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      Hair Cell Bundles: Flexoelectric Motors of the Inner Ear

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          Abstract

          Microvilli (stereocilia) projecting from the apex of hair cells in the inner ear are actively motile structures that feed energy into the vibration of the inner ear and enhance sensitivity to sound. The biophysical mechanism underlying the hair bundle motor is unknown. In this study, we examined a membrane flexoelectric origin for active movements in stereocilia and conclude that it is likely to be an important contributor to mechanical power output by hair bundles. We formulated a realistic biophysical model of stereocilia incorporating stereocilia dimensions, the known flexoelectric coefficient of lipid membranes, mechanical compliance, and fluid drag. Electrical power enters the stereocilia through displacement sensitive ion channels and, due to the small diameter of stereocilia, is converted to useful mechanical power output by flexoelectricity. This motor augments molecular motors associated with the mechanosensitive apparatus itself that have been described previously. The model reveals stereocilia to be highly efficient and fast flexoelectric motors that capture the energy in the extracellular electro-chemical potential of the inner ear to generate mechanical power output. The power analysis provides an explanation for the correlation between stereocilia height and the tonotopic organization of hearing organs. Further, results suggest that flexoelectricity may be essential to the exquisite sensitivity and frequency selectivity of non-mammalian hearing organs at high auditory frequencies, and may contribute to the “cochlear amplifier” in mammals.

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          Most cited references55

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          A physiological place-frequency map of the cochlea in the CBA/J mouse.

          Genetically manipulated mice have gained a prominent role in in vivo research on development and function of the auditory system. A prerequisite for the interpretation of normal and abnormal structural and functional features of the inner ear is the exact knowledge of the cochlear place-frequency map. Using a stereotaxic approach to the projection site of the auditory nerve fibers in the cochlear nucleus, we succeeded in labelling physiologically characterized auditory nerve afferents and determined their peripheral innervation site in the cochlea. From the neuronal characteristic frequency (CF) and the innervation site in the organ of Corti a place-frequency map was established for characteristic frequencies between 7.2 and 61.8 kHz, corresponding to locations between 90% and 10% basilar membrane length (base = 0%, apex = 100%, mean length measured under the inner hair cells 5.13 mm). The relation between normalized distance from the base (d) and frequency (kHz) can be described by a simple logarithmic function: d(%) = 156.5-82.5 x log(f), with a slope of 1.25 mm/octave of frequency. The present map, recorded under physiological conditions, differs from earlier maps determined with different methods. The simple logarithmic place-frequency relation found in the mouse indicates that mice are acoustic generalists rather than specialists.
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            Prestin-based outer hair cell motility is necessary for mammalian cochlear amplification.

            It is a central tenet of cochlear neurobiology that mammalian ears rely on a local, mechanical amplification process for their high sensitivity and sharp frequency selectivity. While it is generally agreed that outer hair cells provide the amplification, two mechanisms have been proposed: stereociliary motility and somatic motility. The latter is driven by the motor protein prestin. Electrophysiological phenotyping of a prestin knockout mouse intimated that somatic motility is the amplifier. However, outer hair cells of knockout mice have significantly altered mechanical properties, making this mouse model unsatisfactory. Here, we study a mouse model without alteration to outer hair cell and organ of Corti mechanics or to mechanoelectric transduction, but with diminished prestin function. These animals have knockout-like behavior, demonstrating that prestin-based electromotility is required for cochlear amplification.
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              Muscular contraction.

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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2009
                22 April 2009
                : 4
                : 4
                : e5201
                Affiliations
                [1 ]Department of Bioengineering, University of Utah, Salt Lake City, Utah, United States of America
                [2 ]Department of Otolaryngology - H&NS, Baylor College of Medicine, Houston, Texas, United States of America
                [3 ]Marine Biological Laboratory, Woods Hole, Massachusetts, United States of America
                Mount Sinai School of Medicine, United States of America
                Author notes

                Conceived and designed the experiments: WEB RDR. Performed the experiments: KDB RDR. Analyzed the data: KDB RDR. Wrote the paper: KDB WEB RDR.

                Article
                09-PONE-RA-08265R1
                10.1371/journal.pone.0005201
                2668172
                19384413
                52b1053b-f8d0-4e36-a24a-b92926229635
                Breneman et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
                History
                : 16 January 2009
                : 16 March 2009
                Page count
                Pages: 9
                Categories
                Research Article
                Computational Biology
                Otolaryngology
                Biophysics/Macromolecular Assemblies and Machines
                Biophysics/Theory and Simulation
                Ecology/Physiological Ecology
                Neuroscience/Sensory Systems
                Neuroscience/Theoretical Neuroscience

                Uncategorized
                Uncategorized

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