Noise-induced cochlear neuropathy is selective for fibers with low spontaneous rates

Abstract

Furman AC, Kujawa SG, Liberman MC. Noise-induced cochlear neuropathy is selective for fibers with low spontaneous rates. J Neurophysiol 110: 577-586, 2013. First published April 17, 2013 doi:10.1152/jn.00164.2013.-Acoustic overexposure can cause a permanent loss of auditory nerve fibers without destroying cochlear sensory cells, despite complete recovery of cochlear thresholds (Kujawa and Liberman 2009), as measured by gross neural potentials such as the auditory brainstem response (ABR). To address this nominal paradox, we recorded responses from single auditory nerve fibers in guinea pigs exposed to this type of neuropathic noise (4-to 8-kHz octave band at 106 dB SPL for 2 h). Two weeks postexposure, ABR thresholds had recovered to normal, while suprathreshold ABR amplitudes were reduced. Both thresholds and amplitudes of distortionproduct otoacoustic emissions fully recovered, suggesting recovery of hair cell function. Loss of up to 30% of auditory-nerve synapses on inner hair cells was confirmed by confocal analysis of the cochlear sensory epithelium immunostained for pre-and postsynaptic markers. In single fiber recordings, at 2 wk postexposure, frequency tuning, dynamic range, postonset adaptation, first-spike latency and its variance, and other basic properties of auditory nerve response were all completely normal in the remaining fibers. The only physiological abnormality was a change in population statistics suggesting a selective loss of fibers with low-and medium-spontaneous rates. Selective loss of these high-threshold fibers would explain how ABR thresholds can recover despite such significant noise-induced neuropathy. A selective loss of high-threshold fibers may contribute to the problems of hearing in noisy environments that characterize the aging auditory system. excitotoxicity; noise-induced hearing loss; auditory nerve AUDITORY NERVE (AN) fibers transmit signals from cochlear inner hair cells (IHCs) to their brainstem targets in the cochlear nucleus. Each AN fiber receives signals from a single IHC via a single ribbon synapse (Liberman 1980;Spoendlin 1969), but each hair cell is contacted by 10 -30 AN fibers depending on cochlear location and species (Bohne et al. 1982;Liberman et al. 1990;Stamataki et al. 2006). This multiple innervation is important in auditory processing, because the AN fibers contacting a single hair cell differ in spontaneous discharge rate (SR) and threshold to acoustic stimulation (Liberman 1978). The SR distribution recorded among AN fibers is fundamentally bimodal, and the low-SR (Ͻ20 sp/s) group has higher thresholds than the high-SR (Ͼ20 sp/s) group (Liberman 1978). In addition to increasing the dynamic range of the auditory periphery, the high-threshold, low-SR fibers are important for hearing in a noisy environment, by virtue of their resistance to masking by continuous background noise (Costalupes et al. 1984).Recent work in both mouse (Kujawa and Liberman 2009) and guinea pig (Lin et al. 2011) has shown that acoustic overexposures causing reversible threshold e...

Olivocochlear Innervation Maintains the Normal Modiolar-Pillar and Habenular-Cuticular Gradients in Cochlear Synaptic Morphology

“…1C), a major component of the presynaptic ribbon (Schmitz et al 2000). The same modiolarpillar ribbon-size gradient is clear in confocal projections from guinea pig (Furman et al 2013) and chinchilla cochleas (Liberman, unpublished). Although the actual size of an IHC ribbon, i.e., a tube~100-nm wide and 400-nm long (Liberman 1980a;Liberman et al 1990), is below the resolution of the light microscope, and thus greatly distorted by the point-spread function of the confocal imaging system, the relative ribbon sizes, as measured here, appear to reflect the underlying morphological differences observed by electron microscopy .…”

Selective Inner Hair Cell Dysfunction in Chinchillas Impairs Hearing-in-Noise in the Absence of Outer Hair Cell Loss

“…This reduction in tuning is believed to underlie poorer ability to resolve signals in noise. The effects of selective IHC loss/dysfunction, or afferent degeneration on hearing-in-noise, however, are less understood but have been speculated to play a significant role (Kujawa and Liberman 2009;Lin et al 2011;Furman et al 2013).…”

Detailed Analysis of High Frequency Auditory Brainstem Response in Patients with Tinnitus: A Preliminary Study

“…Additionally, compound action potential (CAP) measurements utilizing ipsilateral "masked" electrocochleography (ECochG) procedures would provide a thorough examination of the peripheral nerve. Each inner hair cell in the cochlea inherits multiple synaptic connections with each fiber constituting a specific spontaneous firing rate 30 . Intensity coding is determined by the spontaneous firing rates of a neural fiber and theoretically, different fibers can be masked during ECochG recordings to obtain fiber specific threshold recordings.…”

“…Further microscopy revealed an immediate decrease of synaptic ribbon counts and a delayed onset of reduced ganglion cell density (after 64 weeks) at these regions with intact outer hair cell components. This effect is localized to low and medium spontaneously active fibers (< 18 spikes/sec) [30][31][32] . There are multiple synaptic connections associated with each inner hair cell, each constituting a specific spontaneous firing rate thus resulting in different intensity thresholds (low and medium spontaneously active fibers are reserved for detecting loud and medium level sound inputs respectively, whereas high spontaneous fibers dictate perception of soft inputs).…”