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Heterogeneous Calretinin Expression in the Avian Cochlear Nucleus Angularis

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Abstract

Multiple calcium-binding proteins (CaBPs) are expressed at high levels and in complementary patterns in the auditory pathways of birds, mammals, and other vertebrates, but whether specific members of the CaBP family can be used to identify neuronal subpopulations is unclear. We used double immunofluorescence labeling of calretinin (CR) in combination with neuronal markers to investigate the distribution of CR-expressing neurons in brainstem sections of the cochlear nucleus in the chicken (Gallus gallus domesticus). While CR was homogeneously expressed in cochlear nucleus magnocellularis, CR expression was highly heterogeneous in cochlear nucleus angularis (NA), a nucleus with diverse cell types analogous in function to neurons in the mammalian ventral cochlear nucleus. To quantify the distribution of CR in the total NA cell population, we used antibodies against neuronal nuclear protein (NeuN), a postmitotic neuron-specific nuclear marker. In NA neurons, NeuN label was variably localized to the cell nucleus and the cytoplasm, and the intensity of NeuN immunoreactivity was inversely correlated with the intensity of CR immunoreactivity. The percentage of CR + neurons in NA increased from 31 % in embryonic (E)17/18 chicks, to 44 % around hatching (E21), to 51 % in postnatal day (P) 8 chicks. By P8, the distribution of CR + neurons was uniform, both rostrocaudal and in the tonotopic (dorsoventral) axis. Immunoreactivity for the voltage-gated potassium ion channel Kv1.1, used as a marker for physiological type, showed broad and heterogeneous postsynaptic expression in NA, but did not correlate with CR expression. These results suggest that CR may define a subpopulation of neurons within nucleus angularis.

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Abbreviations

NA:

Nucleus angularis

NM:

Nucleus magnocellularis

NL:

Nucleus laminaris

CR:

Calretinin

PV:

Parvalbumin

CaBP:

Calcium-binding protein

NeuN:

Neuronal nuclear protein

MAP2:

Microtubule-associated protein 2

IC:

Inferior colliculus

ICc:

Central nucleus of the inferior colliculus

MLd:

Nucleus mesencephalicus lateralis pars dorsalis (IC)

ITD:

Interaural time difference

ILD:

Interaural level difference

E:

Embryonic (day)

P:

Postnatal (day)

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Acknowledgments

This study was supported by the National Institute of Deafness and Communication Disorders (NIDCD) grant DC10000 (KMM) and P30 NIDCD grant DC0466 to the University of Maryland (Center for the Comparative and Evolutionary Biology of Hearing). We gratefully acknowledge Dr. A. Beaven and the College of Mathematics and Natural Sciences Imaging Core for microscopy support, and Dr. C. E. Carr for technical advice and many helpful discussions.

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The authors declare that they have no conflict of interest.

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Correspondence to K. M. MacLeod.

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Bloom, S., Williams, A. & MacLeod, K.M. Heterogeneous Calretinin Expression in the Avian Cochlear Nucleus Angularis. JARO 15, 603–620 (2014). https://doi.org/10.1007/s10162-014-0453-0

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  • DOI: https://doi.org/10.1007/s10162-014-0453-0

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