Publications by authors named "Elizabeth S Olson"

44 Publications

Model of cochlear microphonic explores the tuning and magnitude of hair cell transduction current.

Biophys J 2021 Sep 10;120(17):3550-3565. Epub 2021 Aug 10.

Otolaryngology, Head and Neck Surgery, New York, New York; Biomedical Engineering, Columbia University, New York, New York. Electronic address:

The mammalian cochlea relies on the active forcing of sensory outer hair cells (OHCs) to amplify traveling wave responses along the basilar membrane. These forces are the result of electromotility, wherein current through the OHCs leads to conformational changes in the cells that provide stresses on surrounding structures. OHC transducer current can be detected via the voltage in the scala tympani (the cochlear microphonic, CM), and the CM can be used as an indicator of healthy cochlear operation. The CM represents a summation of OHC currents (the inner hair cell contribution is known to be small) and to use CM to probe the properties of OHC transduction requires a model that simulates that summation. We developed a finite element model for that purpose. The pattern of current generators (the model input) was initially based on basilar membrane displacement, with the current size based on in vitro data. The model was able to reproduce the amplitude of experimental CM results reasonably well when the input tuning was enhanced slightly (peak increased by ∼6 dB), which can be regarded as additional hair bundle tuning, and with a current/input value of 200-260 pA/nm, which is ∼4 times greater than the largest in vitro measures.
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http://dx.doi.org/10.1016/j.bpj.2021.08.010DOI Listing
September 2021

Impact of Systemic versus Intratympanic Dexamethasone Administration on the Perilymph Proteome.

J Proteome Res 2021 08 22;20(8):4001-4009. Epub 2021 Jul 22.

Department of Otolaryngology-Head and Neck Surgery, Columbia University Vagelos College of Physicians and Surgeons, New York, New York 10032, United States.

Glucocorticoids are the first-line treatment for sensorineural hearing loss, but little is known about the mechanism of their protective effect or the impact of route of administration. The recent development of hollow microneedles enables safe and reliable sampling of perilymph for proteomic analysis. Using these microneedles, we investigate the effect of intratympanic (IT) versus intraperitoneal (IP) dexamethasone administration on guinea pig perilymph proteome. Guinea pigs were treated with IT dexamethasone ( = 6), IP dexamethasone ( = 8), or untreated for control ( = 8) 6 h prior to aspiration. The round window membrane (RWM) was accessed via a postauricular approach, and hollow microneedles were used to perforate the RWM and aspirate 1 μL of perilymph. Perilymph samples were analyzed by liquid chromatography-mass spectrometry-based label-free quantitative proteomics. Mass spectrometry raw data files have been deposited in an international public repository (MassIVE proteomics repository at https://massive.ucsd.edu/) under data set # MSV000086887. In the 22 samples of perilymph analyzed, 632 proteins were detected, including the inner ear protein cochlin, a perilymph marker. Of these, 14 proteins were modulated by IP, and three proteins were modulated by IT dexamethasone. In both IP and IT dexamethasone groups, VGF nerve growth factor inducible was significantly upregulated compared to control. The remaining adjusted proteins modulate neurons, inflammation, or protein synthesis. Proteome analysis facilitated by the use of hollow microneedles shows that route of dexamethasone administration impacts changes seen in perilymph proteome. Compared to IT administration, the IP route was associated with greater changes in protein expression, including proteins involved in neuroprotection, inflammatory pathway, and protein synthesis. Our findings show that microneedles can mediate safe and effective intracochlear sampling and hold promise for inner ear diagnostics.
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http://dx.doi.org/10.1021/acs.jproteome.1c00322DOI Listing
August 2021

Nonlinearity of intracochlear motion and local cochlear microphonic: Comparison between guinea pig and gerbil.

Hear Res 2021 Jun 15;405:108234. Epub 2021 Apr 15.

Department of Biomedical Engineering, Columbia University, New York City, NY, United States; Department of Otolaryngology-Head and Neck Surgery, Columbia University, New York City, NY, United States. Electronic address:

Studying the in-vivo mechanical and electrophysiological cochlear responses in several species helps us to have a comprehensive view of the sensitivity and frequency selectivity of the cochlea. Different species might use different mechanisms to achieve the sharp frequency-place map. The outer hair cells (OHC) play an important role in mediating frequency tuning. In the present work, we measured the OHC-generated local cochlear microphonic (LCM) and the motion of different layers in the organ of Corti using optical coherence tomography (OCT) in the first turn of the cochlea in guinea pig. In the best frequency (BF) band, our observations were similar to our previous measurements in gerbil: a nonlinear peak in LCM responses and in the basilar membrane (BM) and OHC-region displacements, and higher motion in the OHC region than the BM. Sub-BF the responses in the two species were different. In both species the sub-BF displacement of the BM was linear and LCM was nonlinear. Sub-BF in the OHC-region, nonlinearity was only observed in a subset of healthy guinea pig cochleae while in gerbil, robust nonlinearity was observed in all healthy cochleae. The differences suggest that gerbils and guinea pigs employ different mechanisms for filtering sub-BF OHC activity from BM responses. However, it cannot be ruled out that the differences are due to technical measurement differences across the species.
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http://dx.doi.org/10.1016/j.heares.2021.108234DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8113154PMC
June 2021

Time-domain and frequency-domain effects of tensor tympani contraction on middle ear sound transmission in gerbil.

Hear Res 2021 Jun 8;405:108231. Epub 2021 Apr 8.

