The continuing search for outer hair cell afferents in the guinea pig spiral ganglion
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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2020, Current Opinion in PhysiologyCitation Excerpt :The strongest evidence for this is the similarity in the sensitivity and sharpness of the tuning curves of the type I afferents and the efferent fibres [67–69]. In contrast in vivo electrophysiological recordings from putative type II afferents, while equivocal, suggest that these auditory fibres are poorly responsive to sound [70,71]. The need for high sound levels to recruit type II afferents is underpinned by in vitro studies showing requirement for integrated synaptic drive from the majority of the many tens of OHCs innervated by individual type II fibres [61,72,73].
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2020, The Senses: A Comprehensive Reference: Volume 1-7, Second EditionRecent advances in the development and function of type II spiral ganglion neurons in the mammalian inner ear
2017, Seminars in Cell and Developmental BiologyCitation Excerpt :The authors suggested that these “ribbonless” contacts may be involved in cochlear long-term plasticity by converting into ribbon synapses after OHC damage. Historically, determining the physiological properties of type II SGNs has been difficult because of their scarcity compared to type I SGNs, and because it is difficult to record from their thin, unmyelinated fibers [67–69]. Some of the initial indications of differences of type II SGNs came from whole-cell patch clamp recordings of their cell bodies in cochlear slices, which showed a significant difference in membrane properties compared to type Is [70].
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2015, Hearing ResearchCitation Excerpt :However, glutamatergic inputs from OHCs have been shown to trigger occasional action potentials in type II SGNs (Weisz et al., 2009), and ultrastructural analyses show there are fewer vesicles associated with the OHC ribbons than with their IHC counterparts (Weisz et al., 2012). Accordingly, type II SGNs are thought to respond only to the loudest sounds (Brown, 1994; Robertson et al., 1999) after maximal stimulation of the multiple OHCs that are connected to a single fibre (Weisz et al., 2012). Ribbon synapses develop sequentially, in a sequence similar to that observed during the formation of conventional CNS synapses (Friedman et al., 2000).
Synaptic studies inform the functional diversity of cochlear afferents
2015, Hearing ResearchA non-canonical pathway from cochlea to brain signals tissue-damaging noise
2015, Current BiologyCitation Excerpt :Type-II fibers are poorly understood; however, several lines of evidence suggest that synaptic transmission is fundamentally different. Although recordings from neonatal type IIs show responses to OHC depolarization that are blocked by NBQX [23], mature type-II fibers show no response to non-noxious sound [24–26], they do not display AMPA-type glutamate receptors (GluR2/3) [8] or the glutamatergic postsynaptic marker PSD95 [27] in their terminals, and they do not show the dramatic swelling of postsynaptic terminals seen in type Is after either cochlear glutamate perfusion or acoustic overstimulation [28, 29]. After 120 dB noise, cochlear afferents may not be responding to neurotransmitter release, but rather to other signals released during cellular damage.