scholarly journals Outer hair cell electromotility is low-pass filtered relative to the molecular conformational changes that produce nonlinear capacitance

2019 ◽  
Vol 151 (12) ◽  
pp. 1369-1385 ◽  
Author(s):  
Joseph Santos-Sacchi ◽  
Kuni H. Iwasa ◽  
Winston Tan
Keyword(s):  
Guinea Pig ◽  
Hair Cell ◽  
Frequency Response ◽  
Time Constant ◽  
Outer Hair Cell ◽  
Resting Potential ◽  
Nonlinear Capacitance ◽  
Cochlear Amplification ◽  
Low Pass ◽  
Length Changes

The outer hair cell (OHC) of the organ of Corti underlies a process that enhances hearing, termed cochlear amplification. The cell possesses a unique voltage-sensing protein, prestin, that changes conformation to cause cell length changes, a process termed electromotility (eM). The prestin voltage sensor generates a capacitance that is both voltage- and frequency-dependent, peaking at a characteristic membrane voltage (Vh), which can be greater than the linear capacitance of the OHC. Accordingly, the OHC membrane time constant depends upon resting potential and the frequency of AC stimulation. The confounding influence of this multifarious time constant on eM frequency response has never been addressed. After correcting for this influence on the whole-cell voltage clamp time constant, we find that both guinea pig and mouse OHC eM is low pass, substantially attenuating in magnitude within the frequency bandwidth of human speech. The frequency response is slowest at Vh, with a cut-off, approximated by single Lorentzian fits within that bandwidth, near 1.5 kHz for the guinea pig OHC and near 4.3 kHz for the mouse OHC, each increasing in a U-shaped manner as holding voltage deviates from Vh. Nonlinear capacitance (NLC) measurements follow this pattern, with cut-offs about double that for eM. Macro-patch experiments on OHC lateral membranes, where voltage delivery has high fidelity, confirms low pass roll-off for NLC. The U-shaped voltage dependence of the eM roll-off frequency is consistent with prestin’s voltage-dependent transition rates. Modeling indicates that the disparity in frequency cut-offs between eM and NLC may be attributed to viscoelastic coupling between prestin’s molecular conformations and nanoscale movements of the cell, possibly via the cytoskeleton, indicating that eM is limited by the OHC’s internal environment, as well as the external environment. Our data suggest that the influence of OHC eM on cochlear amplification at higher frequencies needs reassessment.

Effectiveness, Active Energy Produced by Molecular Motors, and Nonlinear Capacitance of the Cochlear Outer Hair Cell

2005 ◽  
Vol 127 (3) ◽  
pp. 391-399 ◽  
Author(s):  
Alexander A. Spector
Keyword(s):  
Hair Cell ◽  
Molecular Motors ◽  
Outer Hair Cell ◽  
Molecular Motor ◽  
Force Production ◽  
Outer Hair Cells ◽  
Nonlinear Capacitance ◽  
Effective Capacitance ◽  
Capacitive Properties ◽  
Length Changes

Cochlear outer hair cells are crucial for active hearing. These cells have a unique form of motility, named electromotility, whose main features are the cell’s length changes, active force production, and nonlinear capacitance. The molecular motor, prestin, that drives outer hair cell electromotility has recently been identified. We reveal relationships between the active energy produced by the outer hair cell molecular motors, motor effectiveness, and the capacitive properties of the cell membrane. We quantitatively characterize these relationships by introducing three characteristics: effective capacitance, zero-strain capacitance, and zero-resultant capacitance. We show that zero-strain capacitance is smaller than zero-resultant capacitance, and that the effective capacitance is between the two. It was also found that the differences between the introduced capacitive characteristics can be expressed in terms of the active energy produced by the cell’s molecular motors. The effectiveness of the cell and its molecular motors is introduced as the ratio of the motors’ active energy to the energy of the externally applied electric field. It is shown that the effectiveness is proportional to the difference between zero-strain and zero-resultant capacitance. We analyze the cell and motor’s effectiveness within a broad range of cellular parameters and estimate it to be within a range of 12%–30%.

scholarly journals Prestin-Driven Cochlear Amplification Is Not Limited by the Outer Hair Cell Membrane Time Constant

Neuron ◽  
2011 ◽  
Vol 70 (6) ◽  
pp. 1143-1154 ◽  
Author(s):  
Stuart L. Johnson ◽  
Maryline Beurg ◽  
Walter Marcotti ◽  
Robert Fettiplace
Keyword(s):  
Cell Membrane ◽  
Hair Cell ◽  
Time Constant ◽  
Outer Hair Cell ◽  
Membrane Time Constant ◽  
Cochlear Amplification

scholarly journals State dependent effects on the frequency response of prestin’s real and imaginary components of nonlinear capacitance

2021 ◽  
Vol 11 (1) ◽  
Author(s):  
Joseph Santos-Sacchi ◽  
Dhasakumar Navaratnam ◽  
Winston J. T. Tan
Keyword(s):  
Frequency Response ◽  
Outer Hair Cell ◽  
Absolute Magnitude ◽  
Total Charge ◽  
Charge Movement ◽  
Membrane Tension ◽  
Nonlinear Capacitance ◽  
Complex Component ◽  
Trade Offs ◽  
Voltage Dependent

