scholarly journals Steady-state stiffness of utricular hair cells depends on macular location and hair bundle structure

2011 ◽  
Vol 106 (6) ◽  
pp. 2950-2963 ◽  
Author(s):  
Corrie Spoon ◽  
W. J. Moravec ◽  
M. H. Rowe ◽  
J. W. Grant ◽  
E. H. Peterson
Keyword(s):  
Steady State ◽  
Hair Cells ◽  
Head Movement ◽  
Time Course ◽  
Hair Bundle ◽  
Type I ◽  
Response Dynamics ◽  
Functional Interpretation ◽  
Hair Bundles ◽  
Bundle Structure

Spatial and temporal properties of head movement are encoded by vestibular hair cells in the inner ear. One of the most striking features of these receptors is the orderly structural variation in their mechanoreceptive hair bundles, but the functional significance of this diversity is poorly understood. We tested the hypothesis that hair bundle structure is a significant contributor to hair bundle mechanics by comparing structure and steady-state stiffness of 73 hair bundles at varying locations on the utricular macula. Our first major finding is that stiffness of utricular hair bundles varies systematically with macular locus. Stiffness values are highest in the striola, near the line of hair bundle polarity reversal, and decline exponentially toward the medial extrastriola. Striolar bundles are significantly more stiff than those in medial (median: 8.9 μN/m) and lateral (2.0 μN/m) extrastriolae. Within the striola, bundle stiffness is greatest in zone 2 (106.4 μN/m), a band of type II hair cells, and significantly less in zone 3 (30.6 μN/m), which contains the only type I hair cells in the macula. Bathing bundles in media that break interciliary links produced changes in bundle stiffness with predictable time course and magnitude, suggesting that links were intact in our standard media and contributed normally to bundle stiffness during measurements. Our second major finding is that bundle structure is a significant predictor of steady-state stiffness: the heights of kinocilia and the tallest stereocilia are the most important determinants of bundle stiffness. Our results suggest 1) a functional interpretation of bundle height variability in vertebrate vestibular organs, 2) a role for the striola in detecting onset of head movement, and 3) the hypothesis that differences in bundle stiffness contribute to diversity in afferent response dynamics.

Autocorrelation Analysis of Hair Bundle Structure in the Utricle

2006 ◽  
Vol 96 (5) ◽  
pp. 2653-2669 ◽  
Author(s):  
M. H. Rowe ◽  
E. H. Peterson
Keyword(s):  
Hair Cell ◽  
Hair Cells ◽  
Cell Types ◽  
Head Movements ◽  
Type I ◽  
Autocorrelation Analysis ◽  
Response Dynamics ◽  
Hair Bundles ◽  
Vestibular Organs ◽  
Bundle Structure

The ability of hair bundles to signal head movements and sounds depends significantly on their structure, but a quantitative picture of bundle structure has proved elusive. The problem is acute for vestibular organs because their hair bundles exhibit complex morphologies that vary with endorgan, hair cell type, and epithelial locus. Here we use autocorrelation analysis to quantify stereociliary arrays (the number, spacing, and distribution of stereocilia) on hair cells of the turtle utricle. Our first goal was to characterize zonal variation across the macula, from medial extrastriola, through striola, to lateral extrastriola. This is important because it may help explain zonal variation in response dynamics of utricular hair cells and afferents. We also use known differences in type I and II bundles to estimate array characteristics of these two hair cell types. Our second goal was to quantify variation in array orientation at single macular loci and use this to estimate directional tuning in utricular afferents. Our major findings are that, of the features measured, array width is the most distinctive feature of striolar bundles, and within the striola there are significant, negatively correlated gradients in stereocilia number and spacing that parallel gradients in bundle heights. Together with previous results on stereocilia number and bundle heights, our results support the hypothesis that striolar hair cells are specialized to signal high-frequency/acceleration head movements. Finally, there is substantial variation in bundle orientation at single macular loci that may help explain why utricular afferents respond to stimuli orthogonal to their preferred directions.

