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%.

Theory of electrically driven shape changes of cochlear outer hair cells

1993 ◽  
Vol 70 (1) ◽  
pp. 299-323 ◽  
Author(s):  
P. Dallos ◽  
R. Hallworth ◽  
B. N. Evans
Keyword(s):  
Cell Membrane ◽  
Hair Cell ◽  
Outer Hair Cell ◽  
Linear Motor ◽  
Outer Hair Cells ◽  
Pressure Effects ◽  
Model Parameters ◽  
Minor Importance ◽  
Length Changes ◽  
Shape Changes

1. A theory of cochlear outer hair cell electromotility is developed and specifically applied to somatic shape changes elicited in a microchamber. The microchamber permits the arbitrary electrical and mechanical partitioning of the outer hair cell along its length. This means that the two partitioned segments are stimulated with different input voltages and undergo different shape changes. Consequently, by imposing more constraints than other methods, experiments in the microchamber are particularly suitable for testing different theories of outer hair cell motility. 2. The present model is based on simple hypotheses. They include a distributed motor associated with the cell membrane or cortex and the assumption that the displacement generated by the motor is related to the transmembrane voltage across the associated membrane element. It is expected that the force generated by the motor is counterbalanced by an elastic restoring force indigenous to the cell membrane and cortex, and a tensile force due to intracellular pressure. It is assumed that all changes take place while total cell volume is conserved. The above elements of the theory taken together permit the development of qualitative and quantitative predictions about the expected motile responses of both partitioned segments of the cell. Only a DC treatment is offered here. 3. Both a linear motor and an expanded treatment that incorporates a stochastic molecular motor model are considered. The latter is represented by a two-state Boltzmann process. We show that the linear motor treatment is an appropriate extrapolation of the stochastic motor theory for the case of small voltage driving signals. Comparison of experimental results with model responses permits the estimation of model parameters. Good match of data is obtained if it is assumed that the molecular motors undergo conformational length changes of 0.7-1.0 nm, that they have an effective displacement vector at approximately -20 degrees with the long axis of the cell, and that their linear density is approximately 80/microns. 4. An effort is made to parcel out motile response components that are a direct consequence of the motor action from those that are mediated by cytoplasmic pressure changes brought about by the concerted action of the motors. We show that pressure effects are of minor importance, and thus rule out models that rely on radial constriction/expansion-mediated internal pressure change as the primary cause of longitudinal motility. 5. As a consequence of the interaction between the Boltzmann process and the mechanical characteristics of the cell, the electromotile response is asymmetric.(ABSTRACT TRUNCATED AT 400 WORDS)

Molecular Motor and Electrokinetic Contributions to Outer Hair Cell Electromotility

1998 ◽  
Vol 79 (1) ◽  
pp. 471-473 ◽  
Author(s):  
Rocco A. Jerry ◽  
Ashim Dutta
Keyword(s):  
Hair Cell ◽  
Molecular Motors ◽  
Outer Hair Cell ◽  
Motor Behavior ◽  
Molecular Motor ◽  
High Sensitivity ◽  
Length Change ◽  
The Novel ◽  
Sensitivity And Selectivity ◽  
A New Technique

Jerry, Rocco A. and Ashim Dutta. Molecular motor and electrokinetic contributions to outer hair cell electromotility. J. Neurophysiol. 79: 471–473, 1998. The outer hair cell of the inner ear is believed to be responsible for the high sensitivity and selectivity of mammalian hearing. Molecular motors are generally believed to cause the electrically-driven length change (electromotility) of the outer hair cell. It has been suggested that electrokinetic effects might also play a significant role in electromotility, along with the molecular motors. This paper describes a new technique that can be used to experimentally determine the percentage of the electromotile response that is caused by electrokinetic effects. The technique is based on the novel idea that molecular motor activity cannot in itself generate a net force on the cell, but that electrokinetic effects can. Our method is the first that can separate molecular motor behavior from electrokinetic behavior, during experiments on the outer hair cell.

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.

Modeling the Mechanics of Tethers Pulled From the Cochlear Outer Hair Cell Membrane

2008 ◽  
Vol 130 (3) ◽  
Author(s):  
Kristopher R. Schumacher ◽  
Aleksander S. Popel ◽  
Bahman Anvari ◽  
William E. Brownell ◽  
Alexander A. Spector
Keyword(s):  
Cell Membrane ◽  
Hair Cell ◽  
Outer Hair Cell ◽  
Lateral Wall ◽  
Outer Hair Cells ◽  
The Body ◽  
Computational Method ◽  
Membrane Properties ◽  
Bending Modulus ◽  
Sound Amplification

Cell membrane tethers are formed naturally (e.g., in leukocyte rolling) and experimentally to probe membrane properties. In cochlear outer hair cells, the plasma membrane is part of the trilayer lateral wall, where the membrane is attached to the cytoskeleton by a system of radial pillars. The mechanics of these cells is important to the sound amplification and frequency selectivity of the ear. We present a modeling study to simulate the membrane deflection, bending, and interaction with the cytoskeleton in the outer hair cell tether pulling experiment. In our analysis, three regions of the membrane are considered: the body of a cylindrical tether, the area where the membrane is attached and interacts with the cytoskeleton, and the transition region between the two. By using a computational method, we found the shape of the membrane in all three regions over a range of tether lengths and forces observed in experiments. We also analyze the effects of biophysical properties of the membrane, including the bending modulus and the forces of the membrane adhesion to the cytoskeleton. The model’s results provide a better understanding of the mechanics of tethers pulled from cell membranes.

