Hair-Cell Innervation by Spiral Ganglion Cells in Adult Cats

Kiang, N. Y. S.; Rho, Jiyun; Northrop, Clarinda; Liberman, M. Charles; Ryugo, David K.

doi:10.1126/science.7089553

Cited by 278 publications

(135 citation statements)

References 8 publications

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“…Large type I neurons with peripheral processes synapsing on inner hair cells represent approximately 90Y95% of the afferent auditory neurons and are myelinated. The remaining small type II neurons innervate the outer hair cells and are unmyelinated (Spoendlin 1969;Kiang et al 1982Kiang et al , 1984 (Berglund and Ryugo 1986;Hafidi 1998). Our previous study demonstrated that a small number of neurons with small nuclei survive after acute ouabain treatment (Schmiedt et al 2002).…”

Section: Introductionmentioning

confidence: 88%

Ouabain Induces Apoptotic Cell Death in Type I Spiral Ganglion Neurons, but not Type II Neurons

Lang

Schulte

Schmiedt

2005

JARO

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Application of ouabain to the intact round-window (RW) membrane of the gerbil cochlea induces apoptosis in most spiral ganglion neurons (SGNs), leaving a few neurons intact (Schmiedt et al. 2002). Here, physiological measures and immunostaining were used to examine the process of SGN degeneration at 3, 6, 12, and 24 h, 4 days, and 1 and 5 months after ouabain treatment. The few remaining neurons surviving up to 5 months after ouabain treatment were immunoreactive for peripherin, a type II neuron marker. Peripherin-positive cell counts indicate that about 7% of the SGNs in the gerbil cochlea are type II neurons, and these neurons survive intact after ouabain treatment. Ouabain exposure had little effect on the outer hair cell and lateral wall systems, even after a 5 month loss of auditory-nerve function. The cellular locations of cytochrome c, poly (ADP-ribose) polymerase (PARP), and activated caspase 3 were examined in control and ouabain-treated cochleas. A redistribution of cytochrome c in peripherinnegative (type I) neurons was observed at 3 h after ouabain exposure. Degraded PARP and activated caspase 3 were also detected in peripherin-negative SGNs at 6 and 24 h after treatment, respectively. These results suggest that the redistribution of cytochrome c is an early event during apoptosis in type I SGNs and that activation of PARP and caspase 3 are associated with apoptosis in these cells. Calcineurin and NF-kB are two important signaling pathways that may modulate cell survival in the central nervous system. Here, we found that calcineurin and NF-kB selectively labeled type II neurons. It is speculated that the high levels of calcineurin and NF-kB in type II SGNs, as compared with type I SGNs, may play protective roles in enhancing the survival of type II neurons exposed to ouabain.

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Section: Introductionmentioning

confidence: 88%

Ouabain Induces Apoptotic Cell Death in Type I Spiral Ganglion Neurons, but not Type II Neurons

Lang

Schulte

Schmiedt

2005

JARO

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“…In cats, each inner hair cell is innervated by a single synapse from ten to 20 type I SG neurons (Kiang et al 1982;Liberman et al 1990;Spoendlin 1969Spoendlin , 1975Spoendlin , 1981. Type I cells comprise roughly 95 % of the SG population; they provide the main information pathway to the central auditory system (Kiang et al 1982) and therefore represent the neural substrate for cochlear implant (CI) function. In sensorineural hearing loss, the hair cells degenerate, the distal dendrites of the SG neurons (radial nerve fibers) begin to retract, and subsequently the ganglion cell somata in the cochlear modiolus also degenerate.…”

Section: Introductionmentioning

confidence: 99%

Effects of Brain-Derived Neurotrophic Factor (BDNF) and Electrical Stimulation on Survival and Function of Cochlear Spiral Ganglion Neurons in Deafened, Developing Cats