scholarly journals ELMOD1 stimulates ARF6-GTP hydrolysis to stabilize apical structures in developing vestibular hair cells

2017 ◽  
Author(s):  
Jocelyn F. Krey ◽  
Rachel A. Dumont ◽  
Philip A. Wilmarth ◽  
Larry L. David ◽  
Kenneth R. Johnson ◽  
...  
Keyword(s):  
Hair Cells ◽  
Membrane Trafficking ◽  
Apical Membrane ◽  
Small Gtpase ◽  
Hair Bundle ◽  
Type I ◽  
Sensory Hair ◽  
Cuticular Plate ◽  
Sensory Hair Cells ◽  
Hair Bundles

AbstractSensory hair cells require control of physical properties of their apical plasma membranes for normal development and function. Members of the ARF small GTPase family regulate membrane trafficking and cytoskeletal assembly in many cells. We identified ELMOD1, a guanine nucleoside triphosphatase activating protein (GAP) for ARF6, as the most highly enriched ARF regulator in hair cells. To characterize ELMOD1 control of trafficking, we used a mouse strain lacking functional ELMOD1 (roundabout; rda). In rda/rda mice, cuticular plates of utricle hair cells initially formed normally, then degenerated after postnatal day 5 (P5); large numbers of vesicles invaded the compromised cuticular plate. Hair bundles initially developed normally, but the cell’s apical membrane lifted away from the cuticular plate, and stereocilia elongated and fused. Membrane trafficking in type I hair cells, measured by FM1-43 dye labeling, was altered in rda/rda mice. Consistent with the proposed GAP role for ELMOD1, the ARF6 GTP/GDP ratio was significantly elevated in rda/rda utricles as compared to controls, and the level of ARF6-GTP was correlated with the severity of the rda/rda phenotype. These results suggest that conversion of ARF6 to its GDP-bound form is necessary for final stabilization of the hair bundle.Significance StatementAssembly of the mechanically sensitive hair bundle of sensory hair cells requires growth and reorganization of apical actin and membrane structures. Hair bundles and apical membranes in mice with mutations in the Elmod1 gene degenerate after formation, suggesting that the ELMOD1 protein stabilizes these structures. We show that ELMOD1 is a GTPase-activating protein in hair cells for the small GTP-binding protein ARF6, known to participate in actin assembly and membrane trafficking. We propose that conversion of ARF6 into the GDP-bound form in the apical domain of hair cells is essential for stabilizing apical actin structures like the hair bundle and ensuring that the apical membrane forms appropriately around the stereocilia.

Vestibular Type I and Type II Hair Cells. 2: Morphometric Comparisons of Dissociated Pigeon Hair Cells

1997 ◽  
Vol 7 (5) ◽  
pp. 407-420
Author(s):  
Anthony J. Ricci ◽  
Stephen L. Cochran ◽  
Katherine J. Rennie ◽  
Manning J. Correia
Keyword(s):  
Hair Cells ◽  
Semicircular Canals ◽  
Columba Livia ◽  
Hair Bundle ◽  
Type I ◽  
Type Ii ◽  
Cell Groups ◽  
Hair Bundles

Morphometric properties of solitary hair cells dissociated from the semicircular canals (SCC), utricles (UTR), and lagenas (LAG) of adult white king pigeons, Columba livia, were compared. Measurements were made of the cell body, cuticular plate and hair bundle. Cells were divided into two groups: type 1 (group 1) was predominantly type I hair cells, and type 2 (group 3) was primarily type II hair cells. Comparisons are made initially between end organs for each group. A subpopulation of short otolith hair cells was identified. Quantitative comparisons between isolated type 1 and type 2 hair cells demonstrated that type 1 hair cells were more homogeneous both within and between vestibular end organs; while they had shorter, thinner neck regions, narrower apical surfaces, with longer and thinner bodies than did type 2 hair cells. Generally, for both type 1 and type 2 hair cells, two different hair bundle shapes were present, those (unimodal) with a single sharp taper from longest to shortest stereocilia, and those (bimodal) with an initial steep tape-followed by a less steep taper. An additional subtype of type 1 hair cells with short hair bundles was identified. SCC hair cells have fewer hair bundles with bimodal tapers across all cell groups when compared to UTR or LAG. All cell subtypes identified for dissociated hair cells were corroborated using histologic sections.

