wave V of the ABR, but this was not significant (Pearson’s r = 0.139; p = 0.280; n = 62). This is the first auditory fMRI evaluation of synaptopathy in humans, here we tested the hypothesis that higher lifetime noise exposure would lead to increased responses in central auditory regions compared to lower noise exposure. fMRI of the ascending auditory pathway was performed in 62 individuals with strictly 506 normal hearing thresholds (≤ 20 dB HL) from 500 Hz to 8 kHz, allocated to two groups of low and high noise 507 exposure who widely varied in their individual lifetime noise exposures (0 - 14 vs. 15 - 189 units)

Summary

Introduction

Noise exposure is the main cause of preventable hearing loss (World Health Organization, 1997). Animals exposed to high sound levels exhibit temporary threshold shifts, which may be 6 accompanied by permanent loss of synapses between inner hair cells and auditory nerve fibers and 7 permanent reduction of wave I of the electrophysiological auditory brainstem response (ABR) (Kujawa and 8 Liberman, 2009). This article reports the first investigation of cumulative lifetime noise exposure on ascending auditory pathway function in audiometrically normal adults, as measured by the sustained and transient fMRI response and associated ABR in the same participants. Our primary hypothesis, informed by (Gu et al, 2010) and as pre-registered in Dewey et al (2018a) was that higher lifetime noise exposure would lead to increased fMRI and ABR responses in central auditory regions compared to lower noise exposure, consistent with central gain enhancement (Gu et al, 2010; Gu et al, 2012; Auerbach et al, 2014) as a consequence of cochlear synaptopathy

Materials and Methods

67 Figure 1

Participant characteristics

Discussion

Conclusions