Leake

Stakhovskaya

Hetherington

et al. 2013

JARO

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Both neurotrophic support and neural activity are required for normal postnatal development and survival of cochlear spiral ganglion (SG) neurons. Previous studies in neonatally deafened cats demonstrated that electrical stimulation (ES) from a cochlear implant can promote improved SG survival but does not completely prevent progressive neural degeneration. Neurotrophic agents combined with an implant may further improve neural survival. Short-term studies in rodents have shown that brain-derived neurotrophic factor (BDNF) promotes SG survival after deafness and may be additive to trophic effects of stimulation. Our recent study in neonatally deafened cats provided the first evidence of BDNF neurotrophic effects in the developing auditory system over a prolonged duration Leake et al. (J Comp Neurol 519:1526-1545. Ten weeks of intracochlear BDNF infusion starting at 4 weeks of age elicited significant improvement in SG survival and larger soma size compared to contralateral. In the present study, the same deafening and BDNF infusion procedures were combined with several months of ES from an implant. After combined BDNF + ES, a highly significant increase in SG numerical density (950 % improvement re: contralateral) was observed, which was significantly greater than the neurotrophic effect seen with ES-only over comparable durations. Combined BDNF + ES also resulted in a higher density of myelinated radial nerve fibers within the osseous spiral lamina. However, substantial ectopic and disorganized sprouting of these fibers into the scala tympani also occurred, which may be deleterious to implant function. EABR thresholds improved (re: initial thresholds at time of implantation) on the chronically stimulated channels of the implant. Terminal electrophysiological studies recording in the inferior colliculus (IC) revealed that the basic cochleotopic organization was intact in the midbrain in all studied groups. In deafened controls or after ES-only, lower IC thresholds were correlated with more selective activation widths as expected, but no such correlation was seen after BDNF + ES due to much greater variability in both measures.

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“…The neurons that give rise to these fibers have been subdivided into two types depending on which receptor cell population is contacted in the cochlea. Type I neurons provide the afferent innervation of inner hair cells, whereas type II neurons provide the afferent innervation of outer hair cells (Spoendlin 1971;Kiang et al 1982). It is clear that type I neurons, which comprise more than 90% of all primary auditory neurons, provide the main pathway for auditory input to the brain.…”

Section: Introductionmentioning

confidence: 99%

Postsynaptic Targets of Type II Auditory Nerve Fibers in the Cochlear Nucleus.

Benson

Brown

2004

JARO

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Type II auditory nerve fibers, which provide the primary afferent innervation of outer hair cells of the cochlea, project thin fibers centrally and form synapses in the cochlear nucleus. We investigated the postsynaptic targets of these synapses, which are unknown. Using serial-section electron microscopy of fibers labeled with horseradish peroxidase, we examined the border of the granule-cell lamina in mice, an area of type II termination that receives branches having swellings with complex shapes. About 70% of the swellings examined with the electron microscope formed morphological synapses, which is a much higher value than found in previous studies of type II swellings in other parts of the cochlear nucleus. The high percentage of synapses enabled a number of postsynaptic targets to be identified. Most of the targets were small dendrites. Two of these dendrites were traced to their somata of origin, which were cochlear-nucleus ''small cells'' situated at the border of the granule-cell lamina. These cells did not appear to receive any terminals containing synaptic vesicles that were large and round, indicating a lack of input from type I auditory nerve fibers. Nor did type II swellings or targets participate in the synaptic glomeruli formed by mossy terminals and the dendrites of granule cells. Other type II synapses were axosomatic and their targets were large cells, which were presumed multipolar cells and one cell with characteristics of a globular bushy cell. These large cells almost certainly receive additional input from type I auditory nerve fibers, which provide the afferent innervation of the cochlear inner hair cells. A few type II postsynaptic targets-the two small cells as well as a large dendrite-received synapses that had accompanying postsynaptic bodies, a likely marker for synapses of medial olivocochlear branches. These targets thus probably receive convergent input from type II fibers and medial olivocochlear branches. The diverse nature of the type II targets and the examples of segregated convergence of other inputs illustrates the synaptic complexity of type II input to the cochlear nucleus.

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Hair-Cell Innervation by Spiral Ganglion Cells in Adult Cats

Cited by 278 publications

References 8 publications

Ouabain Induces Apoptotic Cell Death in Type I Spiral Ganglion Neurons, but not Type II Neurons

Ouabain Induces Apoptotic Cell Death in Type I Spiral Ganglion Neurons, but not Type II Neurons

Effects of Brain-Derived Neurotrophic Factor (BDNF) and Electrical Stimulation on Survival and Function of Cochlear Spiral Ganglion Neurons in Deafened, Developing Cats

Postsynaptic Targets of Type II Auditory Nerve Fibers in the Cochlear Nucleus.

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