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The Journal of Neuroscience : the... Nov 2022The outer hair cells in the mammalian cochlea are cellular actuators essential for sensitive hearing. The geometry and stiffness of the structural scaffold surrounding...
The outer hair cells in the mammalian cochlea are cellular actuators essential for sensitive hearing. The geometry and stiffness of the structural scaffold surrounding the outer hair cells will determine how the active cells shape mammalian hearing by modulating the organ of Corti (OoC) vibrations. Specifically, the tectorial membrane and the Deiters cell are mechanically in series with the hair bundle and soma, respectively, of the outer hair cell. Their mechanical properties and anatomic arrangement must determine the relative motion among different OoC structures. We measured the OoC mechanics in the cochleas acutely excised from young gerbils of both sexes at a resolution fine enough to distinguish the displacement of individual cells. A three-dimensional finite element model of fully deformable OoC was exploited to analyze the measured data in detail. As a means to verify the computer model, the basilar membrane deformations because of static and dynamic stimulations were measured and simulated. Two stiffness ratios have been identified that are critical to understand cochlear physics, which are the stiffness of the tectorial membrane with respect to the hair bundle and the stiffness of the Deiters cell with respect to the outer hair cell body. Our measurements suggest that the Deiters cells act like a mechanical equalizer so that the outer hair cells are constrained neither too rigidly nor too weakly. Mammals can detect faint sounds thanks to the action of mammalian-specific receptor cells called the outer hair cells. It is getting clearer that understanding the interactions between the outer hair cells and their surrounding structures such as the tectorial membrane and the Deiters cell is critical to resolve standing debates. Depending on theories, the stiffness of those two structures ranges from negligible to rigid. Because of their perceived importance, their properties have been measured in previous studies. However, nearly all existing data were obtained (after they were detached from the outer hair cells), which obscures their interaction with the outer hair cells. We quantified the mechanical properties of the tectorial membrane and the Deiters cell .
Topics: Male; Animals; Female; Hair Cells, Auditory, Outer; Organ of Corti; Basilar Membrane; Tectorial Membrane; Cochlea; Hair Cells, Vestibular; Gerbillinae
PubMed: 36123119
DOI: 10.1523/JNEUROSCI.2417-21.2022 -
ELife Sep 2018Auditory sensory outer hair cells are thought to amplify sound-induced basilar membrane vibration through a feedback mechanism to enhance hearing sensitivity. For...
Auditory sensory outer hair cells are thought to amplify sound-induced basilar membrane vibration through a feedback mechanism to enhance hearing sensitivity. For optimal amplification, the outer hair cell-generated force must act on the basilar membrane at an appropriate time at every cycle. However, the temporal relationship between the outer hair cell-driven reticular lamina vibration and the basilar membrane vibration remains unclear. By measuring sub-nanometer vibrations directly from outer hair cells using a custom-built heterodyne low-coherence interferometer, we demonstrate in living gerbil cochleae that the reticular lamina vibration occurs after, not before, the basilar membrane vibration. Both tone- and click-induced responses indicate that the reticular lamina and basilar membrane vibrate in opposite directions at the cochlear base and they oscillate in phase near the best-frequency location. Our results suggest that outer hair cells enhance hearing sensitivity through a global hydromechanical mechanism, rather than through a local mechanical feedback as commonly supposed.
Topics: Animals; Basilar Membrane; Cochlea; Female; Gerbillinae; Male; Postmortem Changes; Sound; Time Factors; Vibration
PubMed: 30183615
DOI: 10.7554/eLife.37625 -
Hearing Research Sep 2022It is a common belief that the mammalian cochlea achieves its exquisite sensitivity, frequency selectivity, and dynamic range through an outer hair cell-based active...