A delayed rectifier conductance in type I hair cells of the mouse utricle

1996 ◽  
Vol 76 (2) ◽  
pp. 995-1004 ◽  
Author(s):  
A. Rusch ◽  
R. A. Eatock
Keyword(s):  
Hair Cells ◽  
Time Course ◽  
Dissociation Constants ◽  
Resting Potential ◽  
Delayed Rectifier ◽  
Type I ◽  
Type Ii ◽  
Voltage Range ◽  
Average Maximum

1. Membrane currents of hair cells in acutely excised or cultured mouse utricles were recorded with the whole cell voltage-clamp method at temperatures between 23 and 36 degrees C. 2. Type I and II hair cells both had delayed rectifier conductances that activated positive to -55 mV. 3. Type I, but not type II, hair cells had an additional delayed rectifier conductance (gK,L) with an activation range that was unusually negative and variable. At 23-25 degrees C, V(1/2) values ranged from -88 to -62 mV in 57 cells. 4. gK,L was very large. At 23-25 degrees C, the average maximum chord conductance was 75 +/- 65 nS (mean +/- SD, n = 57; measured at -54 mV), or approximately 21 nS/pF of cell capacitance. 5. gK,L was highly selective for K+ over Na+ (permeability ratio PNa+/PK+:0.006), but unlike other delayed rectifiers, gK,L was significantly permeable to Cs+ (PCs+/PK+:0.31). gK,L was independent of extracellular Ca2+. 6. At -64 mV, Ba2+ and 4-aminopyridine blocked gK,L with apparent dissociation constants of 2.0 mM and 43 microM, respectively. Extracellular Cs+ (5 mM) blocked gK,L by 50% at -124 mV. Apamin (100 nM) and dendrotoxin (10 nM) has no effect. 7. The kinetic data of gK,L are consistent with a sequential gating model with at least two closed states and one open state. The slow activation kinetics (principal time constants at 23-25 degrees C:600-200 ms) had a thermal Q10 of 2.1. Inactivation (Q10:2.7) was partial at all temperatures. Deactivation followed a double-exponential time course and had a Q10 of 2.0. 8. At 23-25 degrees C, gK,L was appreciably activated at the mean resting potential of type I hair cells (-77 +/- 3.1 mV, n = 62), so that input conductances were often more than an order of magnitude larger than those of type II cells. If these conditions hold in vivo, type I cells would produce unusually small receptor potentials. Warming the cells to 36 degrees C produced parallel shifts in gK,L's activation range (0.8 +/- 0.3 mV/degrees C, n = 8), and in the resting potential (0.6 +/- 0.3 mV/degrees C, n = 4). Thus the high input conductances were not an artifact of unphysiological temperatures but remained high near body temperature. It remains possible that in vivo gK,L's activation range is less negative and input conductances are lower; the large variance in the voltage range of activation suggests that it may be subject to modulation.

scholarly journals The calcium-activated potassium channels of turtle hair cells.

1995 ◽  
Vol 105 (1) ◽  
pp. 49-72 ◽  
Author(s):  
J J Art ◽  
Y C Wu ◽  
R Fettiplace
Keyword(s):  
Resonant Frequency ◽  
Time Constant ◽  
Hair Cells ◽  
Time Course ◽  
Voltage Dependence ◽  
Bk Channels ◽  
Hair Bundle ◽  
Sk Channels ◽  
Channel Kinetics ◽  
Ca Current

