Ionic composition of endolymph and perilymph in the inner ear of the oyster toadfish, Opsanus tau

Author Posting. © Marine Biological Laboratory, 2008. This article is posted here by permission of Marine Biological Laboratory for personal use, not for redistribution. The definitive version was published in Biological Bulletin 214 (2008): 83-90.The concentrations of free Na+, K+, Ca2+, and Cl-in endolymph and perilymph from the inner ear of the oyster toadfish, Opsanus tau, were measured in vivo using double-barreled ion-selective electrodes. Perilymph concentrations were similar to those measured in other species, while endolymph concentrations were similar to those measured previously in elasmobranch fish, though significantly different from concentrations reported in mammals. Perilymph concentrations (mean ± std. dev.) were as follows: Na+, 129 mmol l-1 ± 20; K+, 4.96 mmol l-1 ± 2.67; Ca2+, 1.83 mmol l-1 ± 0.27; and Cl-, 171 mmol l-1 ± 20. Saccular endolymph concentrations were Na+, 166 mmol l-1 ± 22; K+, 51.4 mmol l-1 ± 16.7; Ca2+, 2.88 mmol l-1 ± 0.27; and Cl-, 170 mmol l-1 ± 12; and semicircular canal (utricular vestibule) endolymph concentrations were Na+, 122 mmol l-1 ± 15; K+, 47.7 mmol l-1 ± 13.2; Ca2+, 1.78 mmol l-1 ± 0.48; Cl-, 176 mmol l-1 ± 27. The relatively high concentrations of Ca2+ and Na+ in the endolymph may have significant implications for the physiological function of the mechanoelectrical transduction channels in the vestibular hair cells of fish compared to those of their mammalian counterparts.This work was supported by the National Institute of Deafness and Other Communications Disorders P01 DC01837, R01 DC06685, R01 DC04928, NASA NNA-04CK67H, and NSF Igert DGE9987616

Hair Cell Bundles: Flexoelectric Motors of the Inner Ear

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

Dynamic displacement of normal and detached semicircular canal cupula

© 2009 The Authors. This is an open-access article distributed under the terms of the Creative Commons Attribution Noncommercial License. The definitive version was published in JARO - Journal of the Association for Research in Otolaryngology 10 (2009): 497-509, doi:10.1007/s10162-009-0174-y.The dynamic displacement of the semicircular canal cupula and modulation of afferent nerve discharge were measured simultaneously in response to physiological stimuli in vivo. The adaptation time constant(s) of normal cupulae in response to step stimuli averaged 36 s, corresponding to a mechanical lower corner frequency for sinusoidal stimuli of 0.0044 Hz. For stimuli equivalent to 40–200 deg/s of angular head velocity, the displacement gain of the central region of the cupula averaged 53 nm per deg/s. Afferents adapted more rapidly than the cupula, demonstrating the presence of a relaxation process that contributes significantly to the neural representation of angular head motions by the discharge patterns of canal afferent neurons. We also investigated changes in time constants of the cupula and afferents following detachment of the cupula at its apex—mechanical detachment that occurs in response to excessive transcupular endolymph pressure. Detached cupulae exhibited sharply reduced adaptation time constants (300 ms–3 s, n = 3) and can be explained by endolymph flowing rapidly over the apex of the cupula. Partially detached cupulae reattached and normal afferent discharge patterns were recovered 5–7 h following detachment. This regeneration process may have relevance to the recovery of semicircular canal function following head trauma.Financial support was provided by the NIDCD R01 DC06685 (Rabbitt) and NASA GSRP 56000135 & NSF IGERT DGE- 9987616 (Breneman)

