scholarly journals A role for tectorial membrane mechanics in activating the cochlear amplifier

2020 ◽  
Vol 10 (1) ◽  
Author(s):  
Amir Nankali ◽  
Yi Wang ◽  
Clark Elliott Strimbu ◽  
Elizabeth S. Olson ◽  
Karl Grosh

Abstract The mechanical and electrical responses of the mammalian cochlea to acoustic stimuli are nonlinear and highly tuned in frequency. This is due to the electromechanical properties of cochlear outer hair cells (OHCs). At each location along the cochlear spiral, the OHCs mediate an active process in which the sensory tissue motion is enhanced at frequencies close to the most sensitive frequency (called the characteristic frequency, CF). Previous experimental results showed an approximate 0.3 cycle phase shift in the OHC-generated extracellular voltage relative the basilar membrane displacement, which was initiated at a frequency approximately one-half octave lower than the CF. Findings in the present paper reinforce that result. This shift is significant because it brings the phase of the OHC-derived electromotile force near to that of the basilar membrane velocity at frequencies above the shift, thereby enabling the transfer of electrical to mechanical power at the basilar membrane. In order to seek a candidate physical mechanism for this phenomenon, we used a comprehensive electromechanical mathematical model of the cochlear response to sound. The model predicts the phase shift in the extracellular voltage referenced to the basilar membrane at a frequency approximately one-half octave below CF, in accordance with the experimental data. In the model, this feature arises from a minimum in the radial impedance of the tectorial membrane and its limbal attachment. These experimental and theoretical results are consistent with the hypothesis that a tectorial membrane resonance introduces the correct phasing between mechanical and electrical responses for power generation, effectively turning on the cochlear amplifier.

2020 ◽  
Author(s):  
A. Nankali ◽  
Y. Wang ◽  
C. E. Strimbu ◽  
E. S. Olson ◽  
K. Grosh

ABSTRACTThe mechanical and electrical responses of the mammalian cochlea to acoustic stimuli are nonlinear and highly tuned in frequency. This is due to the electromechanical properties of cochlear outer hair cells (OHCs). At each location along the cochlear spiral, the OHCs mediate an active process in which the sensory tissue motion is enhanced at frequencies close to the most sensitive frequency (called the characteristic frequency CF). Previous experimental results showing an approximate 0.3 cycle phase shift in the OHC-generated extracellular voltage relative the basilar membrane displacement that is initiated at a frequency approximately one-half octave lower than the CF are repeated in the present paper with similar findings. This shift is significant because it brings the phase of the OHC-derived electromotile force near to that of the basilar membrane velocity at frequencies above the shift, thereby enabling the transfer of electrical to mechanical power at the basilar membrane. In order to seek a candidate physical mechanism for this phenomenon, we used a comprehensive electromechanical mathematical model of the cochlear response to sound. The model predicts the phase shift in the extracellular voltage referenced to the basilar membrane at a frequency approximately one-half octave below CF, in accordance with the experimental data. In the model, this feature arises from a minimum in the radial impedance of the tectorial membrane and its limbal attachment. These experimental and theoretical results are consistent with the hypothesis that a tectorial membrane resonance introduces the correct phasing between mechanical and electrical responses for power generation, effectively turning on the cochlear amplifier.SIGNIFICANCEThe mechanical and electrical responses of the mammalian cochlea are nonlinear exhibiting up to a thousand-fold difference in gain depending on the frequency and level of sound stimulus. Cochlear outer hair cells (OHC) are broadband electro-mechanical energy converters that mediate this nonlinear active process. However, the mechanism by which the OHC electromotile force acquires the appropriate phase to power this nonlinearity remains unknown. By analyzing new and existing experimental data and using a mathematical model, we address this open issue. We present evidence which suggests that a relatively simple feature, the frequency dependence of the radial impedance of the tectorial membrane, provides requisite mechanics to turn on the frequency-specific nonlinear process essential for healthy hearing.


