scholarly journals Complex nonlinear capacitance in outer hair cell macro-patches: effects of membrane tension

2020 ◽  
Vol 10 (1) ◽  
Author(s):  
Joseph Santos-Sacchi ◽  
Winston Tan
Keyword(s):  
Hair Cell ◽  
Outer Hair Cell ◽  
Membrane Tension ◽  
Nonlinear Capacitance

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.

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 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.

Temperature dependence of outer hair cell nonlinear capacitance

1998 ◽  
Vol 116 (1-2) ◽  
pp. 99-106 ◽  
Author(s):  
J Santos-Sacchi ◽  
Guojie Huang
Keyword(s):  
Hair Cell ◽  
Temperature Dependence ◽  
Outer Hair Cell ◽  
Nonlinear Capacitance

scholarly journals Quantitative Relations between Outer Hair Cell Electromotility and Nonlinear Capacitance

2012 ◽  
Vol 7 (1) ◽  
pp. 45-53
Author(s):  
Wang Xiang ◽  
Guo Wei–Wei ◽  
Yang Shi–Ming
Keyword(s):  
Hair Cell ◽  
Outer Hair Cell ◽  
Nonlinear Capacitance

A THEORETICAL STUDY OF NONLINEAR CAPACITANCE OF MAMMALIAN OUT HAIR CELL BY A NONTRANSPORTING FIVE-STATE MODEL

2012 ◽  
Vol 26 (13) ◽  
pp. 1250080
Author(s):  
LEI ZHANG ◽  
YONG ZHANG ◽  
CHUL KOO KIM ◽  
KONG-JU-BOCK LEE
Keyword(s):  
Equilibrium State ◽  
Hair Cell ◽  
Frequency Dependence ◽  
Theoretical Study ◽  
Outer Hair Cell ◽  
Peak Shift ◽  
State Model ◽  
Nonlinear Capacitance

Understanding the nonlinear capacitance (NLC) of prestin and outer hair cell (OHC) is important for exploring the activity of mammalian cochlea. After introducing a nontransporting five-state model of the OHC motor which is the tetramer of prestin, we obtain the peak of the NLC of OHC and the peak shift of the NLC as functions of the concentration of the intracellular Cl- anions. By employing the same model, we calculate the frequency dependence of the NLC as well. The model results both in equilibrium state and of the frequency dependence agree with the experimental observations. Accordingly, it suggests that the introduced five-state model is a candidate for exploring the NLC of both OHC and prestin.

Sign in / Sign up

Export Citation Format

Share Document