Pre-exposure to Lower-Level Noise Mitigates Cochlear Synaptic Loss Induced by High-Level Noise.

Liqiang Fan,Hui Wang,Zhengnong Chen,Yazhi Xing,Chunyan Li,Jian Wang,Zhen Zhang,Shankai Yin

doi:10.3389/fnsys.2020.00025

Abstract

The auditory sensory organs appear to be less damaged by exposure to high-level noise that is presented after exposure to non-traumatizing low-level noise. This phenomenon is known as the toughening or conditioning effect. Functionally, it is manifested by a reduced threshold shift, and morphologically by a reduced hair cell loss. However, it remains unclear whether prior exposure to toughening noise can mitigate the synaptic loss induced by exposure to damaging noise. Since the cochlear afferent synapse between the inner hair cells and primary auditory neurons has been identified as a novel site involved in noise-induced cochlear damage, we were interested in assessing whether this synapse can be toughened. In the present study, the synaptic loss was induced by a damaging noise exposure (106 dB SPL) and compared across Guinea pigs who had and had not been previously exposed to a toughening noise (85 dB SPL). Results revealed that the toughening noise heavily reduced the synaptic loss observed 1 day after exposure to the damaging noise. Although it was significant, the protective effect of the toughening noise on permanent synaptic loss was much smaller. Compared with cases in the control group without noise exposure, coding deficits were seen in both toughened groups, as reflected in the compound action potential (CAP) by signals with amplitude modulation. In general, the pre-exposure to the toughening noise resulted in a significantly reduced synaptic loss by the high-level noise. However, this morphological protection was not accompanied by a robust functional benefit.

Highlights

The remaining six animals in each of the pre-exposed group and no pre-exposed group groups were tested with auditory brainstem response (ABR) and compound action potential (CAP) tests before being sacrificed for synapse counting at 3 weeks post-high-level noise exposure
Prior exposure to continuous noise at 85 dB SPL produced a toughening effect in Guinea pigs, reducing the synaptic loss incurred by exposure to high-level noise
Similar to our previous studies (Shi et al, 2013, 2015b; Song et al, 2016), exposure to a traumatizing noise at 106 dB SPL for 2 h produces a temporary synaptic loss of ∼50% in the untoughened group. This was heavily reduced in the toughened group to only 16.9% on average. It was much smaller than the change in temporary synaptic loss, the mitigation by the toughening noise on the permanent synaptic loss, which was observed 3 weeks after the exposure to the traumatizing noise, remained significant (Figure 3)

Summary

Introduction

This protective effect exerted by the low-level noise is termed a toughening, priming or conditioning effect This phenomenon is functionally demonstrated by a reduced threshold shift, and morphologically by reduced hair cell loss. Since the noise-induced synaptic damage, or synaptopathy, can be established by noise without causing hearing loss defined by a threshold shift per se, noise-induced hidden hearing loss has been used as an umbrella term to reflect the functional deficits at suprathreshold levels (Moser and Starr, 2016; Plack et al, 2016; Song et al, 2016; Kobel et al, 2017; Liberman and Kujawa, 2017; Liberman, 2017; Lobarinas et al, 2017; Chen et al, 2019a)

Methods

Results

Conclusion