OTO/HNS and BME, Columbia University, 630 W 168th street, New York, NY 10032 United States. Electronic address:

The middle ear is a high-fidelity, broadband impedance transformer that transmits acoustic stimuli at the eardrum to the inner ear. It is home to the two smallest muscles in mammalian species, which modulate middle ear transmission. Of this pair, the function of the tensor tympani muscle (TTM) has remained obscure. We investigated the acoustic effects of this muscle in young adult gerbils. We measured changes in middle ear vibration produced by pulse-train-elicited TTM contraction - in the time-domain with a click stimulus and in the frequency-domain with multitone zwuis stimuli. In our click experiments, there was generally a small reduction in the primary peak of the response and a slight increase in the subsequent ringing, but there was essentially no change in the delay of the click response at the umbo (less than 1 µs change). In our multitone experiments, there were consistent patterns of attenuation and enhancement in the velocity responses at the umbo and ossicles. TTM contraction produced a narrow band of enhancement around 6 kHz (maximally ~5 dB) that can be modeled with an increased stiffness of an overdamped spring-mass resonance. At frequencies below 2 kHz and above 35 kHz, TTM contraction attenuated middle ear vibrations by as much as fivefold.
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http://dx.doi.org/10.1016/j.heares.2021.108231DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8113157PMC
June 2021

Novel 3D-printed hollow microneedles facilitate safe, reliable, and informative sampling of perilymph from guinea pigs.

Hear Res 2021 02 2;400:108141. Epub 2020 Dec 2.

Department of Otolaryngology - Head and Neck Surgery, Columbia University Vagelos College of Physicians and Surgeons, 180 Fort Washington Avenue, Harkness Pavilion, 8th Floor, New York, NY 10032, United States; Department of Mechanical Engineering, Columbia University, New York, NY, United States. Electronic address:

Background: Inner ear diagnostics is limited by the inability to atraumatically obtain samples of inner ear fluid. The round window membrane (RWM) is an attractive portal for accessing perilymph samples as it has been shown to heal within one week after the introduction of microperforations. A 1 µL volume of perilymph is adequate for proteome analysis, yet the total volume of perilymph within the scala tympani of the guinea pig is limited to less than 5 µL. This study investigates the safety and reliability of a novel hollow microneedle device to aspirate perilymph samples adequate for proteomic analysis.

Methods: The guinea pig RWM was accessed via a postauricular surgical approach. 3D-printed hollow microneedles with an outer diameter of 100 µm and an inner diameter of 35 µm were used to perforate the RWM and aspirate 1 µL of perilymph. Two perilymph samples were analyzed by liquid chromatography-mass spectrometry-based quantitative proteomics as part of a preliminary study. Hearing was assessed before and after aspiration using compound action potential (CAP) and distortion product otoacoustic emissions (DPOAE). RWMs were harvested 72 h after aspiration and evaluated for healing using confocal microscopy.

Results: There was no permanent damage to hearing at 72 h after perforation as assessed by CAP (n = 7) and DPOAE (n = 8), and all perforations healed completely within 72 h (n = 8). In the two samples of perilymph analyzed, 620 proteins were detected, including the inner ear protein cochlin, widely recognized as a perilymph marker.

Conclusion: Hollow microneedles can facilitate aspiration of perilymph across the RWM at a quality and volume adequate for proteomic analysis without causing permanent anatomic or physiologic dysfunction. Microneedles can mediate safe and effective intracochlear sampling and show great promise for inner ear diagnostics.
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http://dx.doi.org/10.1016/j.heares.2020.108141DOI Listing
February 2021

Cochlear mechanics: new insights from vibrometry and Optical Coherence Tomography.

Curr Opin Physiol 2020 Dec 5;18:56-62. Epub 2020 Sep 5.

Department of Otolaryngolgy Head and Neck Surgery, Vagelos College of Physicians and Surgeons, Columbia University, 630 W 168th St, New York, NY 10032.

The cochlea is a complex biological machine that transduces sound-induced mechanical vibrations to neural signals. Hair cells within the sensory tissue of the cochlea transduce vibrations into electrical signals, and exert electromechanical feedback that enhances the passive frequency separation provided by the cochlea's traveling wave mechanics; this enhancement is termed cochlear amplification. The vibration of the sensory tissue has been studied with many techniques, and the current state of the art is optical coherence tomography (OCT). The OCT technique allows for motion of intra-organ structures to be measured at many layers within the sensory tissue, at several angles and in previously under-explored species. OCT-based observations are already impacting our understanding of hair cell excitation and cochlear amplification.
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http://dx.doi.org/10.1016/j.cophys.2020.08.022DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7584129PMC
December 2020

Manipulation of the Endocochlear Potential Reveals Two Distinct Types of Cochlear Nonlinearity.

Biophys J 2020 11 20;119(10):2087-2101. Epub 2020 Oct 20.

Columbia University Medical Center, Department of Otolaryngology, New York, New York; Columbia University, Department of Biomedical Engineering, New York, New York. Electronic address:

The mammalian hearing organ, the cochlea, contains an active amplifier to boost the vibrational response to low level sounds. Hallmarks of this active process are sharp location-dependent frequency tuning and compressive nonlinearity over a wide stimulus range. The amplifier relies on outer hair cell (OHC)-generated forces driven in part by the endocochlear potential, the ∼+80 mV potential maintained in scala media, generated by the stria vascularis. We transiently eliminated the endocochlear potential in vivo by an intravenous injection of furosemide and measured the vibrations of different layers in the cochlea's organ of Corti using optical coherence tomography. Distortion product otoacoustic emissions were also monitored. After furosemide injection, the vibrations of the basilar membrane lost the best frequency (BF) peak and showed broad tuning similar to a passive cochlea. The intra-organ of Corti vibrations measured in the region of the OHCs lost the BF peak and showed low-pass responses but retained nonlinearity. This strongly suggests that OHC electromotility was operating and being driven by nonlinear OHC current. Thus, although electromotility is presumably necessary to produce a healthy BF peak, the mere presence of electromotility is not sufficient. The BF peak recovered nearly fully within 2 h, along with the recovery of odd-order distortion product otoacoustic emissions. The recovery pattern suggests that physical shifts in operating condition are a critical step in the recovery process.
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http://dx.doi.org/10.1016/j.bpj.2020.10.005DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7732743PMC
November 2020

A role for tectorial membrane mechanics in activating the cochlear amplifier.