It is a common belief that the mammalian cochlea achieves its exquisite sensitivity, frequency selectivity, and dynamic range through an outer hair cell-based active process, or cochlear amplification. As a sound-induced traveling wave propagates from the cochlear base toward the apex, outer hair cells at a narrow region amplify the low level sound-induced vibration through a local feedback mechanism. This widely accepted theory has been tested by measuring sound-induced sub-nanometer vibrations within the organ of Corti in the sensitive living cochleae using heterodyne low-coherence interferometry and optical coherence tomography. The aim of this short review is to summarize experimental findings on the cochlear active process by the authors' group. Our data show that outer hair cells are able to generate substantial forces for driving the cochlear partition at all audible frequencies in vivo. The acoustically induced reticular lamina vibration is larger and more broadly tuned than the basilar membrane vibration. The reticular lamina and basilar membrane vibrate approximately in opposite directions at low frequencies and in the same direction at the best frequency. The group delay of the reticular lamina is larger than that of the basilar membrane. The magnitude and phase differences between the reticular lamina and basilar membrane vibration are physiologically vulnerable. These results contradict predictions based on the local feedback mechanism but suggest a global hydromechanical mechanism for cochlear amplification. This article is part of the Special Issue Outer hair cell Edited by Joseph Santos-Sacchi and Kumar Navaratnam.
Topics: Animals; Basilar Membrane; Cochlea; Hair Cells, Auditory, Outer; Mammals; Organ of Corti; Sound; Vibration
PubMed: 34922772
DOI: 10.1016/j.heares.2021.108407 -
Hearing Research Sep 2022Cochlear distortions afford researchers and clinicians a glimpse into the conditions and properties of inner ear signal processing mechanisms. Until recently, our... (Review)
Review
Cochlear distortions afford researchers and clinicians a glimpse into the conditions and properties of inner ear signal processing mechanisms. Until recently, our examination of these distortions has been limited to measuring the vibration of the basilar membrane or recording acoustic distortion output in the ear canal. Despite its importance, the generation mechanism of cochlear distortion remains a substantial task to understand. The ability to measure the vibration of the reticular lamina in rodent models is a recent experimental advance. Surprising mechanical properties have been revealed. These properties merit both discussion in context with our current understanding of distortion, and appraisal of the significance of new interpretations of cochlear mechanics. This review focusses on some of the recent data from our research groups and discusses the implications of these data on our understanding of vocalization processing in the periphery, and their influence upon future experimental directions. This article is part of the Special Issue Outer hair cell Edited by Joseph Santos-Sacchi and Kumar Navaratnam.
Topics: Acoustic Stimulation; Basement Membrane; Basilar Membrane; Cochlea; Hair Cells, Auditory, Outer; Vibration
PubMed: 34916081
DOI: 10.1016/j.heares.2021.108405 -
Journal of the Association For Research... Oct 2014The mouse has become an important animal model in understanding cochlear function. Structures, such as the tectorial membrane or hair cells, have been changed by gene...
The mouse has become an important animal model in understanding cochlear function. Structures, such as the tectorial membrane or hair cells, have been changed by gene manipulation, and the resulting effect on cochlear function has been studied. To contrast those findings, physical properties of the basilar membrane (BM) and tectorial membrane (TM) in mice without gene mutation are of great importance. Using the hemicochlea of CBA/CaJ mice, we have demonstrated that tectorial membrane (TM) and basilar membrane (BM) revealed a stiffness gradient along the cochlea. While a simple spring mass resonator predicts the change in the characteristic frequency of the BM, the spring mass model does not predict the frequency change along the TM. Plateau stiffness values of the TM were 0.6 ± 0.5, 0.2 ± 0.1, and 0.09 ± 0.09 N/m for the basal, middle, and upper turns, respectively. The BM plateau stiffness values were 3.7 ± 2.2, 1.2 ± 1.2, and 0.5 ± 0.5 N/m for the basal, middle, and upper turns, respectively. Estimations of the TM Young's modulus (in kPa) revealed 24.3 ± 25.2 for the basal turns, 5.1 ± 4.5 for the middle turns, and 1.9 ± 1.6 for the apical turns. Young's modulus determined at the BM pectinate zone was 76.8 ± 72, 23.9 ± 30.6, and 9.4 ± 6.2 kPa for the basal, middle, and apical turns, respectively. The reported stiffness values of the CBA/CaJ mouse TM and BM provide basic data for the physical properties of its organ of Corti.
