Central trajectories of type II spiral ganglion neurons

Brown, M. Christian; Berglund, A. M.; Kiang, N. Y. S.; Ryugo, David K.

doi:10.1002/cne.902780409

Cited by 146 publications

(105 citation statements)

References 33 publications

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“…1). Fibers with these characteristics have been traced back to parent fibers and cell bodies of origin and confirmed to be type II in previous studies (Brown et al 1988a;Brown and Ledwith 1990;Berglund and Brown 1994;Berglund et al 1996). These studies also suggest that the complete extent of the type II projection into the cochlear nucleus is revealed with HRP labeling.…”

Section: Light Microscopic Observationssupporting

confidence: 70%

“…1) and terminate in the cochlear nucleus (Lorente de No 1933;Fekete et al 1984;Brown et al 1988a). Type I fibers have an excitatory influence on their postsynaptic targets, leading to discharge of cochlear-nucleus neurons (Pfeiffer 1966;Golding et al 1995;Kopp-Scheinpflug et al 2002).…”

Section: Introductionmentioning

confidence: 99%

“…Ellipsoidal swellings may thus arise merely as a consequence of the few organelles they contain. In the lamina, type II fibers are relatively isolated from the more numerous terminations of type I fibers that are restricted to the core (Brown et al 1988a;Brown and Ledwith 1990;Berglund and Brown 1994). Perhaps this segregation results from type II fibers projecting to unique targets in the lamina; whatever the reason, the offset allows study of labeled type II fibers in relative isolation.…”

Section: Introductionmentioning

confidence: 99%

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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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Section: Light Microscopic Observationssupporting

confidence: 70%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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

Benson

Brown

2004

JARO

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“…The granule cell domain of the cochlear complex was shown to receive projections from a number of auditory and non-auditory nuclei, and from the thin and unmyelinated type II auditory nerve fibers (Brown et al, 1988). Furthermore, Doucet and Ryugo (1997) showed that microneurons of the granule cell domain projected to the DCN.…”

Section: Discussionmentioning

confidence: 99%

Neurons in the cochlear nuclei controlling the tensor tympani muscle in the rat: A study using pseudorabies virus

et al. 2007

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The middle ear muscle reflex has been implicated in modulation of auditory input and protection of the inner ear from acoustic trauma. However, the identification of neurons in the cochlear nuclei participating in this reflex has not been fully elucidated. In the present study, we injected the retrograde transynaptic tracer pseudorabies virus into single tensor tympani (TT) muscles, and identified transynaptically labeled cochlear nucleus neurons at multiple survival times. Motoneurons controlling TT were located ventral to the ipsilateral motor trigeminal nucleus and extended rostrally towards the medial aspect of the lateral lemniscus. Transynaptically-labeled neurons were observed bilaterally in the dorsal and dorso-medial parts of ventral cochlear nuclei as early as 48 h after virus injection, and had morphological features of radiate multipolar cells. After ≥ 69 h, labeled cells of different types were observed in all cochlear nuclei. At those times, labeling was also detected bilaterally in the medial nucleus of the trapezoid body and periolivary cell groups in the superior olivary complex. Based on the temporal course of viral replication, our data strongly suggest the presence of a direct projection of neurons from the ventral cochlear nuclei bilaterally to the TT motoneuron pool in rats. The influence of neurons in the cochlear nuclei upon TT activity through direct and indirect pathways may account for multifunctional roles of this muscle in auditory functions. Keywordsdirect and indirect acoustic reflex pathways; middle ear muscle; transynaptic transport

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“…Type I and type II axons arborize in parallel to the dorsal and ventral cochlear nuclei in the brainstem; but only type II endings are found within the small cell cap and granule cell layers that envelope the principal nuclei (28)(29)(30)(31)(32). The granule cell domain is thought to be a site for multimodal integration as well as the target of collaterals from olivocochlear efferents (29,30,(33)(34)(35)(36)(37)(38).…”

Section: Discussionmentioning

confidence: 99%

Unmyelinated type II afferent neurons report cochlear damage

Liu

Glowatzki

Fuchs

2015

Proc. Natl. Acad. Sci. U.S.A.

114

102

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In the mammalian cochlea, acoustic information is carried to the brain by the predominant (95%) large-diameter, myelinated type I afferents, each of which is postsynaptic to a single inner hair cell. The remaining thin, unmyelinated type II afferents extend hundreds of microns along the cochlear duct to contact many outer hair cells. Despite this extensive arbor, type II afferents are weakly activated by outer hair cell transmitter release and are insensitive to sound. Intriguingly, type II afferents remain intact in damaged regions of the cochlea. Here, we show that type II afferents are activated when outer hair cells are damaged. This response depends on both ionotropic (P2X) and metabotropic (P2Y) purinergic receptors, binding ATP released from nearby supporting cells in response to hair cell damage. Selective activation of P2Y receptors increased type II afferent excitability by the closure of KCNQ-type potassium channels, a potential mechanism for the painful hypersensitivity (that we term "noxacusis" to distinguish from hyperacusis without pain) that can accompany hearing loss. Exposure to the KCNQ channel activator retigabine suppressed the type II fiber's response to hair cell damage. Type II afferents may be the cochlea's nociceptors, prompting avoidance of further damage to the irreparable inner ear.type II cochlear afferents | ATP | acoustic trauma | hyperacusis | noxacusis T he mammalian cochlea is the most elaborate of vertebrate auditory organs. The elegantly coiled, mechanically tuned cochlear duct and functional differentiation between inner hair cells (IHCs) and outer hair cells (OHCs), afferent and efferent neuronal connections are among the features that enable the widest acoustic frequency range and most complex vocalizations among vertebrate species. This benefit, however, has been gained at a significant cost in the metabolic and mechanical vulnerability of cochlear hair cells and neurons. Loud sound progressively damages type I afferent neurons and OHCs (1). Once damaged beyond repair, these do not regenerate as they do in nonmammalian vertebrates, suggesting that protective mechanisms should exist to preserve cochlear function. Indeed, middle ear reflexes (2) and efferent inhibition of hair cells (3) can mitigate acoustic trauma to some extent. However, a more effective strategy is simply to avoid or withdraw from sources of trauma, by analogy to limb withdrawal triggered by C-fiber activation in skin.Here, we provide evidence that unmyelinated type II cochlear afferents can report cochlear trauma, a potential trigger for nocifensive behavior. Hyperactivity of type II neurons could contribute as well to the paradoxical hypersensitivity to loud sound that can accompany hearing loss, despite diminished type I afferent function. Hyperacusis is a comorbidity in 80% of tinnitus patients (4) suggesting common pathogenic mechanisms (5). In the most severe cases, hyperacusis is described as debilitating "ear pain" (6). The response to trauma by type II afferents may relate most directly to such ...

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Central trajectories of type II spiral ganglion neurons

Cited by 146 publications

References 33 publications

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

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

Neurons in the cochlear nuclei controlling the tensor tympani muscle in the rat: A study using pseudorabies virus

Unmyelinated type II afferent neurons report cochlear damage

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