A major factor determining the electrical resonant frequency of turtle cochlear hair cells is the time course of the Ca-activated K current (Art, J. J., and R. Fettiplace. 1987. Journal of Physiology. 385:207-242). We have examined the notion that this time course is dictated by the K channel kinetics by recording single Ca-activated K channels in inside-out patches from isolated cells. A hair cell's resonant frequency was estimated from its known correlation with the dimensions of the hair bundle. All cells possess BK channels with a similar unit conductance of approximately 320 pS but with different mean open times of 0.25-12 ms. The time constant of relaxation of the average single-channel current at -50 mV in 4 microM Ca varied between cells from 0.4 to 13 ms and was correlated with the hair bundle height. The magnitude and voltage dependence of the time constant agree with the expected behavior of the macroscopic K(Ca) current, whose speed may thus be limited by the channel kinetics. All BK channels had similar sensitivities to Ca which produced half-maximal activation for a concentration of approximately 2 microM at +50 mV and 12 microM at -50 mV. We estimate from the voltage dependence of the whole-cell K(Ca) current that the BK channels may be fully activated at -35 mV by a rise in intracellular Ca to 50 microM. BK channels were occasionally observed to switch between slow and fast gating modes which raises the possibility that the range of kinetics of BK channels observed in different hair cells reflects a common channel protein whose kinetics are regulated by an unidentified intracellular factor. Membrane patches also contained 30 pS SK channels which were approximately 5 times more Ca-sensitive than BK channels at -50 mV. The SK channels may underlie the inhibitory synaptic potential produced in hair cells by efferent stimulation.

scholarly journals Dynamics of mechanically coupled hair-cell bundles of the inner ear

2020 ◽  
Author(s):  
Y. Roongthumskul ◽  
J. Faber ◽  
D. Bozovic
Keyword(s):  
Inner Ear ◽  
Auditory System ◽  
Hair Cells ◽  
Coupled System ◽  
Acoustic Energy ◽  
Hair Bundle ◽  
Free Standing ◽  
Physiological Level ◽  
Mechanical Coupling ◽  
Hair Bundles

ABSTRACTThe high sensitivity and effective frequency discrimination of sound detection performed by the auditory system rely on the dynamics of a system of hair cells. In the inner ear, these acoustic receptors are primarily attached to an overlying structure which provides mechanical coupling between the hair bundles. While the dynamics of individual hair bundles have been extensively investigated, the influence of mechanical coupling on the motility of the system of bundles remains underdetermined. We developed a technique of mechanically coupling two active hair bundles, enabling us to probe the dynamics of the coupled system experimentally. We demonstrated that the coupling could enhance the coherence of hair bundles’ spontaneous oscillation as well as their phase-locked response to sinusoidal stimuli, at the calcium concentration in the surrounding fluid near the physiological level. The empirical data were consistent with numerical results from a model of two coupled nonisochronous oscillators, each displaying a supercritical Hopf bifurcation. The model revealed that weak coupling can poise the system of unstable oscillators closer to the bifurcation by a shift in the critical point. In addition, the dynamics of strongly coupled oscillators far from criticality suggested that individual hair bundles may be regarded as nonisochronous oscillators. An optimal degree of nonisochronicity was required for the observed tuning behavior in the coherence of autonomous motion of the coupled system.STATEMENT OF SIGNIFICANCEHair cells of the inner ear transduce acoustic energy into electrical signals via a deflection of hair bundles. Unlike a passive mechanical antenna, a free-standing hair bundle behaves as an active oscillator that can sustain autonomous oscillations, as well as amplify a low-level stimulus. Hair bundles under physiological conditions are elastically coupled to each other via an extracellular matrix. Therefore, the dynamics of coupled nonlinear oscillators underlie the performance of the peripheral auditory system. Despite extensive theoretical investigations, there are limited experimental evidence that support the significance of coupling on hair bundle motility. We develop a technique to mechanically couple hair bundles and demonstrate the benefits of coupling on hair bundle spontaneous motility.

