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Catecholamine-independent transient expression of tyrosine hydroxylase in primary auditory neurons is coincident with the onset of hearing in the rat cochlea

Authors

  • Nuno Trigueiros-Cunha,

    1. INSERM U.583 and Université Montpellier 1, 71 rue de Navacelles, F-34090 Montpellier, France
    2. Faculdade de Medicina da Universidade do Porto, Instituto de Anatomia, 4200 Porto, Portugal
    3. Instituto de Biologia Molecular e Celular (IBMC), 4150 Porto, Portugal
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  • Nicole Renard,

    1. INSERM U.583 and Université Montpellier 1, 71 rue de Navacelles, F-34090 Montpellier, France
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  • Ghislaine Humbert,

    1. INSERM U.583 and Université Montpellier 1, 71 rue de Navacelles, F-34090 Montpellier, France
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  • Maria Amélia Tavares,

    1. Faculdade de Medicina da Universidade do Porto, Instituto de Anatomia, 4200 Porto, Portugal
    2. Instituto de Biologia Molecular e Celular (IBMC), 4150 Porto, Portugal
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  • Michel Eybalin

    1. INSERM U.583 and Université Montpellier 1, 71 rue de Navacelles, F-34090 Montpellier, France
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: Dr Michel Eybalin, as above.
E-mail: eybalin@montp.inserm.fr

Abstract

During the last stages of neuronal maturation, tyrosine hydroxylase is transiently expressed in the absence of the other catecholamine-synthesizing enzymes. We show here that it is expressed in rat spiral ganglion neurons between postnatal days 8 and 20, with a peak of expression at postnatal day 12. These tyrosine hydroxylase-immunoreactive neurons did not display aromatic amino acid decarboxylase- or dopamine-β-hydroxylase-immunoreactivities, ruling out the possibilities of dopamine or noradrenaline synthesis. They also did not display peripherin- or intense neurofilament 200-kDa-immunoreactivities, two indicators of type II primary auditory neurons. Tyrosine hydroxylase-immunoreactive dendrites were seen in synaptic contact with the inner hair cells and expressed the GluR2 subunit of α-amino-3-hydroxy-5-methyl-4-isoxazole propionic acid receptors, further confirming the type I nature of the neurons transiently expressing the enzyme. The end of the tyrosine hydroxylase expression was not due to cell death because the immunoreactive neurons did not show TUNEL-labelled nuclei. Finally, all the type I neurons expressed the tyrosine hydroxylase mRNA at postnatal day 12, suggesting that the expression of the enzyme is a maturational step common to all these neurons and that the expression of the protein is not synchronized. Because the period of transient expression of tyrosine hydroxylase in type I neurons parallels the periods of maturation of evoked exocytosis in inner hair cells and of appearance and maturation of the cochlear potentials, we propose that the expression of the enzyme indicates the onset of hearing in individual type I primary auditory neurons. This enzyme expression could rely on a Ca2+ activation of its encoding gene subsequent to a sudden and massive Ca2+ entry through voltage-activated Ca2+ channels.

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