Time-dependence and cell-type specificity of synergistic neurotrophin actions on spiral ganglion neurons

Mou, Kewa; Adamson, Crista L.; Davis, Robin L.

doi:10.1002/(sici)1096-9861(19981207)402:1<129::aid-cne9>3.0.co;2-a

Cited by 43 publications

(31 citation statements)

References 71 publications

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“…Peripherin antibody was used to distinguish type II neurons from the total population of spiral ganglion neurons. On the basis of results reported in vivo (Hafidi, 1998) and confirmed in vitro (Mou et al, 1998), this intermediate filament has been found to be enriched in type II spiral ganglion neurons. Monoclonal (MAB 1527; Chemicon, Temecula, CA) and polyclonal (AB-1530; Chemicon) peripherin antisera were used in the following dilutions: 1:75 and 1:4000, respectively.…”

Section: Methodssupporting

confidence: 90%

“…Type II neurons, however, possess molecular markers that can be used to distinguish them from type I neurons. We have shown previously that antibodies to the neurofilament protein peripherin label type II neurons preferentially in vitro (Mou et al, 1998). We also observed recently that two of the four family members of the membrane-associated guanylate kinases (MAGUKs), synapse-associated protein (SAP) and SAP102, are enriched in the type II spiral ganglion neurons (Hsu et al, 2002).…”

Section: Resultsmentioning

confidence: 62%

“…The challenge was to identify unequivocally type II neurons without the aid of their connections to peripheral receptors and to do so for neurons that compose only ϳ5% of the spiral ganglion. Our approach was to record from neurons that were subsequently stained with an antibody to a protein that is highly enriched in type II neurons (Hafidi, 1998;Mou et al, 1998). Thus, we have undertaken this study with the understanding that literally hundreds of recordings must be made to obtain even a limited number of type II recordings.…”

Section: Introductionmentioning

confidence: 84%

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Firing Patterns of Type II Spiral Ganglion NeuronsIn Vitro

Reid¹,

Flores‐Otero²,

Davis³

2004

J. Neurosci.

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Type I and type II spiral ganglion neurons convey auditory information from the sensory receptors in the cochlea to the CNS. The numerous type I neurons have been extensively characterized, but the small population of type II neurons with their unmyelinated axons are undetectable with most recording methods. Despite the paucity of information about the type II neurons, it is clear that they must have a significant role in sound processing because they innervate the large number of outer hair cells that are critical for maintaining normal responses to stimuli. To elucidate the function of type II neurons, we have developed an approach for studying their electrophysiological features in vitro.Type II neurons obtained from postnatal day 6 -7 mice displayed distinctly different firing properties than type I neurons. They showed slower accommodation, lower action potential thresholds, and more prolonged responses to depolarizing current injection than the type I neurons. These differences were most evident in neurons from the basal, high-frequency region of the cochlea. The basal type I neurons displayed uniformly fast firing features, whereas the basal type II neurons showed particularly slow accommodation and responses to depolarization. Interestingly, neurons from the apical, low-frequency region of the cochlea showed the opposite trend. These data suggest that the type I and type II neurons have specialized electrophysiological characteristics tailored to their different roles in auditory signal processing. In particular, the type II neuron properties are consistent with cells in other sensory systems that receive convergent synaptic input for high-sensitivity stimulus detection.

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Section: Methodssupporting

confidence: 90%

Section: Resultsmentioning

confidence: 62%

Section: Introductionmentioning

confidence: 84%

See 1 more Smart Citation

Firing Patterns of Type II Spiral Ganglion NeuronsIn Vitro

Reid¹,

Flores‐Otero²,

Davis³

2004

J. Neurosci.

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“…However, various factors can limit the use of peripherin as a type II biomarker. Peripherin immunolabeling can vary with species and tonotopic position (Mou et al 1998). Further, peripherin antibodies label type I as well as type II afferents in the perinatal cochlea (Hafidi et al 1993).…”