Time Course and Extent of Mechanotransducer Adaptation in Mouse Utricular Hair Cells: Comparison With Frog Saccular Hair Cells

2003 ◽  
Vol 90 (4) ◽  
pp. 2676-2689 ◽  
Author(s):  
Melissa A. Vollrath ◽  
Ruth Anne Eatock
Keyword(s):  
Hair Cells ◽  
Rise Time ◽  
Regional Variation ◽  
Time Course ◽  
Range Shift ◽  
Type I ◽  
Cell Type ◽  
Operating Range ◽  
Mean Time ◽  
Constant Percentage

Whole cell transduction currents were recorded from hair cells in early postnatal mouse utricles in response to step deflections of the hair bundle. For displacement steps delivered by a stiff probe (1-ms rise time), half-maximal responses decayed monoexponentially with a mean time constant of 30 ms. Adaptation and other transduction properties did not vary systematically with hair cell type (I vs. II) or region (striola vs. extrastriola). Thus regional variation in the phasic properties of utricular afferents arises through other mechanisms. When bundles were deflected by a fluid jet, which delivers force steps, transduction currents decayed about 3-fold more slowly than during displacement steps. A simple model of myosin-mediated adaptation predicts such slowing through forward creep of the bundle during a force step. For a faster stiff probe (rise time 200 μs), step responses of both mouse utricular and frog saccular hair cells decayed with two exponential components, which may correspond to distinct feedback processes. For half-maximal responses, the two components had mean time constants of 5 and 45 ms (mouse) and 2 and 18 ms (frog). The fast and slow components dominated the decay of responses to small and large stimuli, respectively. Adaptation shifts the instantaneous operating range in the direction of the adapting step. In frog saccular hair cells, the operating range shift is a constant percentage of the displacement. In mouse utricular hair cells, the percentage shift increases for large displacements, extending the range of background stimuli over which adaptation can restore instantaneous sensitivity.

Effects of KCNQ channel blockers on K+ currents in vestibular hair cells

2001 ◽  
Vol 280 (3) ◽  
pp. C473-C480 ◽  
Author(s):  
Katherine J. Rennie ◽  
Tianxiang Weng ◽  
Manning J. Correia
Keyword(s):  
Steady State ◽  
Hair Cells ◽  
Low Voltage ◽  
Dissociation Constants ◽  
Channel Blockers ◽  
Type I ◽  
Type Ii ◽  
Kcnq Channels ◽  
Vestibular Hair Cells ◽  
Inward Currents

Linopirdine and XE991, selective blockers of K+ channels belonging to the KCNQ family, were applied to hair cells isolated from gerbil vestibular system and to hair cells in slices of pigeon crista. In type II hair cells, both compounds inhibited a slowly activating, slowly inactivating component of the macroscopic current recruited at potentials above −60 mV. The dissociation constants for linopirdine and XE991 block were <5 μM. A similar component of the current was also blocked by 50 μM capsaicin in gerbil type II hair cells. All three drugs blocked a current component that showed steady-state inactivation and a biexponential inactivation with time constants of ∼300 ms and 4 s. Linopirdine (10 μM) reduced inward currents through the low-voltage-activated K+ current in type I hair cells, but concentrations up to 200 μM had little effect on steady-state outward K+ current in these cells. These results suggest that KCNQ channels may be present in amniote vestibular hair cells.

Functional Analysis of Whole Cell Currents From Hair Cells of the Turtle Posterior Crista

2002 ◽  
Vol 88 (6) ◽  
pp. 3279-3292 ◽  
Author(s):  
Jay M. Goldberg ◽  
Alan M. Brichta
Keyword(s):  
Hair Cells ◽  
Low Frequency ◽  
Type I ◽  
Type Ii Cells ◽  
Type Ii ◽  
Active Components ◽  
Response Dynamics ◽  
Steady Current ◽  
Slow Type ◽  
Sinusoidal Currents

