Elsevier

Hearing Research

Volume 136, Issues 1–2, October 1999, Pages 151-158
Hearing Research

The continuing search for outer hair cell afferents in the guinea pig spiral ganglion

https://doi.org/10.1016/S0378-5955(99)00120-3Get rights and content

Abstract

Antidromic stimulation of the stump of the VIIIth nerve was combined with microelectrode recording in the spiral ganglion of the guinea pig cochlea in an attempt to identify a sub-population of neurons with long-latency antidromic action potentials that might correspond to the thin unmyelinated afferent neurons emanating from the outer hair cells. The techniques used were similar but not identical to those employed in an earlier study by Brown (1994). By far the largest population of cells contacted had short antidromic latencies (0.58±0.12 ms, 76 units) and also responded to acoustic stimulation. These were assumed to be type I afferents emanating from inner hair cells. Eight cells had antidromic latencies larger than 1 ms, all but one of which had a zero spontaneous rate. All eight of these longer-latency cells were unresponsive to acoustic stimulation despite the fact that short-latency neurons in the same cochleas showed robust responses to sound before and after they were contacted. Four of these longer-latency cells had their antidromic thresholds accurately measured and two had significantly higher thresholds to electrical stimulation (0.1 ms duration) than type I cells in the same animal while two had similar electrical thresholds. Attempts to trace the eight long-latency neurons to the outer hair cells using intracellular injection of horseradish peroxidase were unsuccessful. On the basis of present evidence, we cannot conclude definitively that the long-latency neurons found in the spiral ganglion belong to the outer hair cell afferent population.

Introduction

The physiological properties of primary afferent neurons emanating from the inner hair cells of the mammalian cochlea (type I afferents) have long been established by a series of studies combining microelectrode recording with single fiber intracellular labelling (see for example Liberman, 1982, Robertson, 1984, Tsuji and Liberman, 1997). On the other hand, the physiological properties of the much sparser afferent population coming from the outer hair cells (type II afferents) are unknown.

In an early study, Robertson (1984) reported intracellular labelling of a single type II afferent in the guinea pig spiral ganglion that was totally unresponsive to sound and had zero spontaneous activity. More recently, in an heroic landmark study, Brown (1994) used antidromic stimulation of the central processes of the primary afferents combined with a single cell recording in the spiral ganglion to identify a small population of slowly conducting neurons that he attributed to the fine unmyelinated type II afferents. Brown reported only one instance of a slowly conducting neuron that was also acoustically responsive.

We set out to repeat Brown’s basic experiment and to combine the physiological measurements with intracellular injection of horseradish peroxidase (HRP). Our results basically confirm Brown’s findings with some interesting variations, but leave the question of the physiological properties of the type II outer hair cell afferents unresolved.

Section snippets

Materials and methods

The experiments reported here were performed on 32 young pigmented guinea pigs (235–404 g) of either sex. All procedures conformed to the Guidelines of the National Health and Medical Research Council of Australia and were approved by an institutional Animal Experimentation Ethics Committee. Antidromic stimulation was achieved by aspiration of the lateral portion of the cerebellum and cochlear nucleus to expose the nerve root in the internal auditory meatus and direct placement of insulated

Results

The vast majority of neurons showed all the characteristics of type I afferents. They had a range of spontaneous firing rates (0–117 spikes/s) and responded to acoustic stimulation with increased discharge rates of a classical stochastic temporal character. Typical records of antidromically evoked action potentials for these type I neurons are shown in Fig. 2, Fig. 6, illustrating their short latency. A small number of these neurons was selected for filling with HRP. Fig. 3 shows examples of

Discussion

This study used techniques very similar to those of Brown (1994). The motivating hypothesis was that type II afferents emanating from the outer hair cells should have markedly slower antidromic action potential conduction velocities and higher thresholds to electrical stimulation than the thicker, myelinated type I afferents, because they have fine diameters and are unmyelinated (Spoendlin, 1972). We confirm Brown’s observation, albeit with a smaller sample, that there exists a small population

Acknowledgements

Supported by grants from the National Health and Medical Research Council, The Medical Health and Research Infrastructure Fund of the state of Western Australia and The University of Western Australia. The authors are indebted to G. Yates for unstinting help with computing, G. Nancarrow for assistance with computing and electronic hardware and G. Bennett for expert care of experimental animals.

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