Sci Rep 2020 10 19;10(1):17620. Epub 2020 Oct 19.

Department of Mechanical Engineering, University of Michigan, Ann Arbor, MI, 48109, USA.

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.
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http://dx.doi.org/10.1038/s41598-020-73873-9DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7573614PMC
October 2020

Anatomical and Functional Consequences of Microneedle Perforation of Round Window Membrane.

Otol Neurotol 2020 02;41(2):e280-e287

Department of Otolaryngology-Head and Neck Surgery, Columbia University Vagelos College of Physicians and Surgeons.

Hypothesis: Microneedles can create microperforations in the round window membrane (RWM) without causing anatomic or physiologic damage.

Background: Reliable delivery of agents into the inner ear for therapeutic and diagnostic purposes remains a challenge. Our novel approach employs microneedles to facilitate intracochlear access via the RWM. This study investigates the anatomical and functional consequences of microneedle perforations in guinea pig RWMs in vivo.

Methods: Single three-dimensional-printed, 100 μm diameter microneedles were used to perforate the guinea pig RWM via the postauricular sulcus. Hearing was assessed both before and after microneedle perforation using compound action potential and distortion product otoacoustic emissions. Confocal microscopy was used ex vivo to examine harvested RWMs, measuring the size, shape, and location of perforations and documenting healing at 0 hours (n = 7), 24 hours (n = 6), 48 hours (n = 6), and 1 week (n = 6).

Results: Microneedles create precise and accurate perforations measuring 93.1 ± 29.0 μm by 34.5 ± 16.8 μm and produce a high-frequency threshold shift that disappears after 24 hours. Examination of perforations over time demonstrates healing progression over 24 to 48 hours and complete perforation closure by 1 week.

Conclusion: Microneedles can create a temporary microperforation in the RWM without causing significant anatomic or physiologic dysfunction. Microneedles have the potential to mediate safe and effective intracochlear access for diagnosis and treatment of inner ear disease.
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http://dx.doi.org/10.1097/MAO.0000000000002491DOI Listing
February 2020

Nonlinearity and amplification in cochlear responses to single and multi-tone stimuli.

Hear Res 2019 06 11;377:271-281. Epub 2019 Apr 11.

Department of Biomedical Engineering Columbia University, New York City, NY, United States; Department of Otolaryngology-Head & Neck Surgery, Columbia University, New York City, NY, United States. Electronic address:

Mechanical displacements of the basilar membrane (BM) and the electrophysiological responses of the auditory outer hair cells (OHCs) are key components of the frequency tuning and cochlear amplification in the mammalian cochlea. In the work presented here, we measured the responses of (1) the extracellular voltage generated by OHCs (V) and (2) displacements within the organ of Corti complex (OCC) to a multi-tone stimulus, and to single tones. Using optical coherence tomography (OCT), we were able to measure displacements of different layers in the OCC simultaneously, in the base of the gerbil cochlea. We explored the effect of the two types of sound stimuli to the nonlinear behavior of voltage and displacement in two frequency regions: a frequency region below the BM nonlinearity (sub-BF region: f < ∼0.7 BF), and in the best frequency (BF) region. In the sub-BF region, BM motion (X) had linear growth for both stimulus types, and the motion in the OHC region (X) was mildly nonlinear for single tones, and relatively strongly nonlinear for multi-tones. Sub-BF, the nonlinear character of V was similar to that of X. In the BF region X, V and X all possessed the now-classic nonlinearity of the BF peak. Coupling these observations with previous findings on phasing between OHC force and traveling wave motions, we propose the following framework for cochlear nonlinearity: The BF-region nonlinearity is an amplifying nonlinearity, in which OHC forces input power into the traveling wave, allowing it to travel further apical to the region where it peaks. The sub-BF nonlinearity is a non-amplifying nonlinearity; it represents OHC electromotility, and saturates due to OHC current saturation, but the OHC forces do not possess the proper phasing to feed power into the traveling wave.
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http://dx.doi.org/10.1016/j.heares.2019.04.001DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6511461PMC
June 2019

Adaptation of Cochlear Amplification to Low Endocochlear Potential.

Biophys J 2019 05 30;116(9):1769-1786. Epub 2019 Mar 30.

Biomedical Engineering, Columbia University, New York, New York; Otalaryngology/Head & Neck Surgery, Columbia University, New York, New York. Electronic address:

Endocochlear potential (EP) is essential for cochlear amplification by providing the voltage source needed to drive outer hair cell (OHC) transducer current, which leads to OHC electromechanical force. An early study using furosemide to reversibly reduce EP showed that distortion product otoacoustic emissions (DPOAEs) recovered before EP. This indicated that cochlear amplification may be able to adjust to a new, lower EP. To investigate the mechanism of this adjustment, the extracellular OHC voltage, which we term local cochlear microphonic (LCM), was measured simultaneously with DPOAE and EP while using intraperitoneal (IP) and intravenous injection of furosemide to reversibly reduce EP. With IP injection, the DPOAEs recovered fully, whereas the EP was reduced, but LCM showed a similar time course as EP. The DPOAEs failed to accurately report the variation of cochlear amplification. With intravenous injection, for which both reduction and recovery of EP are known to occur relatively quickly compared to IP, the cochlear amplification observed in LCM could attain nearly full or even full recovery with reduced EP. This showed the cochlea has an ability to adjust to diminished operating condition. Furthermore, the cochlear amplifier and EP recovered with different time courses: cochlear amplification just started to recover after the EP was nearly fully recovered and stabilized. Using a Boltzmann model and the second harmonic of the LCM to estimate the mechanoelectric transducer channel operating point, we found that the recovery of cochlear amplification occurred with recentering of the operating point.
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http://dx.doi.org/10.1016/j.bpj.2019.03.020DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6506630PMC
May 2019

Scanning optical coherence tomography probe for in vivo imaging and displacement measurements in the cochlea.