Controlled currents were used to study possible functions of voltage-sensitive, outwardly rectifying conductances. Results were interpreted with linearized Hodgkin-Huxley theory. Because of their more hyperpolarized resting potentials and lower impedances, type I hair cells require larger currents to be depolarized to a given voltage than do type II hair cells. “Fast” type II cells, so-called because of the fast activation of their outward currents, show slightly underdamped responses to current steps with resonant (best) frequencies of 40–85 Hz, well above the bandwidth of natural head movements. Reflecting their slower activation kinetics, type I and “slow” type II cells have best frequencies of 15–30 Hz and are poorly tuned, being critically damped or overdamped. Linearized theory identified the factors responsible for tuning quality. Our fast type II hair cells show only modestly underdamped responses because their steady-state I-V curves are not particularly steep. The even poorer tuning of our type I and slow type II cells can be attributed to their slow activation kinetics and large conductances. To study how ionic currents shape response dynamics, we superimposed sinusoidal currents of 0.1–100 Hz on a small depolarizing steady current intended to simulate resting conditions in vivo. The steady current resulted in a slow inactivation, most pronounced in fast type II cells and least pronounced in type I cells. Because of inactivation, fast type II cells have nearly passive response dynamics with low-frequency gains of 500–1,000 MΩ. In contrast, type I and slow type II cells show active components in the vestibular bandwidth and low-frequency gains of 20–100 and 100–500 MΩ, respectively. As there are no differences in the responses to sinusoidal currents for fast type II cells from the torus and planum, voltage-sensitive currents are unlikely to be responsible for the large differences in gains and response dynamics of afferents innervating these two regions of the peripheral zone. The low impedances and active components of type I cells may be related to the low gains and modestly phasic response dynamics of calyx-bearing afferents.

Morphological Identification of Physiologically Characterized Afferents Innervating the Turtle Posterior Crista

2000 ◽  
Vol 83 (3) ◽  
pp. 1202-1223 ◽  
Author(s):  
Alan M. Brichta ◽  
Jay M. Goldberg
Keyword(s):  
Hair Cells ◽  
Central Zone ◽  
Peripheral Zone ◽  
Morphological Identification ◽  
Type I ◽  
Type Ii ◽  
Response Dynamics ◽  
Multivariate Statistical ◽  
Class B ◽  
Longitudinal Position

The turtle posterior crista consists of two hemicristae. Each hemicrista extends from the planum semilunatum to the nonsensory torus and includes a central zone (CZ) surrounded by a peripheral zone (PZ). Type I and type II hair cells are found in the CZ and are innervated by calyx, dimorphic and bouton afferents. Only type II hair cells and bouton fibers are found in the PZ. Units were intraaxonally labeled in a half-head preparation. Bouton (B) units could be near the planum (BP), near the torus (BT), or in midportions of a hemicrista, including the PZ and CZ. Discharge properties of B units vary with longitudinal position in a hemicrista but not with morphological features of their peripheral terminations. BP units are regularly discharging and have small gains and small phase leads re angular head velocity. BT units are irregular and have large gains and large phase leads. BM units have intermediate properties. Calyx (C) and dimorphic (D) units have similar discharge properties and were placed into a single calyx-bearing (CD) category. While having an irregular discharge resembling BT units, CD units have gains and phases similar to those of BM units. Rather than any single discharge property, it is the relation between discharge regularity and either gain or phase that makes CD units distinctive. Multivariate statistical formulas were developed to infer a unit's morphological class (B or CD) and longitudinal position solely from its discharge properties. To verify the use of the formulas, discharge properties were compared for units recorded intraaxonally or extracellularly in the half-head or extracellularly in intact animals. Most B units have background rates of 10–30 spikes/s. The CD category was separated into CD-high and CD-low units with background rates above or below 5 spikes/s, respectively. CD-low units have lower gains and phases and are located nearer the planum than CD-high units. In their response dynamics over a frequency range from 0.01–3 Hz, BP units conform to an overdamped torsion-pendulum model. Other units show departures from the model, including high-frequency gain increases and phase leads. The longitudinal gradient in the physiology of turtle B units resembles a similar gradient in the anamniote crista. In many respects, turtle CD units have discharge properties resembling those of calyx-bearing units in the mammalian central zone.

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