Basilar membrane vibration in the basal turn of the sensitive gerbil cochlea
Introduction
The most straightforward technique for studying cochlear mechanics is to measure cochlear partition vibration directly. Because it is more easily accessible than the organ of Corti and the tectorial membrane, the basilar membrane (BM) has been the most commonly used location for vibration measurement in the cochlea. Measurements of BM vibration have been accomplished with a variety of techniques in a number of different animal species.
Georg von Békésy’s BM vibration experiments in the early part of the last century were accomplished with great success using light microscopy (von Bekesy, 1960). However, a major problem with light microscopy techniques is low sensitivity, which essentially limits the observations to vibration amplitudes greater than about 1 μm (Tonndorf, 1977). Although the capacitive probe method provides better sensitivity than light microscopy (Wilson, 1973), the requirement of removal of perilymph from the scala tympani may alter cochlear mechanical properties (Robertson, 1974). Use of the Mössbauer technique for BM measurements was a major technical improvement, leading to a series of very important findings (Johnstone and Boyle, 1967, LePage, 1987, Rhode, 1971, Sellick et al., 1982). The main disadvantages of this approach are its nonlinearity, low signal to noise ratio, the load on the BM, and possible radioactive damage (Kliauga and Khanna, 1983). LePage (1989) and Xue et al. (1996) applied fiber optic displacement sensors to measure BM vibration using incoherent light from a light-emitting diode. The difficulties in positioning the sensor close to the BM without damage and the load on the BM by the reflector and the probe limit application of this method.
Currently, a widely used method for cochlear mechanical measurement is laser interferometry (Khanna and Leonard, 1982, Willemin et al., 1988), due to its high sensitivity and ease of use. High sensitivity and the linearity of the laser interferometer give this technique a wide dynamic range and high signal to noise ratio, both of which are necessary for BM measurement. However, the reflection coefficient of the cochlear partition is extremely low, approximately 0.0039–0.033% (Khanna et al., 1989). Most measurements using laser interferometry require application of reflective objects (gold crystals or beads of various materials) on the cochlear partition (Cooper and Rhode, 1995, Gummer et al., 1996, Khanna and Leonard, 1982, Mammano and Ashmore, 1993, Nuttall et al., 1991, Nuttall et al., 1999, Rhode and Cooper, 1993, Rhode and Cooper, 1996, Ruggero and Rich, 1991a, Ruggero et al., 1997). These measurements have provided considerable data for understanding cochlear mechanics. Nevertheless, and in spite of Cooper’s (1999) report that placing a bead did not change the mechanical response of the BM, there still remains a concern regarding possible effects of the reflective object on the mechanical properties of the cochlear partition. It has been suggested that a reflective object or a Mössbauer source placed on the BM may cause a loss in sensitivity (Khanna and Leonard, 1982, Xue et al., 1996). Additionally, the load of the reflective object may alter the motion pattern of the cochlear partition (Sellick et al., 1983b). Moreover, it is uncertain whether the mechanical coupling between the cochlear partition and the reflective object contributes to results (Khanna et al., 1998). These concerns and the desire for multiple-point measurement have motivated researchers to develop a technique for measurement of cochlear partition vibration in the sensitive cochlea without placing reflective objects (Cooper, 1999, Khanna and Hao, 1999, Russell and Nilsen, 1997).
Although the gerbil is one of the most common animals for auditory research, data on BM mechanics in this species are limited. The aim of this study is to develop a method of measuring BM vibration of the first turn in sensitive gerbil cochleae without placing a reflective object. To visualize the cochlear partition of the first turn, a hole was made in the bony capsule. Using a modified heterodyne laser interferometer microscope, the BM velocity in response to an acoustical tone was measured at different frequencies and levels.
Section snippets
Animals and surgical approach
Thirty healthy young Mongolian gerbils (45–90 g) were used in this study. Animals were housed in American Association for Accreditation of Laboratory Animal Care-approved facilities. Experimental protocols were approved by the Oregon Health Sciences University Committee on Use and Care of Animals.
