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

ABSTRACT: 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 colocalization 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 subdistributions were noted. For example, calretinin levels were highest in neurons innervating the midcochlea region, whereas calbindin levels were similar across the entire ganglion. Furthermore, we noted that apical type II neurons, identified by antiperipherin 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 subthreshold response showed a pattern related to quantified calretinin and calbindin staining levels. Taken together, our results suggest an additional dimension of complexity within the spiral ganglion beyond that currently categorized.

SUBMITTER: Liu W

PROVIDER: S-EPMC3997597 | biostudies-literature | 2014 Jul

REPOSITORIES: biostudies-literature

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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 Wenke W Davis Robin L RL

The Journal of comparative neurology 20140701 10

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 level ...[more]

PMID: 24414968

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Project description:PurposeIntracellular free calcium ions (Ca(2+)) are an important element in retinal ganglion cell response. Two major EF-hand (E-helix-loop-F-helix-hand) calcium binding proteins in the retina, calretinin and calbindin-28 kDa, are important buffers of intracellular free Ca(2+) in neurons, and may also serve as Ca(2+)-dependent regulators of enzymes and ion channels.MethodsThis study used immunohistochemistry to investigate the subcellular expression patterns of calretinin and calbindin-28 kDa, in the soma, dendrites, and the axonal compartment of rat retinal ganglion cells.ResultsAntibodies for calretinin and calbindin-28 kDa labeled different cell populations in the retinal ganglion cell layer. In this layer, calretinin labeled a larger number of cells compared to calbindin-28 kDa, many, but not all, of which were displaced amacrine cells. The calbindin-28 kDa immunopositive neurons were distinct in that their somata were peripherally encircled by microtubule associated protein 1 (MAP-1) or neurofilament-200 kDa subunit (NF-200 kDa) immunofluorescence. Although somata of retinal ganglion cells contained these calcium binding proteins, neither protein was found in the dendrites or initial segments of the axons. However, both were expressed in the ganglion cell axons in nerve fiber layer. Calretinin and calbindin-28 kDa staining overlapped in some fibers and not in others. Calretinin immunofluorescence was concentrated in discrete axonal regions, which showed limited staining for calbindin-28 kDa or for NF200 kDa, suggesting its close proximity to the plasma membrane.ConclusionsThere is a clear compartmentalization of calbindin-28 kDa and calretinin distribution in retinal ganglion cells. This suggests that the two calcium binding proteins perform distinct functions in localized calcium signaling. It also indicates that rather than freely diffusing through the cytoplasm to attain a homogeneous distribution, calbindin-28 kDa and calretinin must be bound to cellular structures through interactions that are likely important for their functions.

Dataset Information

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

Publications

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

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