Biomed Opt Express 2019 Feb 1;10(2):1032-1043. Epub 2019 Feb 1.

Department of Biomedical Engineering, Columbia University, 1210 Amsterdam Ave, New York, NY 10027, USA.

We developed a spectral domain optical coherence tomography (SDOCT) fiber optic probe for imaging and sub-nanometer displacement measurements inside the mammalian cochlea. The probe, 140 μm in diameter, can scan laterally up to 400 μm by means of a piezoelectric bender. Two different sampling rates are used, 10 kHz for high-resolution B-scan imaging, and 100 kHz for displacement measurements in order to span the auditory frequency range of gerbil (~50 kHz). Once the cochlear structures are recognized, the scanning range is gradually decreased and ultimately stopped with the probe pointing at the selected angle to measure the simultaneous displacements of multiple structures inside the organ of Corti (OC). The displacement measurement is based on spectral domain phase microscopy. The displacement noise level depends on the A-scan signal of the structure within the OC and we have attained levels as low as ~0.02 nm in in vivo measurements. The system's broadband infrared light source allows for an imaging depth of ~2.7 mm, and axial resolution of ~3 μm. In future development, the probe can be coupled with an electrode for time-locked voltage and displacement measurements in order to explore the electro-mechanical feedback loop that is key to cochlear processing. Here, we describe the fabrication of the laterally-scanning optical probe, and demonstrate its functionality with in vivo experiments.
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http://dx.doi.org/10.1364/BOE.10.001032DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6377895PMC
February 2019

Experimental and Theoretical Explorations of Traveling Waves and Tuning in the Bushcricket Ear.

Biophys J 2019 01 29;116(1):165-177. Epub 2018 Nov 29.

Goethe University, Frankfurt am Main, Germany.

The ability to detect airborne sound is essential for many animals. Examples from the inner ear of mammals and bushcrickets demonstrate that similar detection strategies evolved in taxonomically distant species. Both mammalian and bushcricket ears possess a narrow strip of sensory tissue that exhibits an anatomical gradient and traveling wave motion responses used for frequency discrimination. We measured pressure and motion in the bushcricket ear to investigate physical properties, stiffness, and mass, which govern the mechanical responses to sound. As in the mammalian cochlea, sound-induced fluid pressure and motion responses were tonotopically organized along the longitudinal axis of the crista acustica, the bushcricket's hearing organ. The fluid pressure at the crista and crista motion were used to calculate the acoustic impedance of the organ-bounded fluid mass (Z). We used a theoretical wave analysis of wavelength data from a previous study to predict the crista acustica stiffness. The wave analysis also predicts Z, and that result agreed reasonably well with the directly measured Z, lending support to the theoretical wave analysis. The magnitude of the crista stiffness was similar to basilar membrane stiffness in mammals, and as in mammals, the stiffness decreased from the high-frequency to the low-frequency region. At a given location, the stiffness increased with increasing frequency, corresponding to increasing curvature of the traveling wave (decreasing wavelength), indicating that longitudinal coupling plays a substantial role in determining crista stiffness. This is in contrast to the mammalian ear, in which stiffness is independent of frequency and longitudinal coupling is relatively small.
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http://dx.doi.org/10.1016/j.bpj.2018.11.3124DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6342706PMC
January 2019

PVDF-Based Piezoelectric Microphone for Sound Detection Inside the Cochlea: Toward Totally Implantable Cochlear Implants.

Trends Hear 2018 Jan-Dec;22:2331216518774450

4 Department of Otolaryngology Head and Neck Surgery, 21611 Columbia University Medical Center , New York City, NY, USA.

We report the fabrication and characterization of a prototype polyvinylidene fluoride polymer-based implantable microphone for detecting sound inside gerbil and human cochleae. With the current configuration and amplification, the signal-to-noise ratios were sufficiently high for normally occurring sound pressures and frequencies (ear canal pressures >50-60 dB SPL and 0.1-10 kHz), though 10 to 20 dB poorer than for some hearing aid microphones. These results demonstrate the feasibility of the prototype devices as implantable microphones for the development of totally implantable cochlear implants. For patients, this will improve sound reception by utilizing the outer ear and will improve the use of cochlear implants.
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http://dx.doi.org/10.1177/2331216518774450DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5987900PMC
March 2019

Signal competition in optical coherence tomography and its relevance for cochlear vibrometry.

J Acoust Soc Am 2017 01;141(1):395

Department of Otolaryngology, Head and Neck Surgery, and Department of Biomedical Engineering, Columbia University, 630 West 168th Street, New York, New York 10032, USA.

The usual technique for measuring vibration within the cochlear partition is heterodyne interferometry. Recently, spectral domain phase microscopy (SDPM) was introduced and offers improvements over standard heterodyne interferometry. In particular, it has a penetration depth of several mm due to working in the infrared range, has narrow and steep optical sectioning due to using a wideband light source, and is able to measure from several cochlear layers simultaneously. However, SDPM is susceptible to systematic error due to "phase leakage," in which the signal from one layer competes with the signal from other layers. Here, phase leakage is explored in vibration measurements in the cochlea and a model structure. The similarity between phase leakage and signal competition in heterodyne interferometry is demonstrated both experimentally and theoretically. Due to phase leakage, erroneous vibration amplitudes can be reported in regions of low reflectivity that are near structures of high reflectivity. When vibration amplitudes are greater than ∼0.1 of the light source wavelength, phase leakage can cause reported vibration waveforms to be distorted. To aid in the screening of phase leakage in experimental results, the error is plotted and discussed as a function of the important parameters of signal strength and vibration amplitude.
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http://dx.doi.org/10.1121/1.4973867DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5849049PMC
January 2017

The path of a click stimulus from ear canal to umbo.

Hear Res 2017 03 11;346:1-13. Epub 2017 Jan 11.