Topics: Animals; Basilar Membrane; Biomechanical Phenomena; Guinea Pigs; Mice; Mice, Inbred CBA; Tectorial Membrane
PubMed: 24865766
DOI: 10.1007/s10162-014-0463-y -
Hearing Research Sep 2022In the cochlea, mechano-electrical transduction is preceded by dynamic range compression. Outer hair cells (OHCs) and their voltage dependent length changes, known as... (Review)
Review
In the cochlea, mechano-electrical transduction is preceded by dynamic range compression. Outer hair cells (OHCs) and their voltage dependent length changes, known as electromotility, play a central role in this compression process, but the exact mechanisms are poorly understood. Here we review old and new experimental findings and show that (1) just audible high-frequency tones evoke an ∼1-microvolt AC receptor potential in basal OHCs; (2) any mechanical amplification of soft high-frequency tones by OHC motility would have an adverse effect on their audibility; (3) having a higher basolateral K+ conductance, while increasing the OHC corner frequency, does not boost the magnitude of the high-frequency AC receptor potential; (4) OHC receptor currents display a substantial rectified (DC) component; (5) mechanical DC responses (baseline shifts) to acoustic stimuli, while insignificant on the basilar membrane, can be comparable in magnitude to AC responses when recorded in the organ of Corti, both in the apex and the base. In the basal turn, the DC component may even exceed the AC component, lending support to Dallos' suggestion that both apical and basal OHCs display a significant degree of rectification. We further show that (6) low-intensity cochlear traveling waves, by virtue of their abrupt transition from fast to slow propagation, are well suited to transport high-frequency energy with minimal losses (∼2-dB loss for 16-kHz tones in the gerbil); (7) a 90-dB, 16-kHz tone, if transmitted without loss to its tonotopic place, would evoke a destructive displacement amplitude of 564 nm. We interpret these findings in a framework in which local dissipation is regulated by OHC motility. This article is part of the Special Issue Outer hair cell Edited by Joseph Santos-Sacchi and Kumar Navaratnam.
Topics: Acoustic Stimulation; Basilar Membrane; Cochlea; Hair Cells, Auditory, Outer; Hair Cells, Vestibular
PubMed: 34686384
DOI: 10.1016/j.heares.2021.108367 -
Advances in Experimental Medicine and... 2016Dynamic aspects of cochlear mechanical compression were studied by recording basilar membrane (BM) vibrations evoked by tone pairs ("beat stimuli") in the 11-19 kHz...
Dynamic aspects of cochlear mechanical compression were studied by recording basilar membrane (BM) vibrations evoked by tone pairs ("beat stimuli") in the 11-19 kHz region of the gerbil cochlea. The frequencies of the stimulus components were varied to produce a range of "beat rates" at or near the characteristic frequency (CF) of the BM site under study, and the amplitudes of the components were balanced to produce near perfect periodic cancellations, visible as sharp notches in the envelope of the BM response. We found a compressive relation between instantaneous stimulus intensity and BM response magnitude that was strongest at low beat rates (e.g., 10-100 Hz). At higher beat rates, the amount of compression reduced progressively (i.e. the responses became linearized), and the rising and falling flanks of the response envelope showed increasing amounts of hysteresis; the rising flank becoming steeper than the falling flank. This hysteresis indicates that cochlear mechanical compression is not instantaneous, and is suggestive of a gain control mechanism having finite attack and release times. In gain control terms, the linearization that occurs at higher beat rates occurs because the instantaneous gain becomes smoothened, or low-pass filtered, with respect to the magnitude fluctuations in the stimulus. In terms of peripheral processing, the linearization corresponds to an enhanced coding, or decompression, of rapid amplitude modulations. These findings are relevant both to those who wish to understand the underlying mechanisms and those who need a realistic model of nonlinear processing by the auditory periphery.