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.

Molecular Motors: Force and Movement Generated by Single Myosin II Molecules

Physiology ◽  
2002 ◽  
Vol 17 (5) ◽  
pp. 213-218 ◽  
Author(s):  
Caspar Rüegg ◽  
Claudia Veigel ◽  
Justin E. Molloy ◽  
Stephan Schmitz ◽  
John C. Sparrow ◽  
...  
Keyword(s):  
Optical Tweezers ◽  
Single Molecule ◽  
Molecular Motors ◽  
Molecular Motor ◽  
Myosin Ii ◽  
Force Production ◽  
Myosin Isoforms ◽  
Single Molecule Level ◽  
Recent Developments ◽  
Muscle Myosin

Muscle myosin II is an ATP-driven, actin-based molecular motor. Recent developments in optical tweezers technology have made it possible to study movement and force production on the single-molecule level and to find out how different myosin isoforms may have adapted to their specific physiological roles.

Early Evidence of Cochlear Damage in a Large Sample of Percussionists

2005 ◽  
Vol 20 (3) ◽  
pp. 135-139
Author(s):  
Jodee A Pride ◽  
David R Cunningham
Keyword(s):  
Hearing Loss ◽  
Hair Cell ◽  
Otoacoustic Emissions ◽  
Outer Hair Cell ◽  
Cell Damage ◽  
Normal Hearing ◽  
Outer Hair Cells ◽  
Sensory Loss ◽  
Distortion Product ◽  
Hair Cell Damage

Percussionists can be exposed to intermittent sound stimuli that exceed 145 dB SPL, although damage may occur to the outer hair cells at levels of 120 dB SPL. The present study measured distortion-product otoacoustic emissions (DPOAEs) in a group of 86 normal-hearing percussionists and 39 normal-hearing nonpercussionists. Results indicate that normal-hearing percussionists have lower DPOAE amplitudes than normal-hearing nonpercussionists. DPOAE amplitudes were significantly lower at 6000 Hz in both the left and right ears for percussionists. Percussionists also more frequently had absent DPOAEs, with the greatest differences occurring at 6000 Hz (absent DPOAEs in 25% of percussionists vs 10% of nonpercussionists). When all frequencies are considered as a group, 33% of the percussionists had an absent DPOAE in either ear at some frequency, compared to only 23% of the nonpercussionists. Otoacoustic emissions are more sensitive to outer hair cell damage than pure-tone threshold measurements and can serve as an important measurement of sensory loss (i.e., outer hair cell damage) in musicians before the person perceives the hearing loss. DPOAE monitoring for musicians, along with appropriate education and intervention, might help prevent or minimize music-induced hearing loss.

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

A Dynamic Escape Problem of Molecular Motors

2020 ◽  
Vol 142 (5) ◽  
Author(s):  
Dean Culver ◽  
Bryan Glaz ◽  
Samuel Stanton
Keyword(s):  
Molecular Motors ◽  
Binding Sites ◽  
Molecular Motor ◽  
Myosin Ii ◽  
Three Dimensional ◽  
Production Capacity ◽  
Force Production ◽  
Actin Binding ◽  
Three Dimensional Model ◽  
Thermal Agitation

Abstract Animal skeletal muscle exhibits very interesting behavior at near-stall forces (when the muscle is loaded so strongly that it can barely contract). Near this physical limit, the myosin II proteins may be unable to reach advantageous actin binding sites through simple attractive forces. It has been shown that the advantageous utilization of thermal agitation is a likely source for an increased force-production capacity and reach in myosin-V (a processing motor protein), and here we explore the dynamics of a molecular motor without hand-over-hand motion including Brownian motion to show how local elastic energy well boundaries may be overcome. We revisit a spatially two-dimensional mechanical model to illustrate how thermal agitation can be harvested for useful mechanical work in molecular machinery inspired by this biomechanical phenomenon without rate functions or empirically inspired spatial potential functions. Additionally, the model accommodates variable lattice spacing, and it paves the way for a full three-dimensional model of cross-bridge interactions where myosin II may be azimuthally misaligned with actin binding sites. With potential energy sources based entirely on realizable components, this model lends itself to the design of artificial, molecular-scale motors.

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