Department of Otolaryngology & Head and Neck Surgery, Department of Biomedical Engineering, Columbia University, 630 West 168th Street, P&S 11-452, New York, NY 10032, USA. Electronic address:

The tympanic membrane (TM) has a key role in transmitting sounds to the inner ear, but a concise description of how the TM performs this function remains elusive. This paper probes TM operation by applying a free field click stimulus to the gerbil ear and exploring the consequent motions of the TM and umbo. Motions of the TM were measured both on radial tracks starting close to the umbo and on a grid distal and adjacent to the umbo. The experimental results confirmed the high fidelity of sound transmission from the ear canal to the umbo. A delay of 5-15 μs was seen in the onset of TM motion between points just adjacent to the umbo and mid-radial points. The TM responded with a ringing motion, with different locations possessing different primary ringing frequencies. A simple analytic model from the literature, treating the TM as a string, was used to explore the experimental results. The click-based experiments and analysis led to the following description of TM operation: A transient sound pressure on the TM causes a transient initial TM motion that is maximal ∼ at the TM's radial midpoints. Mechanical forces generated by this initial prominent TM distortion then pull the umbo inward, leading to a delayed umbo response. The initial TM deformation also gives rise to prolonged mechanical ringing on the TM that does not result in significant umbo motion, likely due to destructive interference from the range of ringing frequencies. Thus, the umbo's response is a high-fidelity representation of the transient stimulus. Because any sound can be considered as a consecutive series of clicks, this description is applicable to any sound stimulus.
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http://dx.doi.org/10.1016/j.heares.2017.01.007DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5348280PMC
March 2017

Two-Tone Suppression of Simultaneous Electrical and Mechanical Responses in the Cochlea.

Biophys J 2016 Oct;111(8):1805-1815

Otalaryngology/Head & Neck Surgery and Biomedical Engineering, Columbia University, New York, New York. Electronic address:

Cochlear frequency tuning is based on a mildly tuned traveling-wave response that is enhanced in amplitude and sharpness by outer hair cell (OHC)-based forces. The nonlinear and active character of this enhancement is the fundamental manifestation of cochlear amplification. Recently, mechanical (pressure) and electrical (extracellular OHC-generated voltage) responses were simultaneously measured close to the sensory tissue's basilar membrane. Both pressure and voltage were tuned and showed traveling-wave phase accumulation, evidence that they were locally generated responses. Approximately at the frequency where nonlinearity commenced, the phase of extracellular voltage shifted up, to lead pressure by >1/4 cycle. Based on established and fundamental relationships among voltage, force, pressure, displacement, and power, the observed phase shift was identified as the activation of cochlear amplification. In this study, the operation of the cochlear amplifier was further explored, via changes in pressure and voltage responses upon delivery of a second, suppressor tone. Two different suppression paradigms were used, one with a low-frequency suppressor and a swept-frequency probe, the other with two swept-frequency tones, either of which can be considered as probe or suppressor. In the presence of a high-level low-frequency suppressor, extracellular voltage responses at probe-tone frequencies were greatly reduced, and the pressure responses were reduced nearly to their linear, passive level. On the other hand, the amplifier-activating phase shift between pressure and voltage responses was still present in probe-tone responses. These findings are consistent with low-frequency suppression being caused by the saturation of OHC electrical responses and not by a change in the power-enabling phasing of the underlying mechanics. In the two-tone swept-frequency suppression paradigm, mild suppression was apparent in the pressure responses, while deep notches could develop in the voltage responses. A simple analysis, based on a two-wave differencing scheme, was used to explore the observations.
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http://dx.doi.org/10.1016/j.bpj.2016.08.048DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5073056PMC
October 2016

An Intracochlear Pressure Sensor as a Microphone for a Fully Implantable Cochlear Implant.

Otol Neurotol 2016 12;37(10):1596-1600

*Department of Otolaryngology, Massachusetts Eye and Ear Infirmary, Harvard Medical School, Boston†Harvard Program in Speech and Hearing Bioscience and Technology, Cambridge, Massachusetts‡Department of Electrical Engineering§Department of Otolaryngology Head and Neck Surgery, Columbia University Medical Center¶Department of Biomedical Engineering, Columbia University, New York City, New York||Korea Advanced Institute of Science and Technology, Daejon, South Korea.

Objective: To validate an intracochlear piezoelectric sensor for its ability to detect intracochlear pressure and function as a microphone for a fully implantable cochlear implant.

Methods: A polyvinylidene fluoride (PVDF) piezoelectric pressure sensor was inserted into a human fresh cadaveric round window at varying depths. An external sound pressure stimulus was applied to the external auditory canal (EAC). EAC pressure, stapes velocity, and piezoelectric sensor voltage output were recorded.

Results: The PVDF sensor was able to detect the intracochlear sound pressure response to an acoustic input to the EAC. The frequency response of the pressure measured with the intracochlear sensor was similar to that of the pressure at the EAC, with the expected phase delay of the middle ear transmission. The magnitude of the response increased and smoothened with respect to frequency as the sensor was inserted more deeply into the scala tympani. Artifact measurements, made with the sensor in air near the round window, showed flat frequency response in both magnitude and phase, which were distinct from those measured when the sensor was inserted in the round window.

Conclusion: This study describes a novel method of measuring intracochlear pressure for an otologic microphone composed of a piezoelectric polymer, and demonstrates feasibility. Our next goal is to improve device sensitivity and bandwidth. Our long-term objective is to imbed the piezoelectric sensor within a conventional cochlear implant electrode, to enable a device to both measure intracochlear sound pressure and deliver electrical stimulus to the cochlea, for a fully implantable cochlear implant.
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http://dx.doi.org/10.1097/MAO.0000000000001209DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5102785PMC
December 2016

Cochlear perfusion with a viscous fluid.

Hear Res 2016 07 21;337:1-11. Epub 2016 May 21.