Power efficiency of outer hair cell somatic electromotility

© 2009 Rabbitt et al. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in PLoS Computational Biology 5 (2009): e1000444, doi:10.1371/journal.pcbi.1000444.Cochlear outer hair cells (OHCs) are fast biological motors that serve to enhance the vibration of the organ of Corti and increase the sensitivity of the inner ear to sound. Exactly how OHCs produce useful mechanical power at auditory frequencies, given their intrinsic biophysical properties, has been a subject of considerable debate. To address this we formulated a mathematical model of the OHC based on first principles and analyzed the power conversion efficiency in the frequency domain. The model includes a mixture-composite constitutive model of the active lateral wall and spatially distributed electro-mechanical fields. The analysis predicts that: 1) the peak power efficiency is likely to be tuned to a specific frequency, dependent upon OHC length, and this tuning may contribute to the place principle and frequency selectivity in the cochlea; 2) the OHC power output can be detuned and attenuated by increasing the basal conductance of the cell, a parameter likely controlled by the brain via the efferent system; and 3) power output efficiency is limited by mechanical properties of the load, thus suggesting that impedance of the organ of Corti may be matched regionally to the OHC. The high power efficiency, tuning, and efferent control of outer hair cells are the direct result of biophysical properties of the cells, thus providing the physical basis for the remarkable sensitivity and selectivity of hearing.This work was supported by NIDCD R01 DC04928 (Rabbitt), NIDCD R01 DC00384 (Brownell) and NASA Ames GSRA56000135 (Breneman)

Flexoelectric Work Cycle.

<p>During excitatory stimulation, the bundle is pushed towards the tallest stereocilium causing opening of the MET channel and an influx of depolarizing current. b) Under these conditions, flexoelectricity compels an increase in the curvature (decrease in the radius) and an isochoric increase in length resulting in an increase in the tip-link tension and bundle movement towards the applied bundle force. This is accompanied by MET adaptation and associated nonlinearities. d) As the stimulus moves in the inhibitory direction, hyperpolarizing MET current causes decreased stereocilium curvature, axial shortening, tip-link slackening, and further relaxation of the bundle in the direction of applied force.</p

Universal phylogenetic law.

<p>Raw data (symbols) showing the height of the tallest stereocilia for cochlear hair cells from mouse <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0005201#pone.0005201-Garfinkle1" target="_blank">[2]</a>, <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0005201#pone.0005201-Muller1" target="_blank">[44]</a>, human <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0005201#pone.0005201-Garfinkle1" target="_blank">[2]</a>, <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0005201#pone.0005201-Muller1" target="_blank">[44]</a>, guinea pig <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0005201#pone.0005201-Wright1" target="_blank">[45]</a>, mustached bat <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0005201#pone.0005201-Vater1" target="_blank">[46]</a>, chick <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0005201#pone.0005201-Tilney1" target="_blank">[47]</a>, alligator lizard <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0005201#pone.0005201-Mulroy1" target="_blank">[1]</a>, <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0005201#pone.0005201-Frishkopf1" target="_blank">[13]</a>, <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0005201#pone.0005201-Weiss2" target="_blank">[48]</a> and the basilar papilla of turtle <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0005201#pone.0005201-Hackney2" target="_blank">[49]</a>. Flexoelectric model predictions show the frequency of peak efficiency for stereocilia of different heights that impart power to accessory structures (e.g. TM) but lose power to the fluid, and for freestanding stereocilia that impart power to the fluid through viscous pumping alone.</p

Power Efficiency.

<p>a) Taxonomy of power conversion for 6 µm long stereocilia showing peak efficiency of conversion at a specific best frequency (*). Input electrical MET power is lost to conductance of the soma and lost due to intrinsic mechanical properties of the stereocilia, including axial stiffness at low frequencies and entrained mass at high frequencies. Efficiency is further limited at high frequencies primarily by transverse viscous drag (light blue hatch). b) Peak conversion efficiency is tuned, with the optimum frequency (, *) increasing as the stereocilia becomes shorter (3 lengths shown). Efficiencies are predicted to be higher for axial motion (dashed curves, , **) vs. transverse motion (solid curves, *). c) Power output is also predicted to be tuned with peak power occurring at a specific frequency (solid curves, , ***). Tuning is reduced if axial length changes are not coupled to cause transverse bundle motion (dashed curves).</p

Stereocilium flexoelectric biophysics.

<p>a) As an excitatory force is applied the bundle deflects towards the tallest stereocilia and the tip link tension increases. Tip displacement causes the MET to open, current (<i>I_T</i>) to enter the stereocilia, thus leading to cable-like membrane depolarization. b–c) Through the membrane flexoelectric effect, depolarization compels a decrease in radius () and increase in height () under constant volume. Changes in length are accompanied by transverse motion due to the staircase gradient in stereocilia lengths and diagonal tip links. Deflections are resisted by actin stiffness and polymerization at the tip, the angular stiffness at the base, and fluid drag in the axial and transverse directions.</p

Model coefficients and parameters.

<p>Model coefficients and parameters.</p

Nominal Physical Parameters.

<p>Nominal Physical Parameters.</p