AbstractThe outer hair cell (OHC) membrane harbors a voltage-dependent protein, prestin (SLC26a5), in high density, whose charge movement is evidenced as a nonlinear capacitance (NLC). NLC is bell-shaped, with its peak occurring at a voltage, Vh, where sensor charge is equally distributed across the plasma membrane. Thus, Vh provides information on the conformational state of prestin. Vh is sensitive to membrane tension, shifting to positive voltage as tension increases and is the basis for considering prestin piezoelectric (PZE). NLC can be deconstructed into real and imaginary components that report on charge movements in phase or 90 degrees out of phase with AC voltage. Here we show in membrane macro-patches of the OHC that there is a partial trade-off in the magnitude of real and imaginary components as interrogation frequency increases, as predicted by a recent PZE model (Rabbitt in Proc Natl Acad Sci USA 17:21880–21888, 2020). However, we find similar behavior in a simple 2-state voltage-dependent kinetic model of prestin that lacks piezoelectric coupling. At a particular frequency, Fis, the complex component magnitudes intersect. Using this metric, Fis, which depends on the frequency response of each complex component, we find that initial Vh influences Fis; thus, by categorizing patches into groups of different Vh, (above and below − 30 mV) we find that Fis is lower for the negative Vh group. We also find that the effect of membrane tension on complex NLC is dependent, but differentially so, on initial Vh. Whereas the negative group exhibits shifts to higher frequencies for increasing tension, the opposite occurs for the positive group. Despite complex component trade-offs, the low-pass roll-off in absolute magnitude of NLC, which varies little with our perturbations and is indicative of diminishing total charge movement, poses a challenge for a role of voltage-driven prestin in cochlear amplification at very high frequencies.

The location and mechanism of electromotility in guinea pig outer hair cells

1993 ◽  
Vol 70 (2) ◽  
pp. 549-558 ◽  
Author(s):  
R. Hallworth ◽  
B. N. Evans ◽  
P. Dallos
Keyword(s):  
Guinea Pig ◽  
Hair Cells ◽  
Outer Hair Cell ◽  
Length Change ◽  
Opposite Polarity ◽  
Outer Hair Cells ◽  
Response Amplitude ◽  
Change Function ◽  
Length Changes ◽  
Diameter Change

1. The microchamber method was used to examine the motile responses of isolated guinea pig outer hair cells to electrical stimulation. In the microchamber method, an isolated cell is drawn partway into a suction pipette and stimulated transcellularly. The relative position of the cell in the microchamber is referred to as the exclusion fraction. 2. The length changes of the included and excluded segments were compared for constant sinusoidal stimulus amplitude as functions of the exclusion fraction. Both included and excluded segments showed maximal responses when the cell was excluded approximately halfway. Both segments showed smaller or absent responses when the cell was almost fully excluded or almost fully included. 3. When the cell was near to, but not at, the maximum exclusion, the included segment response amplitude was zero, whereas the excluded segment response amplitude was nonzero. In contrast, when the cell was nearly fully included, the excluded segment response amplitude was zero, but the included segment response amplitude was still detectable. A simple model of outer hair cell motility based on these results suggests that the cell has finite-resistance terminations and that the motors are restricted to a region above the nucleus and below its ciliated apex (cuticular plate). 4. The function describing length change as a function of command voltage was measured for each segment as the exclusion fraction was varied. The functions were similar at midrange exclusions (i.e., when the segments were about equal length), showing nonlinearity and saturability. The functions were strikingly different when the segment lengths were different. The effects of exclusion on the voltage to length-change functions suggested that the nonlinearity and saturability are local properties of the motility mechanism. 5. The diameter changes of both segments were examined. The segment diameter changes were always antiphasic to the length changes. This finding implies that the motility mechanism has an active antiphasic diameter component. The diameter change amplitude was a monotonically increasing function of exclusion for the included segment, and a decreasing function for the excluded segment. 6. The voltage to length-change and voltage to diameter-change functions were measured for the same cell and exclusion fraction. The voltage to diameter-change function was smaller in amplitude than the voltage to length-change function. The functions were of opposite polarity to each other, but were otherwise similar in character. Thus it is likely that the same motor mechanism is responsible for both axial and diameter deformations.

Effect of Neuroregulators on the Intracellular Calcium Level in the Outer Hair Cell Isolated from the Guinea Pig

ORL ◽  
1991 ◽  
Vol 53 (2) ◽  
pp. 78-81 ◽  
Author(s):  
Katsuhisa Ikeda ◽  
Yoshitaka Saito ◽  
Akinori Nishiyama ◽  
Tomonori Takasaka
Keyword(s):  
Guinea Pig ◽  
Hair Cell ◽  
Intracellular Calcium ◽  
Calcium Level ◽  
Outer Hair Cell ◽  
Intracellular Calcium Level

scholarly journals In Vivo Outer Hair Cell Length Changes Expose the Active Process in the Cochlea

PLoS ONE ◽  
2012 ◽  
Vol 7 (4) ◽  
pp. e32757 ◽  
Author(s):  
Dingjun Zha ◽  
Fangyi Chen ◽  
Sripriya Ramamoorthy ◽  
Anders Fridberger ◽  
Niloy Choudhury ◽  
...  
Keyword(s):  
Hair Cell ◽  
Outer Hair Cell ◽  
Cell Length ◽  
Active Process ◽  
Length Changes

Mechanosensitive Channels in the Lateral Wall Can Enhance the Cochlear Outer Hair Cell Frequency Response

2005 ◽  
Vol 33 (8) ◽  
pp. 991-1002 ◽  
Author(s):  
Alexander A. Spector ◽  
Aleksander S. Popel ◽  
Ruth Anne Eatock ◽  
William E. Brownell
Keyword(s):  
Hair Cell ◽  
Frequency Response ◽  
Outer Hair Cell ◽  
Lateral Wall ◽  
Mechanosensitive Channels ◽  
Cell Frequency
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