Department of Biomedical Engineering, Columbia University, New York, NY 10025, USA; Department of Otolaryngology-Head & Neck Surgery, Columbia University, New York, NY 10032, USA. Electronic address:

The flow of viscous fluid in the cochlea induces shear forces, which could provide benefit in clinical practice, for example to guide cochlear implant insertion or produce static pressure to the cochlear partition or wall. From a research standpoint, studying the effects of a viscous fluid in the cochlea provides data for better understanding cochlear fluid mechanics. However, cochlear perfusion with a viscous fluid may damage the cochlea. In this work we studied the physiological and anatomical effects of perfusing the cochlea with a viscous fluid. Gerbil cochleae were perfused at a rate of 2.4 μL/min with artificial perilymph (AP) and sodium hyaluronate (Healon, HA) in four different concentrations (0.0625%, 0.125%, 0.25%, 0.5%). The different HA concentrations were applied either sequentially in the same cochlea or individually in different cochleae. The perfusion fluid entered from the round window and was withdrawn from basal scala vestibuli, in order to perfuse the entire perilymphatic space. Compound action potentials (CAP) were measured after each perfusion. After perfusion with increasing concentrations of HA in the order of increasing viscosity, the CAP thresholds generally increased. The threshold elevation after AP and 0.0625% HA perfusion was small or almost zero, and the 0.125% HA was a borderline case, while the higher concentrations significantly elevated CAP thresholds. Histology of the cochleae perfused with the 0.0625% HA showed an intact Reissner's membrane (RM), while in cochleae perfused with 0.125% and 0.25% HA RM was torn. Thus, the CAP threshold elevation was likely due to the broken RM, likely caused by the shear stress produced by the flow of the viscous fluid. Our results and analysis indicate that the cochlea can sustain, without a significant CAP threshold shift, up to a 1.5 Pa shear stress. Beside these finding, in the 0.125% and 0.25% HA perfusion cases, a temporary CAP threshold shift was observed, perhaps due to the presence and then clearance of viscous fluid within the cochlea, or to a temporary position shift of the Organ of Corti. After 0.5% HA perfusion, a short latency positive peak (P0) appeared in the CAP waveform. This P0 might be due to a change in the cochlea's traveling-wave pattern, or distortion in the cochlear microphonic.
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http://dx.doi.org/10.1016/j.heares.2016.05.007DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4912859PMC
July 2016

Intracochlear Scala Media Pressure Measurement: Implications for Models of Cochlear Mechanics.

Biophys J 2015 Dec;109(12):2678-2688

Department of Otolaryngology, Columbia University, New York, New York; Department of Biomedical Engineering, Columbia University, New York, New York.

Models of the active cochlea build upon the underlying passive mechanics. Passive cochlear mechanics is based on physical and geometrical properties of the cochlea and the fluid-tissue interaction between the cochlear partition and the surrounding fluid. Although the fluid-tissue interaction between the basilar membrane and the fluid in scala tympani (ST) has been explored in both active and passive cochleae, there was no experimental data on the fluid-tissue interaction on the scala media (SM) side of the partition. To this aim, we measured sound-evoked intracochlear pressure in SM close to the partition using micropressure sensors. All the SM pressure data are from passive cochleae, likely because the SM cochleostomy led to loss of endocochlear potential. Thus, these experiments are studies of passive cochlear mechanics. SM pressure close to the tissue showed a pattern of peaks and notches, which could be explained as an interaction between fast and slow (i.e., traveling wave) pressure modes. In several animals SM and ST pressure were measured in the same cochlea. Similar to previous studies, ST-pressure was dominated by a slow, traveling wave mode at stimulus frequencies in the vicinity of the best frequency of the measurement location, and by a fast mode above best frequency. Antisymmetric pressure between SM and ST supported the classic single-partition cochlear models, or a dual-partition model with tight coupling between partitions. From the SM and ST pressure we calculated slow and fast modes, and from active ST pressure we extrapolated the passive findings to the active case. The passive slow mode estimated from SM and ST data was low-pass in nature, as predicted by cochlear models.
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http://dx.doi.org/10.1016/j.bpj.2015.10.052DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4699921PMC
December 2015

A study of sound transmission in an abstract middle ear using physical and finite element models.

J Acoust Soc Am 2015 Nov;138(5):2972-85

Department of Otolaryngology/Head and Neck Surgery and Department of Biomedical Engineering, Columbia University, New York, New York 10032, USA.

The classical picture of middle ear (ME) transmission has the tympanic membrane (TM) as a piston and the ME cavity as a vacuum. In reality, the TM moves in a complex multiphasic pattern and substantial pressure is radiated into the ME cavity by the motion of the TM. This study explores ME transmission with a simple model, using a tube terminated with a plastic membrane. Membrane motion was measured with a laser interferometer and pressure on both sides of the membrane with micro-sensors that could be positioned close to the membrane without disturbance. A finite element model of the system explored the experimental results. Both experimental and theoretical results show resonances that are in some cases primarily acoustical or mechanical and sometimes produced by coupled acousto-mechanics. The largest membrane motions were a result of the membrane's mechanical resonances. At these resonant frequencies, sound transmission through the system was larger with the membrane in place than it was when the membrane was absent.
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http://dx.doi.org/10.1121/1.4934515DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4644151PMC
November 2015

Microperforations significantly enhance diffusion across round window membrane.

Otol Neurotol 2015 Apr;36(4):694-700

*Department of Otolaryngology-Head and Neck Surgery, Columbia University College of Physicians and Surgeons; †Department of Mechanical Engineering; and ‡Department of Biomedical Engineering, Columbia University, New York, New York, U.S.A.

Hypothesis: Introduction of microperforations in round window membrane (RWM) will allow reliable and predictable intracochlear delivery of pharmaceutical, molecular, or cellular therapeutic agents.

Background: Reliable delivery of medications into the inner ear remains a formidable challenge. The RWM is an attractive target for intracochlear delivery. However, simple diffusion across intact RWM is limited by what material can be delivered, size of material to be delivered, difficulty with precise dosing, timing, and precision of delivery over time. Further, absence of reliable methods for measuring diffusion across RWM in vitro is a significant experimental impediment.

