The spiral ganglion: Connecting the peripheral and central auditory systems

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Abstract

In mammals, the initial bridge between the physical world of sound and perception of that sound is established by neurons of the spiral ganglion. The cell bodies of these neurons give rise to peripheral processes that contact acoustic receptors in the organ of Corti, and the central processes collect together to form the auditory nerve that projects into the brain. In order to better understand hearing at this initial stage, we need to know the following about spiral ganglion neurons: (1) their cell biology including cytoplasmic, cytoskeletal, and membrane properties, (2) their peripheral and central connections including synaptic structure; (3) the nature of their neural signaling; and (4) their capacity for plasticity and rehabilitation. In this report, we will update the progress on these topics and indicate important issues still awaiting resolution.

Highlights

► The anatomy of the spiral ganglion neurons of the mammalian cochlea is reviewed. ► The cell biology, peripheral and central connections, structure of the synapse, and neurochemistry are discussed in detail, ► Important issues still awaiting resolution are indicated throughout.

Section snippets

Spiral ganglion

In the inner ear, a channel formed by a latticework of bone spirals around in parallel to the coiled labyrinth. This channel is called Rosenthal’s canal within which reside the somata of the spiral ganglion neurons. Each cell body emits a peripheral process that extends toward the organ of Corti and a central process that projects into the auditory nerve. Two populations of neurons have been described in the spiral ganglion (Fig. 1A). The classification has been made on the basis of somatic

Cytoskeletal properties of the spiral ganglion neurons

On the basis of cytoplasmic and cytoskeletal contents, the type I and II spiral ganglion neurons can be distinguished using different kinds of stains. Basic dyes stain nucleic acids (DNA and RNA), thereby imparting dye onto ribosomes and chromatin of all cells, including endothelial cells (that comprise blood vessels), smooth muscle cells (that encircle arterioles), Schwann cells that form myelin, and neurons. Although type I neurons will stain darker than the filamentous type II neurons, the

Type I neurons

One of the striking and consistent features of the type I neuron across species is the thin caliber of its peripheral process (Fig. 1, Fig. 5). This difference was mentioned in an ultrastructural study of the guinea pig spiral ganglion (Thomsen, 1966) and quantified as a ratio of central process diameter to peripheral process diameter for a variety of mammals, including cat, mouse, opossum, guinea pig, squirrel monkey, and human (Kiang et al., 1982, Kiang et al., 1984, Berglund and Ryugo, 1986

Central projections of the spiral ganglion to the cochlear nucleus

The central axons of spiral ganglion cells bundle together to form the modiolar segment of the auditory nerve. The nerve fibers run through the center of the cochlea, pass through the internal auditory meatus, and approach the cochlear nucleus from a ventral aspect (Fig. 7, Fig. 8). Individual fibers enter the cochlear nucleus at the Schwann-glia border. The axons of both type I and type II spiral ganglion neurons ascend into the cochlear nucleus and bifurcate (Fig. 7, Fig. 8). The position of

Differences in synaptic input to the somata of type I and II neurons

Type II ganglion cells in the human were shown to receive axosomatic synapses (Kimura et al., 1979, Thiers et al., 2000). Similar kinds of synapses with asymmetric membrane thickenings and round synaptic vesicles were also observed in macaque monkeys (Kimura et al., 1987). The presence of these synapses raises the possibility of efferent modulation of type II activity from neurons whose cell bodies reside in the superior olivary complex. There have also been reports of dendrodendritic synapses

Neurotrophins, development, and survival of spiral ganglion neurons

The neurotrophins form a large family of proteins that act via tyrosine receptor kinase (Trk) signaling to promote the survival of neurons. In situ hybridization studies have implicated two neurotrophins in normal ear development and function: brain-derived neurotrophic factor (BDNF) and neurotrophin-3 (NT3) (Pirvola et al., 1992). Specifically, these authors illustrated that the mRNAs for both BDNF and NT3 were expressed in overlapping and distinct regions in the developing otic vesicle and

Summary

The spiral ganglion neurons of the cochlea represent a defined and isolated population of primary sensory neurons of critical importance in the normal transmission of sound information to the brain, in both the normal hearing individual and the cochlear implant recipient. A greater knowledge of the anatomical and neurochemical composition of spiral ganglion neurons will aid in the design of potential treatment strategies for their preservation and replacement in the deaf cochlea. Finally,

Acknowledgments

We are grateful to those researchers who contributed data to this article. We were supported in part by NIH grants DC000232, DC004395, a Life Sciences Research Award from the Office for Medical and Scientific Research, New South Wales, a grant from Advanced Bionics Corporation, the National Health and Medical Research Council of Australia, The University of Melbourne, The Garnett Passe and Rodney Williams Memorial Foundation, and the Royal Victorian Eye and Ear Hospital.

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