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The Journal of Neuroscience, December 12, 2007, 27(50):13890-13902; doi:10.1523/JNEUROSCI.2159-07.2007

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Cellular/Molecular
Stepwise Morphological and Functional Maturation of Mechanotransduction in Rat Outer Hair Cells

Jessica Waguespack,^1,2 Felipe T. Salles,² Bechara Kachar,² and Anthony J. Ricci^1,2,3

¹Neuroscience Center, Louisiana State Health Sciences Center, New Orleans, Louisiana 70112, ²Laboratory of Cellular Biology, National Institute on Deafness and Other Communication Disorders, National Institutes of Health, Bethesda, Maryland 20892, and ³Department of Otolaryngology, Stanford University, Stanford, California 94305

Correspondence should be addressed to either of the following: Anthony J. Ricci, Department of Otolaryngology, Stanford University, 801 Welch Road, Stanford, CA 94305, Email: aricci{at}stanford.edu; or Bechara Kachar, Laboratory of Cellular Biology, National Institute on Deafness and Other Communication Disorders, National Institutes of Health, Bethesda, MD 20892, Email: kacharb{at}nidcd.nih.gov

Inner ear mechanosensory hair cells convert mechanical vibrations into electrical signals via the coordinated interaction of multiple proteins precisely positioned within the sensory hair bundle. Present work identifies the time course for the acquisition and maturation of mechanoelectric transduction (MET) in rat cochlea outer hair cells maintained in organotypic cultures. A spatiotemporal developmental progression was observed morphologically and functionally with basal cochlea maturation preceding apical cochlea by 2–3 d in all measured properties. The fraction of mechanosensitive cells increased rapidly, with a midpoint at postnatal day 0 for basal cells, and correlated with myosin IIIa immunoreactivity. MET current magnitude increased over several days. Adaptation lagged the onset of transduction by a day and matured more slowly, overlapping but preceding the rise in myosin Ic immunoreactivity. Less than 25% of myosin Ic expression was required for the mature adaptation response, suggesting multiple roles for this protein in hair bundle function. Directional sensitivity, lacking in immature responses, developed rapidly and correlated with the pruning of radial links and an increase in tenting of stereociliary tips. Morphological and electrophysiological data support a hypothesis in which key elements arrive independently at the site of MET, with a mature response occurring as membrane tension increases, likely by the increased tensioning of the tip link with the onset of adaptation. Organotypic cultures developed normal, tonotopically specific, MET response properties, suggesting that maturation was not influenced significantly by external factors such as innervation, endolymph, normal mechanical stimulation, or an intact organ of Corti.

Key words: outer hair cells; mechanoelectrical transduction; auditory; adaptation; myosin Ic; myosin IIIa; stereocilium links

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Received May 10, 2007; revised Nov. 2, 2007; accepted Nov. 3, 2007.

Correspondence should be addressed to either of the following: Anthony J. Ricci, Department of Otolaryngology, Stanford University, 801 Welch Road, Stanford, CA 94305, Email: aricci{at}stanford.edu; or Bechara Kachar, Laboratory of Cellular Biology, National Institute on Deafness and Other Communication Disorders, National Institutes of Health, Bethesda, MD 20892, Email: kacharb{at}nidcd.nih.gov

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