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The Journal of Neuroscience, November 29, 2006, 26(48):12526-12536; doi:10.1523/JNEUROSCI.3569-06.2006

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Cellular/Molecular
Steady-State Adaptation of Mechanotransduction Modulates the Resting Potential of Auditory Hair Cells, Providing an Assay for Endolymph [Ca²⁺]

Hamilton E. Farris,¹ Gregg B. Wells,² and Anthony J. Ricci¹

¹Center for Neuroscience and Kresge Hearing Laboratories, Louisiana State University Health Science Center, New Orleans, Louisiana 70112, and ²Department of Molecular and Cellular Medicine, College of Medicine, Texas A & M University System Health Science Center, College Station, Texas 77843-1114

Correspondence should be addressed to Hamilton E. Farris, Center for Neuroscience and Kresge Hearing Laboratories, Louisiana State University Health Science Center, 2020 Gravier Street, New Orleans, LA 70112. Email: hfarri{at}lsuhsc.edu

The auditory hair cell resting potential is critical for proper translation of acoustic signals to the CNS, because it determines their filtering properties, their ability to respond to stimuli of both polarities, and, because the hair cell drives afferent firing rates, the resting potential dictates spontaneous transmitter release. In turtle auditory hair cells, the filtering properties are established by the interactions between BK calcium-activated potassium channels and an L-type calcium channel (electrical resonance). However, both theoretical and in vitro recordings indicate that a third conductance is required to set the resting potential to a point on the I_Ca and I_BK activation curves in which filtering is optimized like that found in vivo. Present data elucidate a novel mechanism, likely universal among hair cells, in which mechanoelectric transduction (MET) and its calcium-dependent adaptation provide the depolarizing current to establish the hair cell resting potential. First, mechanical block of the MET current hyperpolarized the membrane potential, resulting in broadband asymmetrical resonance. Second, altering steady-state adaptation by altering the [Ca²⁺] bathing the hair bundle changed the MET current at rest, the magnitude of which resulted in membrane potential changes that encompassed the best resonant voltage. The Ca²⁺ sensitivity of adaptation allowed for the first physiological estimate of endolymphatic Ca²⁺ near the MET channel (56 ± 11 µM), a value similar to bulk endolymph levels. These effects of MET current on resting potential were independently confirmed using a theoretical model of electrical resonance that included the steady-state MET conductance.

Key words: resting potential; mechanoelectric transduction; auditory hair cells; calcium; adaptation; electrical resonance

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Received Aug. 17, 2006; revised Oct. 23, 2006; accepted Oct. 26, 2006.

Correspondence should be addressed to Hamilton E. Farris, Center for Neuroscience and Kresge Hearing Laboratories, Louisiana State University Health Science Center, 2020 Gravier Street, New Orleans, LA 70112. Email: hfarri{at}lsuhsc.edu

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