Methods: A novel model for measuring diffusion across guinea pig RWM, with and without microperforation, was developed and tested: cochleae, sparing the RWM, were embedded in 3D-printed acrylic holders using hybrid dental composite and light cured to adapt the round window niche to 3 ml Franz diffusion cells. Perforations were created with 12.5-μm-diameter needles and examined with light microscopy. Diffusion of 1 mM Rhodamine B across RWM in static diffusion cells was measured via fluorescence microscopy.

Results: The diffusion cell apparatus provided reliable and replicable measurements of diffusion across RWM. The permeability of Rhodamine B across intact RWM was 5.1 × 10(9-) m/s. Manual application of microperforation with a 12.5-μm-diameter tip produced an elliptical tear removing 0.22 ± 0.07% of the membrane and was associated with a 35× enhancement in diffusion (P < 0.05).

Conclusion: Diffusion cells can be applied to the study of RWM permeability in vitro. Microperforation in RWM is an effective means of increasing diffusion across the RWM.
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http://dx.doi.org/10.1097/MAO.0000000000000629DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4359065PMC
April 2015

A novel perfusion-based method for cochlear implant electrode insertion.

Hear Res 2014 Aug 29;314:33-41. Epub 2014 May 29.

Department of Otolaryngology-Head & Neck Surgery, Columbia University, New York, NY 10032, USA; Department of Biomedical Engineering, Columbia University, New York, NY 10025, USA.

A cochlear implant (CI) restores partial hearing to profoundly deaf individuals. CI electrodes are inserted manually in the cochlea and surgeons rely on tactile feedback from the implant to determine when to stop the insertion. This manual insertion method results in a large degree of variability in surgical outcomes and intra-cochlear trauma. Additionally, implants often span only the basal turn. In the present study we report on the development of a new method to assist CI electrode insertion. The design objectives are (1) an automated and standardized insertion technique across patients with (2) more apical insertion than is possible by the contemporary methods, while (3) minimizing insertion trauma. The method relies on a viscous fluid flow through the cochlea to carry the electrode array with it. A small cochleostomy (∼100-150 um in diameter) is made in scala vestibuli (SV) and the round window (RW) membrane is opened. A flow of diluted Sodium Hyaluronate (also known as Hyaluronic Acid, (HA)) is set up from the RW to the SV opening using a perfusion pump that sets up a unidirectional flow. Once the flow is established an implant is dropped into the ongoing flow. Here we present a proof-of-concept study where we used this technique to insert silicone implants all the way to the cochlear apex in rats and gerbils. In light-microscopic histology, the implantation occurred without cochlear trauma. To further assess the ototoxicity of the HA perfusion, we measured compound action potential (CAP) thresholds following the perfusion of HA, and found that the CAP thresholds were substantially elevated. Thus, at this point the method is promising, and requires further development to become clinically viable.
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http://dx.doi.org/10.1016/j.heares.2014.05.003DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4143137PMC
August 2014

External and middle ear sound pressure distribution and acoustic coupling to the tympanic membrane.

J Acoust Soc Am 2014 Mar;135(3):1294-312

Department of Otolaryngology & Head and Neck Surgery, Department of Biomedical Engineering, Columbia University, 630 West 168th Street, P&S 11-452 New York, New York 10032.

Sound energy is conveyed to the inner ear by the diaphanous, cone-shaped tympanic membrane (TM). The TM moves in a complex manner and transmits sound signals to the inner ear with high fidelity, pressure gain, and a short delay. Miniaturized sensors allowing high spatial resolution in small spaces and sensitivity to high frequencies were used to explore how pressure drives the TM. Salient findings are: (1) A substantial pressure drop exists across the TM, and varies in frequency from ∼10 to 30 dB. It thus appears reasonable to approximate the drive to the TM as being defined solely by the pressure in the ear canal (EC) close to the TM. (2) Within the middle ear cavity (MEC), spatial variations in sound pressure could vary by more than 20 dB, and the MEC pressure at certain locations/frequencies was as large as in the EC. (3) Spatial variations in pressure along the TM surface on the EC-side were typically less than 5 dB up to 50 kHz. Larger surface variations were observed on the MEC-side.
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http://dx.doi.org/10.1121/1.4864475DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3985947PMC
March 2014

Detection of cochlear amplification and its activation.

Biophys J 2013 Aug;105(4):1067-78

Otolaryngology, Head and Neck Surgery, Columbia University, New York, NY, USA.

The operation of the mammalian cochlea relies on a mechanical traveling wave that is actively boosted by electromechanical forces in sensory outer hair cells (OHCs). This active cochlear amplifier produces the impressive sensitivity and frequency resolution of mammalian hearing. The cochlear amplifier has inspired scientists since its discovery in the 1970s, and is still not well understood. To explore cochlear electromechanics at the sensory cell/tissue interface, sound-evoked intracochlear pressure and extracellular voltage were measured using a recently developed dual-sensor with a microelectrode attached to a micro-pressure sensor. The resulting coincident in vivo observations of OHC electrical activity, pressure at the basilar membrane and basilar membrane displacement gave direct evidence for power amplification in the cochlea. Moreover, the results showed a phase shift of voltage relative to mechanical responses at frequencies slightly below the peak, near the onset of amplification. Based on the voltage-force relationship of isolated OHCs, the shift would give rise to effective OHC pumping forces within the traveling wave peak. Thus, the shift activates the cochlear amplifier, serving to localize and thus sharpen the frequency region of amplification. These results are the most concrete evidence for cochlear power amplification to date and support OHC somatic forces as its source.
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http://dx.doi.org/10.1016/j.bpj.2013.06.049DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3752116PMC
August 2013

Sound transmission along the ossicular chain in common wild-type laboratory mice.