Section: Synaptic Structures Of Type II Afferentssupporting

confidence: 91%

Tyrosine Hydroxylase Expression in Type II Cochlear Afferents in Mice

Vyas

Zimmerman

et al. 2016

JARO

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Acoustic information propagates from the ear to the brain via spiral ganglion neurons that innervate hair cells in the cochlea. These afferents include unmyelinated type II fibers that constitute 5 % of the total, the majority being myelinated type I neurons. Lack of specific genetic markers of type II afferents in the cochlea has been a roadblock in studying their functional role. Unexpectedly, type II afferents were visualized by reporter proteins induced by tyrosine hydroxylase (TH)-driven Cre recombinase. The present study was designed to determine whether TH-driven Cre recombinase (TH-2A-CreER) provides a selective and reliable tool for identification and genetic manipulation of type II rather than type I cochlear afferents. The BTH-2A-CreER neurons^radiated from the spiral lamina, crossed the tunnel of Corti, turned towards the base of the cochlea, and traveled beneath the rows of outer hair cells. Neither the processes nor the somata of TH-2A-CreER neurons were labeled by antibodies that specifically labeled type I afferents and medial efferents.TH-2A-CreER-positive processes partially co-labeled with antibodies to peripherin, a known marker of type II afferents. Individual TH-2A-CreER neurons gave off short branches contacting 7-25 outer hair cells (OHCs). Only a fraction of TH-2A-CreER boutons were associated with CtBP2-immunopositive ribbons. These results show that TH-2A-CreER provides a selective marker for type II versus type I afferents and can be used to describe the morphology and arborization pattern of type II cochlear afferents in the mouse cochlea.

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“…In addition to exerting a powerful effect on survival (Pirvola et al, 1992;Zheng et al, 1995;Mou et al, 1998;Hossain et al, 2002), BDNF and NT-3 have opposing actions on the firing features of spiral ganglion neurons. BDNF is responsible for fast firing characteristics that typify the basal neurons which transmit high frequency sound signals into the brain; NT-3, however, mediates slower and more heterogeneous firing patterns that characterize the apical neurons which convey low frequency sound information (Davis, 2003).…”

Section: Introductionmentioning

confidence: 99%

Reciprocal Regulation of Presynaptic and Postsynaptic Proteins in Bipolar Spiral Ganglion Neurons by Neurotrophins

Flores‐Otero¹,

Xue²,

Davis³

2007

J. Neurosci.

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A unifying principle of sensory system organization is feature extraction by modality-specific neuronal maps in which arrays of neurons show systematically varied response properties and receptive fields. Only beginning to be understood, however, are the mechanisms by which these graded systems are established. In the peripheral auditory system, we have shown previously that the intrinsic firing features of spiral ganglion neurons are influenced by brain-derived neurotrophic factor (BDNF) and neurotrophin-3 (NT-3). We now show that is but a part of a coordinated package of neurotrophin actions that also includes effects on presynaptic and postsynaptic proteins, thus encompassing the input, transmission, and output functions of the spiral ganglion neurons. Using immunocytochemical methods, we determined that proteins targeted to opposite ends of the neuron were organized and regulated in a reciprocal manner. AMPA receptor subunits GluR2 and GluR3 were enriched in base neurons compared with their apex counterparts. This distribution pattern was enhanced by exposure to BDNF but reduced by NT-3. SNAP-25 and synaptophysin were distributed and regulated in the mirror image: enriched in the apex, enhanced by NT-3 and reduced by BDNF. Moreover, we used a novel coculture to identify potential endogenous sources of neurotrophins by showing that sensory receptors from different cochlear regions were capable of altering presynaptic and postsynaptic protein levels in these neurons. From these studies, we suggest that BDNF and NT-3, which are systematically distributed in complementary gradients, are responsible for orchestrating a comprehensive set of electrophysiological specializations along the frequency contour of the cochlea.

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Time-dependence and cell-type specificity of synergistic neurotrophin actions on spiral ganglion neurons

Cited by 43 publications

References 71 publications

Firing Patterns of Type II Spiral Ganglion NeuronsIn Vitro

Firing Patterns of Type II Spiral Ganglion NeuronsIn Vitro

Tyrosine Hydroxylase Expression in Type II Cochlear Afferents in Mice

Reciprocal Regulation of Presynaptic and Postsynaptic Proteins in Bipolar Spiral Ganglion Neurons by Neurotrophins

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