The spiral ganglion: Connecting the peripheral and central auditory systems
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.
References (191)
- et al.
Some quantitative observations on the cochlear division of the eighth nerve in the squirrel monkey (Saimiri sciureus)
Brain Res.
(1971) - et al.
Central trajectories of type II spiral ganglion cells from various cochlear regions in mice
Hear Res.
(1994) - et al.
A monoclonal antibody labels type II neurons of the spiral ganglion
Brain Res.
(1986) - et al.
Tonotopic organization of the anteroventral cochlear nucleus of the cat
Hear Res.
(1981) - et al.
Cochlear innervation in the greater horseshoe bat: demonstration of an acoustic fovea
Hear Res.
(1980) - et al.
Morphologic evidence for innervation of Deiters’ and Hensen’s cells in the guinea pig
Hear Res.
(1997) - et al.
The bushy cells in the anteroventral cochlear nucleus of the cat. A study with the electron microscope
Neuroscience
(1979) - et al.
Does cochlear implantation and electrical stimulation affect residual hair cells and spiral ganglion neurons?
Hear Res.
(2007) - et al.
Immunocytochemical localization of neurofilament subunits in the spiral ganglion of normal and neomycin-treated guinea pigs
Hear Res.
(1989) - et al.
Complementary roles of BDNF and NT-3 in vestibular and auditory development
Neuron
(1995)
Patterns of innervation of outer hair cells in a chimpanzee: I. Afferent and reciprocal synapses
Hear Res.
The role of neurotrophic factors in regulating the devlopment of inner ear innervation
Trends Neurosci.
The expression of the neuronal intermediate filament protein peripherin in the rat embryo
Brain Res. Dev. Brain Res.
Peripherin-like immunoreactivity in type II spiral ganglion cell body and projections
Brain Res.
Ontogenesis of type II spiral ganglion neurons during development: peripherin immunohistochemistry
Int. J. Dev. Neurosci.
The number of primary auditory afferents in the rat
Hear. Res.
Sensorineural hearing loss during development: morphological and physiological response of the cochlear and auditory brainstem
Hear Res.
Sequential alterations of neuronal architecture in nucleus magnocellularis of the developing chicken: a Golgi study
Neuroscience
Expression of intermediate filament proteins in the mature inner ear of the rat and guinea pig
Hear Res.
Chronic intracochlear electrical stimulation induces selective survival of spiral ganglion neurons in neonatally deafened cats
Hear Res.
Morphological differences among radial afferent fibers in the cat cochlea: an electron-microscopic study of serial sections
Hear Res.
Developmental changes of frequency representation in the rat cochlea
Hear Res.
A physiological place-frequency map of the cochlea in the CBA/J mouse
Hear Res.
Ultrastructural features of neurons and nerve fibres in the spiral ganglia of cats
J. Neurocytol
Neuronal morphology in the human cochlear nucleus
Arch. Otolaryngol. Head Neck Surg.
Enhanced survival of spiral ganglion cells after cessation of treatment with brain-derived neurotrophic factor in deafened guinea pigs
J. Assoc. Res. Otolaryngol.
Effects of chronic electrical stimulation on spiral ganglion neuron survival and size in deafened kittens
Laryngoscope
Hair cell innervation by spiral ganglion neurons in the mouse
J. Comp. Neurol.
Neurofilament antibodies and spiral ganglion neurons of the mammalian cochlea
J. Comp. Neurol.
Degeneration of vestibular neurons in late embryogenesis of both heterozygous and homozygous BDNF null mutant mice
Development
Degeneration of cochlear neurons after amikacin intoxication in the rat
Arch. Otorhinolaryngol.
Relations between auditory nerve endings and cell types in the cat’s anteroventral cochlear nucleus seen with the Golgi method and Nomarski optics
J. Comp. Neurol.
Cellular pattern and nerve supply of the human organ of Corti
Acta Otolaryngol.
Morphology of labeled afferent fibers in the guinea pig cochlea
J. Comp. Neurol.
Central trajectories of type II spiral ganglion neurons
J. Comp. Neurol.
Two-stage expression of neurofilament polypeptides during rat neurogenesis with early establishment of adult phosphorylation patterns
J. Neurosci.
Development of the time coding pathways in the auditory brainstem of the barn owl
J. Comp. Neurol.
The effect of cochlear implant-mediated electrical stimulation on spiral ganglion cells in congenitally deaf white cats
J. Assoc. Res. Otolaryngol.
Modulation of axon diameter and neurofilaments by hypomyelinating Schwann cells in transgenic mice
J. Neurosci.
Protective effect of neurofilament heavy gene overexpression in motor neuron disease induced by mutant superoxide dismutase
Proc. Natl. Acad. Sci. U S A
Gradients of neurotrophins, ion channels, and tuning in the cochlea
Neuroscientist
Correlations between cochlear hair cell loss and shifts of masked and absolute behavioral auditory thresholds in the house mouse
Acta Otolaryngol. (Stockholm)
Peripheral anatomy and physiology II
Quantitative analysis of nerve fibre densities in the cochlea of the house mouse (Mus musculus)
J. Comp. Neurol.
Cells expressing mRNA for neurotrophins and their receptors during embryonic rat development
Eur. J. Neurosci.
Mice lacking brain-derived neurotrophic factor develop with sensory deficits
Nature
Protection of auditory neurons from aminoglycoside toxicity by neurotrophin-3
Nat. Med.
Differential expression of two neuronal intermediate-filament proteins, peripherin and the low-molecular-mass neurofilament protein (NF-L), during the development of the rat
J. Neurosci.
Severe sensory and sympathetic deficits in mice lacking neurotrophin-3
Nature
Spatial shaping of cochlear innervation by temporally regulated neurotrophin expression
J. Neurosci.
Cited by (150)
Hidden hearing loss: Fifteen years at a glance
2024, Hearing ResearchExpression and distribution of Nob1 in the developing rat cochleae
2022, Gene Expression PatternsScope of using hollow fibers as a medium for drug delivery
2022, Fiber and Textile Engineering in Drug Delivery Systems