Hear Res 2013 Jul 23;301:27-34. Epub 2012 Nov 23.

Department of Otolaryngology, Head and Neck Surgery, Columbia University, P&S 11-452, 630 West 168th Street, New York, NY 10032, USA.

The use of genetically modified mice can accelerate progress in auditory research. However, the fundamental profile of mouse hearing has not been thoroughly documented. In the current study, we explored mouse middle ear transmission by measuring sound-evoked vibrations at several key points along the ossicular chain using a laser-Doppler vibrometer. Observations were made through an opening in pars flaccida. Simultaneously, the pressure at the tympanic membrane close to the umbo was monitored using a micro-pressure-sensor. Measurements were performed in C57BL mice, which are widely used in hearing research. Our results show that the ossicular local transfer function, defined as the ratio of velocity to the pressure at the tympanic membrane, was like a high-pass filter, almost flat at frequencies above ∼15 kHz, decreasing rapidly at lower frequencies. There was little phase accumulation along the ossicles. Our results suggested that the mouse ossicles moved almost as a rigid body. Based on these 1-dimensional measurements, the malleus-incus-complex primarily rotated around the anatomical axis passing through the gonial termination of the anterior malleus and the short process of the incus, but secondary motions were also present. This article is part of a special issue entitled "MEMRO 2012".
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http://dx.doi.org/10.1016/j.heares.2012.11.015DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3669248PMC
July 2013

Von Békésy and cochlear mechanics.

Hear Res 2012 Nov 22;293(1-2):31-43. Epub 2012 May 22.

OTO/HNS and Biomedical Engineering, Columbia University, NY, USA.

Georg Békésy laid the foundation for cochlear mechanics, foremost by demonstrating the traveling wave that is the substrate for mammalian cochlear mechanical processing. He made mechanical measurements and physical models in order to understand that fundamental cochlear response. In this tribute to Békésy we make a bridge between modern traveling wave observations and those of Békésy, discuss the mechanical properties and measurements that he considered to be so important, and touch on the range of computational traveling wave models.
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http://dx.doi.org/10.1016/j.heares.2012.04.017DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3572775PMC
November 2012

Subharmonic distortion in ear canal pressure and intracochlear pressure and motion.

J Assoc Res Otolaryngol 2012 Aug 24;13(4):461-71. Epub 2012 Apr 24.

Department of Biomedical Engineering, Columbia University, New York, NY, USA.

When driven at sound pressure levels greater than ~110 dB stimulus pressure level, the mammalian middle ear is known to produce subharmonic distortion. In this study, we simultaneously measured subharmonics in the ear canal pressure, intracochlear pressure, and basilar membrane or round window membrane velocity, in gerbil. Our primary objective was to quantify the relationship between the subharmonics measured in the ear canal and their intracochlear counterparts. We had two primary findings: (1) The subharmonics emerged suddenly, with a substantial amplitude in the ear canal and the cochlea; (2) at the stimulus level for which subharmonics emerged, the pressure in scala vestibuli/pressure in the ear canal amplitude relationship was similar for the subharmonic and fundamental components. These findings are important for experiments and clinical conditions in which high sound pressure level stimuli are used and could lead to confounding subharmonic stimulation.
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http://dx.doi.org/10.1007/s10162-012-0326-3DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3387311PMC
August 2012

Reverse transmission along the ossicular chain in gerbil.

J Assoc Res Otolaryngol 2012 Aug 31;13(4):447-59. Epub 2012 Mar 31.

Department of Otolaryngology, Head and Neck Surgery, Columbia University, 630 West 168th Street, New York, NY 10032, USA.

In a healthy cochlea stimulated with two tones f (1) and f (2), combination tones are generated by the cochlea's active process and its associated nonlinearity. These distortion tones travel "in reverse" through the middle ear. They can be detected with a sensitive microphone in the ear canal (EC) and are known as distortion product otoacoustic emissions. Comparisons of ossicular velocity and EC pressure responses at distortion product frequencies allowed us to evaluate the middle ear transmission in the reverse direction along the ossicular chain. In the current study, the gerbil ear was stimulated with two equal-intensity tones with fixed f (2)/f (1) ratio of 1.05 or 1.25. The middle ear ossicles were accessed through an opening of the pars flaccida, and their motion was measured in the direction in line with the stapes piston-like motion using a laser interferometer. When referencing the ossicular motion to EC pressure, an additional amplitude loss was found in reverse transmission compared to the gain in forward transmission, similar to previous findings relating intracochlear and EC pressure. In contrast, sound transmission along the ossicular chain was quite similar in forward and reverse directions. The difference in middle ear transmission in forward and reverse directions is most likely due to the different load impedances-the cochlea in forward transmission and the EC in reverse transmission.
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http://dx.doi.org/10.1007/s10162-012-0320-9DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3387306PMC
August 2012

On cochlear impedances and the miscomputation of power gain.

J Assoc Res Otolaryngol 2011 Dec 27;12(6):671-6. Epub 2011 Sep 27.

Eaton-Peabody Laboratories, Massachusetts Eye and Ear Infirmary, Boston, MA 02114, USA.

In their article, "Measurement of cochlear power gain in the sensitive gerbil ear," Ren et al. (Nat Commun 2:216, 2011) claim to provide "the first direct experimental evidence of power amplification in the sensitive living cochlea." While we recognize the technical challenges of the experiments and appreciate the beauty of the data, the authors' analysis and interpretation of the measurements are invalid. We review the concept of impedance (i.e., the ratio of pressure to velocity) as it applies to cochlear mechanics and show that Ren et al. mistakenly equate the impedances near the basilar membrane and stapes with the impedance characteristic of an infinite, uniform tube of fluid. As a consequence of this error, Ren et al.'s measurements and analysis provide no evidence for power amplification in the cochlea. Compelling evidence for power amplification has, however, been previously provided by others.
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http://dx.doi.org/10.1007/s10162-011-0287-yDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3214245PMC
December 2011
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