Elsevier

Hearing Research

Volume 148, Issues 1–2, October 2000, Pages 213-219
Hearing Research

Sound conditioning reduces noise-induced permanent threshold shift in mice

https://doi.org/10.1016/S0378-5955(00)00161-1Get rights and content

Abstract

The phenomenon of conditioning-related protection, whereby prior exposure to moderate-level, non-traumatic, sound protects the ear from subsequent traumatic exposure, has been documented in a number of mammalian species. To probe the molecular mechanisms underlying this effect, the mouse would be a useful model; however, a previous study reported no conditioning effects in this species (Fowler et al., 1995). In our study, mice (CBA/CaJ) were exposed to a traumatic octave-band noise (8–16 kHz at 100 dB SPL for 2 h) with, or without, prior exposure to a sound-conditioning protocol consisting of exposure to the same noise band at lower sound pressure levels. Two conditioning protocols were investigated: one (81 dB SPL for 1 week) was analogous to those used in other conditioning studies in mammals; the second was significantly shorter (89 dB SPL for 15 min). Noise-induced permanent threshold shift (PTS) was assessed in a terminal experiment, after the traumatic exposure, via compound action potentials. Neither conditioning protocol elevated threshold, indeed both protocols increased amplitudes of distortion product otoacoustic emissions when animals were conditioned but not traumatized. Both conditioning exposures significantly reduced PTS from the subsequent traumatic exposure, compared to groups exposed without prior conditioning. Protective effects of 15-min conditioning were maximal when the condition–trauma interval was 24 h; protection disappeared when the traumatic exposure was presented 48 h after conditioning. These data are consistent with the view that protein synthesis is required for expression of the protective effect. The enhancement of distortion products in the condition-only state suggests that conditioning changes outer hair cell function.

Introduction

Sound conditioning by long-term exposure to moderate-level sound can reduce permanent threshold shifts (PTSs) from a subsequent traumatic exposure (Canlon et al., 1988, Canlon, 1996). This effect can be a robust one, in the sense that the PTS reduction in conditioned animals can be as large as 30–40 dB compared with control animals exposed to the traumatic noise without prior sound conditioning. The conditioning effect is also robust in the sense that it has been demonstrated in a number of different species, including guinea pig (Canlon et al., 1988, Kujawa and Liberman, 1997), rabbit (Canlon et al., 1991), chinchilla (Campo et al., 1991, Subramaniam et al., 1992), gerbils (Ryan et al., 1994) and rat (Pukkila et al., 1997). Furthermore, these studies have utilized a wide variety of conditioning exposures coupled with a variety of traumatic exposures as well.

Although well studied phenomenologically, the mechanisms underlying this protective effect are poorly understood. Cutting either of the two efferent feedback pathways to the ear (the middle-ear muscle reflex or the olivocochlear efferent reflex) does not prevent conditioning-related protection (Ryan et al., 1994, Kujawa and Liberman, 1997, Zheng et al., 1997), thus the effect appears to arise from changes in the inner ear itself. The observation that unilateral conditioning does not protect both ears suggests that the mechanisms need not arise from systemic effects of the noise (Yamasoba et al., 1999). On the other hand, the recent demonstration that whole-animal heat shock also protects from subsequent acoustic injury (Yoshida and Liberman, 1999) suggests that systemic stress-induced changes in gene expression can also contribute to changes in cochlear susceptibility to noise trauma.

The best animal model in which to study the molecular basis for conditioning-related protection would be the mouse, given the relative completeness of the genomic description in this species and the availability of interesting mutant and transgenic strains in which to assess the effects of well-described changes in genetic makeup. There has been only one previous study of the conditioning effect in mice, and the results were negative (Fowler et al., 1995). In that study, a narrow-band noise at 4.5 kHz was used as a conditioning stimulus, with a variety of conditioning levels and duty cycles. From 6 h to 1 week after conditioning, CBA/Ca mice were exposed to the same noise band at traumatic levels (107–117 dB SPL for 24 h). None of the eight combinations of conditioning and trauma parameters showed any protective effects of prior exposures relative to control groups exposed to the trauma stimulus only.

In the present study, we re-investigated the question of whether conditioning-related protection is demonstrable in the CBA/CaJ mouse. There were a number of ways in which the present study differed from the previous attempt, including (1) using a noise band centered closer to the best-hearing range of the mouse (8–16 kHz) and (2) decreasing the duration of the conditioning exposure. Two different conditioning paradigms were attempted and both resulted in reduced PTS to a subsequent traumatic exposure. The traumatic noise exposure used is the same as that in two previous studies of acoustic injury in the mouse (Yoshida and Liberman, 1999, Yoshida et al., 2000). The degree of PTS in the unconditioned animals is moderate (roughly 35 dB), and this type of damage is not associated with significant hair cell loss. Rather it appears to be due to stereocilia damage (Yoshida and Liberman, 1999), as in many other animal models of moderate PTS (Saunders et al., 1985).

Section snippets

Experimental groups and experimental design

Experimental animals were male mice (CBA/CaJ: Jackson Laboratory, ME) weighing 23–29 g. All procedures were approved by the IACUC of the Massachusetts Eye and Ear Infirmary. The right ear of each mouse was evaluated at 10–12 weeks of age in a final test to evaluate cochlear function. Prior to final test, six groups of mice underwent different manipulations, as schematized in Fig. 1. Control mice had no noise exposure. Trauma only animals were exposed to a traumatic noise band 1 week before

Effects of conditioning on normal cochlear function

A fundamental aspect of our experiment is to design conditioning exposures which do not, by themselves, damage the ear. Thus, our approach has been to choose a stimulus bandwidth (8–16 kHz) and exposure duration (1 week or 15 min) and then find the maximum exposure level, for each duration, at which cochlear thresholds will not be elevated by the conditioning stimulus itself. To assess this, the present study includes a number of Condition only groups. These animals (as schematized in Fig. 1)

Comparison to previous sound conditioning studies

The present results show that two very different kinds of sound conditioning protocol, i.e. one of 1 week duration and another of 15 min duration, can result in reduction of noise-induced PTS from a subsequent high-level exposure. This result is qualitatively different from the only previous study in mouse of conditioning-related protection from acoustic injury (Fowler et al., 1995), which found that a variety of sound-conditioning protocols actually increased the PTS from a subsequent

Acknowledgments

This work was supported by a grant from the NIDCD: RO1 DC0188.

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