1999 ◽  
Vol 82 (2) ◽  
pp. 676-686 ◽  
Author(s):  
I. J. Russell ◽  
M. Kössl

An extended region of the greater mustached bat’s cochlea, the sparsely innervated (SI) zone, is located just basally to the frequency place of the dominant 61-kHz component of the echolocation signal (CF2). Anatomic adaptations in the SI zone are thought to provide the basis for cochlear resonance to the CF2 echoes and for the extremely sharp tuning throughout the auditory system that allows these bats to detect Doppler shifts in the echoes caused by insect wing beat. We measured basilar membrane (BM) displacements in the SI zone with a laser interferometer and recorded acoustic distortion products at the ear drum at frequencies represented in the SI zone. The basilar membrane in the SI region was tuned both to its characteristic frequency (62–72 kHz) and to the resonance frequency (61–62 kHz). With increasing stimulus levels, the displacement growth functions are compressive curves with initial slopes close to unity, and their properties are consistent with the mammalian cochlear amplifier working at high sound frequencies. The sharp basilar membrane resonance is associated with a phase lag of 180° and with a shift of the peak resonance to lower frequencies for high stimulus levels. Within the range of the resonance, the distortion product otoacoustic emissions, which have been attributed to the resonance of the tectorial membrane in the SI region, are associated with an abrupt phase change of 360°. It is proposed that a standing wave resonance of the tectorial membrane drives the BM in the SI region and that the outer hair cells enhance, fine tune, and control the resonance. In the SI region, cochlear micromechanics appear to be able to work in two different modes: a conventional traveling wave leads to shear displacement between basilar and tectorial membrane and to neuronal excitation for 62–70 kHz. In addition, the SI region responds to 61–62 kHz with a resonance based on standing waves and thus preprocesses signals which are represented more apically in the CF2 region of the cochlea.


2021 ◽  
Author(s):  
Victoria Lukashkina ◽  
Snezana Levic ◽  
Patricio Simões ◽  
Zhenhang Xu ◽  
Joseph DiGuiseppi ◽  
...  

Abstract Cochlear sensitivity, essential for communication and exploiting the acoustic environment, is due to the sensory-motor outer hair cells (OHCs) that operate in the structural scaffold of supporting cells and extracellular spaces in the cochlear organ of Corti (OoC). It is unclear whether supporting cells (e.g., Deiters cells [DCs] and outer pillar cells [OPCs]) control cochlear sensitivity in vivo. Here we employed optogenetics to measure in vivo sound-induced cochlear mechanical and electrical responses, and ex vivo light-induced DC electrical responses in the OoC of mice that conditionally expressed channelrhodopsins (ChR2) specifically in DCs and OPCs. Illumination activated a nonselective ChR2 cation conductance and depolarized the DCs. This transient action reversibly blocked continuous, normally occurring, minor adjustments of tone-evoked basilar membrane displacements, and OHC voltage responses to tones at and close to their characteristic frequency, and speeded recovery from temporary acoustic desensitization. This is the first direct evidence for the interdependency of the structural, mechanical, and electrochemical arrangement of OHCs and OoC supporting cells which together fine control cochlear sensitivity.


1999 ◽  
Vol 82 (5) ◽  
pp. 2798-2807 ◽  
Author(s):  
Xintian Hu ◽  
Burt N. Evans ◽  
Peter Dallos

The basilar membrane in the mammalian cochlea vibrates when the cochlea receives a sound stimulus. This mechanical vibration is transduced into hair cell receptor potentials and thereafter encoded by action potentials in the auditory nerve. Knowledge of the mechanical transformation that converts basilar membrane vibration into hair cell stimulation has been limited, until recently, to hypothetical geometric models. Experimental observations are largely lacking to prove or disprove the validity of these models. We have developed a hemicochlea preparation to visualize the kinematics of the cochlear micromechanism. Direct mechanical drive of 1–2 Hz sinusoidal command was applied to the basilar membrane. Vibration patterns of the basilar membrane, inner and outer hair cells, supporting cells, and tectorial membrane have been recorded concurrently by means of a video optical flow technique. Basilar membrane vibration was driven in a direction transversal to its plane. However, the direction of the resulting vibration was found to be essentially radial at the level of the reticular lamina and cuticular plates of inner and outer hair cells. The tectorial membrane vibration was mainly transversal. The transmission ratio between cilia displacement of inner and outer hair cells and basilar membrane vibration is in the range of 0.7–1.1. These observations support, in part, the classical geometric models at low frequencies. However, there appears to be less tectorial membrane motion than predicted, and it is largely in the transversal direction.


