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The Journal of Neuroscience, September 8, 2004, 24(36):7814-7820; doi:10.1523/JNEUROSCI.2102-04.2004

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Cellular/Molecular
Developmental Regulation of Nicotinic Synapses on Cochlear Inner Hair Cells

Eleonora Katz,^1,2 Ana Belén Elgoyhen,¹ María E. Gómez-Casati,¹ Marlies Knipper,³ Douglas E. Vetter,⁴ Paul A. Fuchs,⁵ and Elisabeth Glowatzki⁵

¹Instituto de Investigaciones en Ingeniería Genética y Biología Molecular, Consejo Nacional de Investigaciones Científicas y Técnicas-Universidad de Buenos Aires (UBA), ²Departamento de Fisiología, Biología Molecular y Celular, Facultad de Ciencias Exactas y Naturales, UBA, 1428 Buenos Aires, Argentina, ³Hearing Research Center Tübingen, 72076 Tübingen, Germany, ⁴Department of Neuroscience, Tufts University School of Medicine, Boston, Massachusetts, and ⁵Department of Otolaryngology, Head and Neck Surgery, Johns Hopkins University, Baltimore, Maryland 21205-2195

In the mature cochlea, inner hair cells (IHCs) transduce acoustic signals into receptor potentials, communicating to the brain by synaptic contacts with afferent fibers. Before the onset of hearing, a transient efferent innervation is found on IHCs, mediated by a nicotinic cholinergic receptor that may contain both 9 and 10 subunits. Calcium influx through that receptor activates calcium-dependent (SK2-containing) potassium channels. This inhibitory synapse is thought to disappear after the onset of hearing [after postnatal day 12 (P12)]. We documented this developmental transition using whole-cell recordings from IHCs in apical turns of the rat organ of Corti. Acetylcholine elicited ionic currents in 88-100% of IHCs between P3 and P14, but in only 1 of 11 IHCs at P16-P22. Potassium depolarization of efferent terminals caused IPSCs in 67% of IHCs at P3, in 100% at P7-P9, in 93% at P10-P12, but in only 40% at P13-P14 and in none of the IHCs tested between P16 and P22. Earlier work had shown by in situ hybridization that 9 mRNA is expressed in adult IHCs but that10 mRNA disappears after the onset of hearing. In the present study, antibodies to10 and to the associated calcium-dependent (SK2) potassium channel showed a similar developmental loss. The correlated expression of these gene products with functional innervation suggests that Alpha10 and SK2, but not Alpha9, are regulated by synaptic activity. Furthermore, this developmental knock-out of 10, but not 9, supports the hypothesis that functional nicotinic acetylcholine receptors in hair cells are heteromers containing both these subunits.

Key words: IHC; mammalian cochlea; cholinergic; efferent innervation; 910 nAChR; transient synapse; Ca²⁺-activated K⁺ channel; neonatal development

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Received Feb 10, 2004; revised July 20, 2004; accepted July 20, 2004.

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