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The Journal of Neuroscience, March 28, 2007, 27(13):3503-3511; doi:10.1523/JNEUROSCI.5185-06.2007

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Development/Plasticity/Repair
Control of Hair Cell Excitability by Vestibular Primary Sensory Neurons

Aurore Brugeaud,¹ Cécile Travo,¹ Danielle Demêmes,¹ Marc Lenoir,¹ Jordi Llorens,² Jean-Luc Puel,¹ and Christian Chabbert¹

¹Institut National de la Santé et de la Recherche Médicale Unité 583, 34091 Montpellier, France, and ²Departament de Ciencies Fisiologiques II, Universitat de Barcelona, l'Hospitalet de Llobregat, 08907 Barcelona, Spain

Correspondence should be addressed to Dr. Christian Chabbert, Institut National de la Santé et de la Recherche Médicale Unité 583, Institut des Neurosciences de Montpellier, Equipe Physiopathologie et Thérapie de l'Oreille Interne, Groupe d'Etude des Désordres Vestibulaires, Hôpital St. Eloi, 34091 Montpellier cedex 5, France. Email: chabbert{at}univ-montp2.fr

In the rat utricle, synaptic contacts between hair cells and the nerve fibers arising from the vestibular primary neurons form during the first week after birth. During that period, the sodium-based excitability that characterizes neonate utricle sensory cells is switched off. To investigate whether the establishment of synaptic contacts was responsible for the modulation of the hair cell excitability, we used an organotypic culture of rat utricle in which the setting of synapses was prevented. Under this condition, the voltage-gated sodium current and the underlying action potentials persisted in a large proportion of nonafferented hair cells. We then studied whether impairment of nerve terminals in the utricle of adult rats may also affect hair cell excitability. We induced selective and transient damages of afferent terminals using glutamate excitotoxicity in vivo. The efficiency of the excitotoxic injury was attested by selective swellings of the terminals and underlying altered vestibular behavior. Under this condition, the sodium-based excitability transiently recovered in hair cells. These results indicate that the modulation of hair cell excitability depends on the state of the afferent terminals. In adult utricle hair cells, this property may be essential to set the conditions required for restoration of the sensory network after damage. This is achieved via re-expression of a biological process that occurs during synaptogenesis.

Key words: voltage-gated sodium channel; hair cells; utricle; excitability; development; excitotoxicity; nerve impairment; repair

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Received July 27, 2006; revised Feb. 15, 2007; accepted Feb. 16, 2007.

Correspondence should be addressed to Dr. Christian Chabbert, Institut National de la Santé et de la Recherche Médicale Unité 583, Institut des Neurosciences de Montpellier, Equipe Physiopathologie et Thérapie de l'Oreille Interne, Groupe d'Etude des Désordres Vestibulaires, Hôpital St. Eloi, 34091 Montpellier cedex 5, France. Email: chabbert{at}univ-montp2.fr

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