Topics: Acoustic Stimulation; Animals; Basilar Membrane; Gerbillinae; Vibration
PubMed: 27080667
DOI: 10.1007/978-3-319-25474-6_28 -
European Annals of Otorhinolaryngology,... Sep 2013Bone conduction hearing inevitably involves vibration of the basilar membrane in response to a pressure gradient on either side of the membrane. The propagated wave that... (Review)
Review
Bone conduction hearing inevitably involves vibration of the basilar membrane in response to a pressure gradient on either side of the membrane. The propagated wave that symbolizes this vibration of the basilar membrane can be triggered intentionally, when a bone vibrator is placed on the mastoid bone, or inadvertently when testing hearing of one ear by air conduction while disregarding transmission of the sound to the other side. When hearing is tested with a bone vibrator, the pathways leading to the basilar membrane can be divided into two main categories. The first type of pathway short-circuits the middle ear and comprises three distinct mechanisms: cochlear fluid inertia, compression of the cochlear walls, and pressure changes exerted via cerebrospinal fluid. In the second type of pathway, the stimulus reaches the basilar membrane via the middle ear, either directly or via the outer ear. Although it is difficult to precisely determine the contribution of each of these pathways to the basilar membrane, bone conduction remains the clinically most reliable way of directly testing cochlear function.
Topics: Acoustic Stimulation; Animals; Basilar Membrane; Bone Conduction; Cerebrospinal Fluid; Cochlea; Ear, Middle; Hearing; Humans
PubMed: 23743177
DOI: 10.1016/j.anorl.2012.11.002 -
Cold Spring Harbor Perspectives in... May 2019Cochlear hair cells employ mechanically gated ion channels located in stereocilia that open in response to sound wave-induced motion of the basilar membrane, converting... (Review)
Review
Cochlear hair cells employ mechanically gated ion channels located in stereocilia that open in response to sound wave-induced motion of the basilar membrane, converting mechanical stimulation to graded changes in hair cell membrane potential. Membrane potential changes in hair cells cause neurotransmitter release from hair cells that initiate electrical signals in the nerve terminals of afferent fibers from spiral ganglion neurons. These signals are then propagated within the central nervous system (CNS) to mediate the sensation of hearing. Recent studies show that the mechanoelectrical transduction (MET) machinery of hair cells is formed by an ensemble of proteins. Candidate components forming the MET channel have been identified, but none alone fulfills all criteria necessary to define them as pore-forming subunits of the MET channel. We will review here recent findings on the identification and function of proteins that are components of the MET machinery in hair cells and consider remaining open questions.
Topics: Animals; Hair Cells, Auditory; Hearing; Humans; Ion Channels; Mechanotransduction, Cellular; Molecular Structure; Synapses; Synaptic Transmission
PubMed: 30082452
DOI: 10.1101/cshperspect.a033167 -
Trends in Hearing 2017Soft tissue conduction (STC) is a recently explored mode of auditory stimulation, complementing air (AC) and bone (BC) conduction stimulation. STC can be defined as the... (Review)
Review
Soft tissue conduction (STC) is a recently explored mode of auditory stimulation, complementing air (AC) and bone (BC) conduction stimulation. STC can be defined as the hearing induced when vibratory stimuli reach skin and soft tissue sites not directly overlying skull bone such as the head, neck, thorax, and body. Examples of STC include the delivery of vibrations to the skin of parts of the body by a clinical bone vibrator, hearing underwater sounds and free field air sounds, while AC hearing is attenuated by earplugs. The vibrations induced in the soft tissues are apparently transmitted along soft tissues, reaching, and exciting the ear. Further research is required to determine whether the mechanism of the final stage of STC hearing involves the excitation of the ear by eliciting inner ear fluid pressures that activate the hair cells directly, by the induction of skull bone vibrations, or by a combination of both mechanisms, depending on the magnitude of each mechanism.
Topics: Acoustic Stimulation; Air; Auditory Threshold; Bone Conduction; Connective Tissue; Hearing; Humans; Skin Physiological Phenomena; Sound; Vibration
PubMed: 28969522
DOI: 10.1177/2331216517734087