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>3.3.co;2-1

Cited by 7 publications

(10 citation statements)

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“…Thus, as with the calretinin and calbindin colabeling pattern in the retina that indicates separate parallel pathways demarked by calcium binding protein distribution (Mojumder et al, ), we wondered whether this was also the case in the spiral ganglion. To explore this possibility further, we took advantage of the type II neuron marker peripherin (Hafidi, ), which has previously been validated to stain type II spiral ganglion neurons specifically (Mou et al, ). Colabeling of peripherin with either calretinin or calbindin was characterized in individual experiments to obtain unequivocal profiles of calretinin and calbindin distributions in type I and type II neurons in vitro.…”

Section: Resultsmentioning

confidence: 99%

“…Monoclonal mouse antiperipherin antibody (Chemicon, Temecula, CA; MAB1527) was used as a marker for type II spiral ganglion neurons according to previous reports (Mou et al, ; Reid et al, ). The appropriate concentration of antiperipherin antibody was determined using a preparation in which the organ of Corti and the ganglion were cultured for 3 days in vitro, such that the type I and type II afferent innervations patterns were retained and could be distinguished by using antiperipherin antibody staining (Flores‐Otero and Davis, ).…”

Section: Methodsmentioning

confidence: 99%

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Calretinin and calbindin distribution patterns specify subpopulations of type I and type II spiral ganglion neurons in postnatal murine cochlea

Liu

Davis²

2014

J of Comparative Neurology

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As the first neural element in the auditory pathway, neurons in the spiral ganglion shape the initial coding of sound stimuli for subsequent processing. Within the ganglion, type I and type II neurons form divergent and convergent innervation patterns, respectively, with their hair cell sensory receptors, indicating that very different information is gathered and conveyed. Layered onto these basic innervation patterns are structural and electrophysiological features that provide additional levels of processing multifaceted sound stimuli. To understand the nature of this additional complexity of signal coding, we characterized the distribution of calretinin and calbindin, two regulators of intracellular calcium that serve as markers for neuronal subpopulations. We showed in acute preparations and in vitro that calretinin and calbindin staining levels were heterogeneous. Immunocytochemical analysis of co-localization further showed that high levels of staining for the two molecules rarely overlapped. Although varied amounts of calbindin and calretinin were found within each tonotopic location and neuronal type, some distinct sub-distributions were noted. For example, calretinin levels were highest in neurons innervating the mid-cochlea region, whereas calbindin levels were similar across the entire ganglion. Furthermore, we noted that apical type II neurons, identified by anti-peripherin labeling had significantly lower levels of calretinin and higher levels of calbindin. We also established that the endogenous firing feature of onset tau of the sub-threshold response showed a pattern related to quantified calretinin and calbindin staining levels. Taken together, our results are suggestive of an additional dimension of complexity within the spiral ganglion beyond that currently categorized.

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Section: Resultsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Calretinin and calbindin distribution patterns specify subpopulations of type I and type II spiral ganglion neurons in postnatal murine cochlea

Liu

Davis²

2014

J of Comparative Neurology

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“…Evidence that these neurons might be especially susceptible to developmental cell death is provided by studies of mice and gerbil spiral ganglion cells growing in organotypic cultures. In these experiments, NT-3 and BDNF, two neurotrophic molecules expressed within the developing cochlea, were found to act synergistically in a time-dependent and cell-specific manner to enhance the survival of Type I, but not Type II neurons (Mou et al, 1997(Mou et al, , 1998. These effects were maximal in cochlear explants obtained from animals during the first 2 postnatal days.…”

Section: Time-course Of Cochlear Neuron Cell Deathmentioning

confidence: 86%

Development of ganglion cell topography in the postnatal cochlea

Echteler

Nofsinger

2000

J. Comp. Neurol.

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In mammals, the size and number of spiral ganglion cells can vary significantly along the length of the cochlea. At present, it is unclear how these topologic differences in spiral ganglion cell morphology and density emerge during development. We addressed this issue by quantifying developmental changes in the number, density, and size of auditory ganglion cells within the cochlea of Mongolian gerbils throughout the first 3 weeks of postnatal life. In each cochlea, cells were measured at five standardized locations along the length of the spiral ganglion, as determined from serial reconstruction of Rosenthal's canal. During the first postnatal week, the total number of gerbil spiral ganglion cells decreased significantly by 27%, without further change thereafter. This brief period of neuronal cell death coincides with a major remodeling in the afferent neural projections to gerbil auditory hair cells (Echteler [1992] Proc. Natl. Acad. Sci. USA 89:6324-6327). The resulting reduction in neuronal density varied with location, being most prominent within the upper basal and lower middle turns of the cochlea. These same regions contained the smallest auditory ganglion cells found within the gerbil ear and exhibited the least amount of developmental expansion in the circumference of Rosenthal's canal. These results suggest the possibility that regional differences in auditory neuron size and number might be influenced by local extrinsic factors, such as the availability of canal space.

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“…While recent studies in rats indicate that peripherin is up-regulated in type I SGN following explant culture of P5 SGN [16], it seems that this up-regulation is species specific. Thorough examination of mouse SGN following organotypic and explant culture has shown that peripherin is not up-regulated in type I SGN [23, 27]. While we show a large number of SGN express peripherin in our P1 explants, this likely reflects the relatively larger representation of type II SGN near birth [14] as the number of peripherin immunolabelled neurons in P7 SGN explants reflects the mature representation of type II SGN in the cochlea (M. Barclay, A. F. Ryan and G. D. Housley, unpublished observations).…”

Section: Discussionmentioning

confidence: 99%

Type III intermediate filament peripherin inhibits neuritogenesis in type II spiral ganglion neurons in vitro

Barclay

Julien

Ryan

et al. 2010

Neuroscience Letters

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Peripherin, a type III intermediate filament protein, forms part of the cytoskeleton in a subset of neurons, most of which have peripheral fibre projections. Studies suggest a role for peripherin in axon outgrowth and regeneration, but evidence for this in sensory and brain tissues is limited. The exclusive expression of peripherin in a sub-population of primary auditory neurons, the type II spiral ganglion neurons (SGN) prompted our investigation of the effect of peripherin gene deletion (pphKO) on these neurons. We used confocal immunofluorescence to examine the establishment of the innervation of the cochlear outer hair cells by the type II SGN neurites in vivo and in vitro, in wildtype (WT) and pphKO mice, in the first postnatal week. The distribution of the type II SGN nerve fibres was normal in pphKO cochleae. However, using P1 spiral ganglion explants under culture conditions where the majority of neurites were derived from type II SGN, pphKO resulted in increased numbers of neurites/explant compared WT controls. Type II SGN neurites from pphKO explants extended ~ double the distance of WT neurites, and had reduced complexity based on greater distance between turning points. Addition of brain-derived neurotrophic factor (BDNF) to the culture media increased neurite number in WT and KO explants ~30-fold, but did not affect neurite length or distance between turning. These results indicate that peripherin may interact with other cytoskeletal elements to regulate outgrowth of the peripheral neurites of type II SGN, distinguishing these neurons from the type I SGN innervating the inner hair cells.

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

Cited by 7 publications

References 0 publications

Calretinin and calbindin distribution patterns specify subpopulations of type I and type II spiral ganglion neurons in postnatal murine cochlea

Calretinin and calbindin distribution patterns specify subpopulations of type I and type II spiral ganglion neurons in postnatal murine cochlea

Development of ganglion cell topography in the postnatal cochlea

Type III intermediate filament peripherin inhibits neuritogenesis in type II spiral ganglion neurons in vitro

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