2018 ◽  
Vol 10 (4) ◽  
pp. 48
Author(s):  
Valeri Goussev

The article is devoted to the specific consideration of the cochlear transduction for the low level sound intensities, which correspond to the regions near the perception threshold. The basic cochlea mechanics is extended by the new concept of the molecular filters, which allows discussing the transduction mechanism on the molecular level in the space-time domain. The molecular filters are supposed to be built on the set of the stereocilia of every inner hair cell. It is hypothesized that the molecular filters are the sensors in the feedback loop, which includes also outer hair cells along with the tectorial membrane and uses the zero compensation method to evaluate the traveling wave shape on the basilar membrane. Besides the compensation, the feedback loop, being spatially distributed along the cochlea, takes control over the tectorial membrane strain field generated by the outer hair cells, and implements it as the mechanism for the automatic gain control in the sound transduction.


2020 ◽  
Vol 2020 ◽  
pp. 1-10
Author(s):  
Jiangtao Su ◽  
Wenjuan Yao ◽  
Zhengshan Zhao

The organ of Corti (OC) in the cochlea is a significant structure for feeling sound. The components of OC and the interaction of the part with the surroundings contribute to the fact that the passive tuning of the cochlear macrostructure is unclear. Based on the interaction between the basilar membrane (BM), tectorial membrane (TM), reticular lamina (RL), and various parts of OC, a mechanical model of the cochlea is established to study the motion patterns of each part under the action of a certain pressure. The variational principle is applied to the calculation of the analytical expression of the displacement of the BM. The results of the analytical solution differ little from the experimental value, and the variation trend is consistent, which presents the correctness of the model. The parameter sensitivity analysis is carried out for obtaining the interaction principle and the primary and secondary roles of each component in the process of the sense of sound. The results show that the absence of the TM and the decrease in the stiffness of the outer hair cells (OHCs) and OHC bundles will shift vibratory response patterns to lower frequencies, in which the lack of TM will result in the greatest reduction of CF. The absence of RL exerts a negative influence on the CF as well as the amplitude of BM and thereby loss of hearing. Therefore, both TM and RL are essential structures during the process of the sense of sound. At the same time, the resonance frequency at the base of the BM is concentrated on the high-frequency segment, while the apex of the BM is mainly in the low frequency. Different points of BM correspond to different CF, which demonstrates the frequency selectivity of the BM.


2001 ◽  
Vol 81 (3) ◽  
pp. 1305-1352 ◽  
Author(s):  
Luis Robles ◽  
Mario A. Ruggero

In mammals, environmental sounds stimulate the auditory receptor, the cochlea, via vibrations of the stapes, the innermost of the middle ear ossicles. These vibrations produce displacement waves that travel on the elongated and spirally wound basilar membrane (BM). As they travel, waves grow in amplitude, reaching a maximum and then dying out. The location of maximum BM motion is a function of stimulus frequency, with high-frequency waves being localized to the “base” of the cochlea (near the stapes) and low-frequency waves approaching the “apex” of the cochlea. Thus each cochlear site has a characteristic frequency (CF), to which it responds maximally. BM vibrations produce motion of hair cell stereocilia, which gates stereociliar transduction channels leading to the generation of hair cell receptor potentials and the excitation of afferent auditory nerve fibers. At the base of the cochlea, BM motion exhibits a CF-specific and level-dependent compressive nonlinearity such that responses to low-level, near-CF stimuli are sensitive and sharply frequency-tuned and responses to intense stimuli are insensitive and poorly tuned. The high sensitivity and sharp-frequency tuning, as well as compression and other nonlinearities (two-tone suppression and intermodulation distortion), are highly labile, indicating the presence in normal cochleae of a positive feedback from the organ of Corti, the “cochlear amplifier.” This mechanism involves forces generated by the outer hair cells and controlled, directly or indirectly, by their transduction currents. At the apex of the cochlea, nonlinearities appear to be less prominent than at the base, perhaps implying that the cochlear amplifier plays a lesser role in determining apical mechanical responses to sound. Whether at the base or the apex, the properties of BM vibration adequately account for most frequency-specific properties of the responses to sound of auditory nerve fibers.


