Cochlear de-efferentation and impulse noise-induced acoustic trauma in the chinchilla

Abstract

The olivocochlear bundle (OCB) has been shown to protect the ear from acoustic trauma induced by continuous noise or tones. The present study examines the OCB’s role in the ear’s response to impulse noise (150 dB pSPL, 100 impulses, 50 s total exposure duration). Successful section of the OCB was achieved through a posterior parafloccular fossa approach for the right ears of six out of 15 adult chinchillas. The left ears from the same animals served as efferent-innervated controls. Measurements of inferior colliculus evoked potentials (ICPs) showed that the de-efferented ears incurred similar temporary and permanent threshold shifts as the control ears. Twenty days after noise exposure, depressed ICP amplitudes had virtually recovered to pre-values in the control ears whereas those in the de-efferented ears remained significantly depressed. Greater loss of inner hair cells was seen in the de-efferented ears than in the control ears. Both control and de-efferented ears incurred large loss of outer hair cells, with no statistically significant differences between groups. The current data are intriguing, yielding tentative evidence to suggest that inner hair cells of de-efferented ears are more susceptible to impulse noise than those in efferented control ears. In contrast, outer hair cell vulnerability to impulse noise appears to be unaffected by de-efferentation.

Introduction

The role of the olivocochlear bundle (OCB), a major component in the inner ear neuroanatomy, in protecting the ear from noise-induced hearing loss has been debated for years (Cody and Johnstone, 1982, Handrock and Zeisberg, 1982, Liberman, 1991, Liberman, 1992, Liberman and Gao, 1995, Rajan, 1988, Rajan, 1995a, Rajan, 1995b, Rajan and Johnstone, 1983, Trahiotis and Elliott, 1970, Yamasoba and Dolan, 1998, Zheng et al., 1997b, Zheng et al., 1997c). Previous studies (Cody and Johnstone, 1982, Rajan and Johnstone, 1983, Trahiotis and Elliott, 1970) showed that the OCB is important in protecting the ear against noise-induced temporary threshold shift (TTS). For example, Rajan et al. reported that the TTS induced by a brief intense pure tone (10 kHz at 103 dB SPL for 1 min) was reduced by acoustically stimulating the OCB (Rajan and Johnstone, 1983). Since then, there have been many reports (e.g., Patuzzi and Thompson, 1991, Rajan, 1988, Rajan, 1995a, Rajan, 1995b) that support a role of the OCB in attenuating noise-induced TTS.

Experiments on the role of the OCB in modulating noise-induced permanent threshold shift (PTS) have yielded mixed results. In one study (Handrock and Zeisberg, 1982), OCB lesion resulted in greater PTS in guinea pigs exposed to a 4 kHz octave band noise at 125 dB SPL, but not at 120 dB SPL. Recently, Yamasoba and Dolan (1998) reported that inactivation of the medial OCB through strychnine infusion into the cochlea potentiated PTS in guinea pigs exposed to broadband noise. Another study (Liberman and Gao, 1995) concluded that sound-evoked activity in the olivocochlear system does not play a major protective role in the auditory periphery, except perhaps for the extreme basal regions of the cochlea. From the same laboratory, however, Kujawa and Liberman (1997) reported that animals with lesion of the entire OCB developed greater PTS than controls or animals with partial lesions of the ‘crossed’ OCB. The results of Kujawa and Liberman (1997) are consistent with our results, which show greater PTS in chinchillas with complete lesions of the entire OCB (Zheng et al., 1997b, Zheng et al., 1997c). In one study (Zheng et al., 1997c), chinchillas were exposed to an octave band noise (4 kHz) at a low level (85 dB SPL) for 10 days (6 h/d) and then at a high level (95 dB SPL) for 48 h. In the chinchillas with completely de-efferented ears, there was substantially more TTS during low-level exposure, and greater PTS and outer hair cell (OHC) loss after high-level exposure. In a subsequent study (Zheng et al., 1997b) in which animals were exposed to a broadband noise at 105 dB SPL, the de-efferented ears sustained more PTS at all the measured frequencies (from 1.2 to 9.6 kHz), suggesting that the OCB is important in protecting the ear from continuous noise-induced PTS at low frequencies as well as high frequencies.

All previous studies on the OCB’s role in protecting ears from TTS and PTS used continuous noise or tones that metabolically distress the ear (Bobbin et al., 1976, Bohne, 1976, Gunther et al., 1989, Liberman and Mulroy, 1982, Salvi et al., 1982). Impulse noise presents a different challenge to the ear than continuous noise because it is punctate in time and can cause mechanical as well as metabolic damage (Hamernik and Henderson, 1974, Hamernik et al., 1987, Henderson and Hamernik, 1986, Slepecky et al., 1982). Impulse noise exposure may be a stressor whose effects can be modulated by the tonic influence of the OCB. The following experiment was designed to further examine the OCB’s effects on PTS by evaluating the influence of chronic cochlear de-efferentation on impulse noise-induced hearing loss.