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The Journal of Neuroscience, June 7, 2006, 26(23):6181-6189; doi:10.1523/JNEUROSCI.1047-06.2006

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Cellular/Molecular
The Role of BK_Ca Channels in Electrical Signal Encoding in the Mammalian Auditory Periphery

Dominik Oliver,¹ Annette M. Taberner,^2,3 Henrike Thurm,¹ Matthias Sausbier,⁴ Claudia Arntz,⁴ Peter Ruth,⁴ Bernd Fakler,¹ and M. Charles Liberman^2,3

¹Physiologisches Institut, Universität Freiburg, D-79104 Freiburg, Germany, ²Eaton-Peabody Laboratory, Massachusetts Eye and Ear Infirmary, Boston, Massachusetts 02114, ³Program in Speech and Hearing Bioscience and Technology, Harvard University–Massachusetts Institute of Technology, Cambridge, Massachusetts 02139, and ⁴Department of Pharmacology and Toxicology, Universität Tübingen, D-72074 Tübingen, Germany

Correspondence should be addressed to Dr. Dominik Oliver, Physiologisches Institut, Universität Freiburg, Hermann-Herder-Strasse 7, 79104 Freiburg, Germany. Email: dominik.oliver{at}physiologie.uni-freiburg.de

Large-conductance voltage- and Ca²⁺-activated K⁺ channels (BK_Ca) are involved in shaping spiking patterns in many neurons. Less is known about their role in mammalian inner hair cells (IHCs), mechanosensory cells with unusually large BK_Ca currents. These currents may be involved in shaping the receptor potential, implying crucial importance for the properties of afferent auditory signals.

We addressed the function of BK_Ca by recording sound-induced responses of afferent auditory nerve (AN) fibers from mice with a targeted deletion of the pore-forming -subunit of BK_Ca (BK^–/–) and comparing these with voltage responses of current-clamped IHCs. BK_Ca-mediated currents in IHCs were selectively abolished in BK^–/–, whereas cochlear physiology was essentially normal with respect to cochlear sensitivity and frequency tuning.

BK^–/– AN fibers showed deteriorated precision of spike timing, measured as an increased variance of first spike latency in response to tone bursts. This impairment could be explained by a slowed voltage response in the presynaptic IHC resulting from the reduced K⁺ conductance in the absence of BK_Ca. Maximum spike rates of AN fibers were reduced nearly twofold in BK^–/–, contrasting with increased voltage responses of IHCs. In addition to presynaptic changes, which may be secondary to a modest depolarization of BK^–/– IHCs, this reduction in AN rates suggests a role of BK_Ca in postsynaptic AN neurons, which was supported by increased refractory periods.

In summary, our results indicate an essential role of IHC BK_Ca channels for precise timing of high-frequency cochlear signaling as well as a function of BK_Ca in the primary afferent neuron.

Key words: calcium-activated potassium channel; Maxi-K; inner ear; hearing; frequency tuning; adaptation

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Received Nov. 17, 2005; revised April 24, 2006; accepted April 24, 2006.

Correspondence should be addressed to Dr. Dominik Oliver, Physiologisches Institut, Universität Freiburg, Hermann-Herder-Strasse 7, 79104 Freiburg, Germany. Email: dominik.oliver{at}physiologie.uni-freiburg.de

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