2018 ◽  
Author(s):  
Valeri Goussev

AbstractThe article is devoted to the specific consideration of the cochlear transduction for the low level sound intensities, which correspond to the regions near the perception threshold. The basic cochlea mechanics is extended by the new concept of the molecular filters, which allows us to discuss the transduction mechanism on the molecular level in the space-time domain. The molecular filters are supposed to be built on the set of the stereocilia of every inner hair cell. It is hypothesized that the molecular filters are the sensors in the feedback loop, which includes also outer hair cells along with the tectorial membrane and uses the zero compensation method to evaluate the traveling wave shape on the basilar membrane. Besides the compensation, the feedback loop, being spatially distributed along the cochlea, takes control over the tectorial membrane strain field generated by the outer hair cells, and implements it as the mechanism for the automatic gain control in the sound transduction.


2016 ◽  
Vol 13 (115) ◽  
pp. 20150913 ◽  
Author(s):  
Guangjian Ni ◽  
Stephen J. Elliott ◽  
Johannes Baumgart

The cochlear amplifier that provides our hearing with its extraordinary sensitivity and selectivity is thought to be the result of an active biomechanical process within the sensory auditory organ, the organ of Corti. Although imaging techniques are developing rapidly, it is not currently possible, in a fully active cochlea, to obtain detailed measurements of the motion of individual elements within a cross section of the organ of Corti. This motion is predicted using a two-dimensional finite-element model. The various solid components are modelled using elastic elements, the outer hair cells (OHCs) as piezoelectric elements and the perilymph and endolymph as viscous and nearly incompressible fluid elements. The model is validated by comparison with existing measurements of the motions within the passive organ of Corti, calculated when it is driven either acoustically, by the fluid pressure or electrically, by excitation of the OHCs. The transverse basilar membrane (BM) motion and the shearing motion between the tectorial membrane and the reticular lamina are calculated for these two excitation modes. The fully active response of the BM to acoustic excitation is predicted using a linear superposition of the calculated responses and an assumed frequency response for the OHC feedback.


2020 ◽  
Vol 10 (1) ◽  
Author(s):  
Haim Sohmer

The three modes of auditory stimulation (air, bone and soft tissue conduction) at threshold intensities are thought to share a common excitation mechanism: the stimuli induce passive displacements of the basilar membrane propagating from the base to the apex (slow mechanical traveling wave), which activate the outer hair cells, producing active displacements, which sum with the passive displacements. However, theoretical analyses and modeling of cochlear mechanics provide indications that the slow mechanical basilar membrane traveling wave may not be able to excite the cochlea at threshold intensities with the frequency discrimination observed. These analyses are complemented by several independent lines of research results supporting the notion that cochlear excitation at threshold may not involve a passive traveling wave, and the fast cochlear fluid pressures may directly activate the outer hair cells: opening of the sealed inner ear in patients undergoing cochlear implantation is not accompanied by threshold elevations to low frequency stimulation which would be expected to result from opening the cochlea, reducing cochlear impedance, altering hydrodynamics. The magnitude of the passive displacements at threshold is negligible. Isolated outer hair cells in fluid display tuned mechanical motility to fluid pressures which likely act on stretch sensitive ion channels in the walls of the cells. Vibrations delivered to soft tissue body sites elicit hearing. Thus, based on theoretical and experimental evidence, the common mechanism eliciting hearing during threshold stimulation by air, bone and soft tissue conduction may involve the fast-cochlear fluid pressures which directly activate the outer hair cells.


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