The general animal preparation and surgical approach for opening the bulla were the same as in a previous study (Ren, 1996). The initial anesthesia was induced by intraperitoneal injection of ketamine
Results
The main factor limiting productivity of this experiment is preparation-induced cochlear damage. Of the 30 animals used in this study, two died during the experiment. Although 28 animals survived from the surgery and showed normal cardiovascular condition, most of them had different degrees of the hearing loss resulting from the preparation procedures. Only five animals had less than a 10 dB threshold increase at 12 and 18 kHz. Data from three of these relatively sensitive cochleae are reported
Mechanical frequency tuning curves
Frequency tuning curves have been used to describe frequency selectivity in different systems. In this study, the mechanical frequency tuning curves (FTCs) at different input levels were measured and produced by plotting the amplitude of the BM vibration velocity amplitude as a function of stimulus frequency for a given sound pressure level in the external ear canal (Fig. 2A). For the region of the BM accessible to measurement in this study, the FTCs at low sound pressure levels (below 40 dB
Summary
Using a newly developed laser interferometer, velocity responses of the BM to different levels of acoustical tones were measured, without a reflective bead, from the basal cochlear turn in sensitive and post-mortem cochleae. This study provides basic information on BM mechanical properties at the basal turn of the gerbil cochlea. It was found that the peak velocity response, indicating best frequency, is level dependent, with a half octave or more shift toward low frequencies with stimulus
Acknowledgements
Supported in part by research grants from the National Institute of Deafness and Other Communication Disorders (R01 DC000105, PO1 0078 and R03 DC033642), the National Institutes of Health, the Research Fund of the American Otological Society, the Medical Research Foundation of Oregon, and VA RR and D Center Grant RCTR-597-0160, Portland, VAMC.
References (42)
An improved heterodyne laser interferometer for use in studies of cochlear mechanics
J. Neurosci. Methods
(1999)- et al.
Basilar membrane tonotopicity in the hook region of the cat cochlea
Hear. Res.
(1992) - et al.
Nonlinear mechanics at the apex of the guinea-pig cochlea
Hear. Res.
(1995) - et al.
Nonlinearity in the apical turn of living guinea pig cochlea
Hear. Res.
(1999) - et al.
Vibration of reflective beads placed on the basilar membrane
Hear. Res.
(1998) Functional role of the olivo-cochlear bundle: A motor unit control system in the mammallian cochlea
Hear. Res.
(1989)- et al.
Rapid force production in the cochlea
Hear. Res.
(1989) - et al.
Laser Doppler velocimetry of basilar membrane vibration
Hear. Res.
(1991) - et al.
The radial pattern of basilar membrane motion evoked by electric stimulation of the cochlea
Hear. Res.
(1999) Acoustic modulation of electrically evoked distortion production otoacoustic emissions in gerbil cochlea
Neurosci. Lett.
(1996)
A reversible ischemia model in gerbil cochlea
Hear. Res.
Two-tone suppression and distortion production on the basilar membrane in the hook region of cat and guinea pig cochleae
Hear. Res.
Application of a commercially-manufactured Doppler-shift laser velocimeter to the measurement of basilar-membrane vibration
Hear. Res.
Comparison between the tuning properties of inner hair cells and basilar membrane motion
Hear. Res.
The influence of Mossbauer source size and position on phase and amplitude measurements of the guinea pig basilar membrane
Hear. Res.
A sub-miniature capacitative probe for vibration measurements of the basilar membrane
J. Sound Vib.
Temporal position of discharges in single auditory nerve fibers within the cycle of a sine-wave stimulus: frequency and intensity effects
J. Acoust. Soc. Am.
Resonant tectorial membrane motion in the inner ear: its crucial role in frequency tuning
Proc. Natl. Acad. Sci. USA
Basilar membrane vibration examined with the Mossbauer technique
Science
Basilar membrane tuning in the cat cochlea
Science
Cited by (103)
An outer hair cell-powered global hydromechanical mechanism for cochlear amplification
2022, Hearing ResearchCitation Excerpt :To understand how the OHC-driven RL vibration interacts with the BM vibration, we measured the time relationship between the RL and BM vibration. The acoustically induced RL and BM vibrations were measured in the gerbil, one of the most commonly used animals for auditory research (He, et al., 2018; Ren and Nuttall, 2001). The group-delay difference between the RL and BM vibrations was derived from the slope of the phase difference, which was obtained by subtracting the BM phase from the RL phase.
Inner hair cell stereocilia displacement in response to focal stimulation of the basilar membrane in the ex vivo gerbil cochlea
2021, Hearing ResearchCitation Excerpt :Theoretical and experimental evidence suggests that to a rough approximation, the complex anatomy of the CP can be simplified to a tuned mechanical plate, and the mechanical parameters (impedance) can be deduced by knowledge of the pressure across, and transverse velocity of the CP (Peterson and Bogert, 1950). Many measurements of BM displacement and velocity were reported in the transverse direction (figure 1) (Ren and Nuttall, 2001; Rhode, 1971; Versteegh and Van Der Heijden, 2012; von Bekesy, 1960). While transverse BM measurements provide biomechanically relevant information about the dynamics of the BM, the inner hair cells (IHC) mechanosensitive poles respond to bending of their stereocilia.
The interplay of organ-of-Corti vibrational modes, not tectorial- membrane resonance, sets outer-hair-cell stereocilia phase to produce cochlear amplification
2020, Hearing ResearchCitation Excerpt :However, the effect of the negative feedback on BM motion from OHC-motility is expected to be small, almost linear, and not easily distinguishable from the normal variation from one measurement to the next. Nonetheless, there is evidence for expansive growth of BM motion at below-CF frequencies that is consistent with BM motion at low frequencies and low levels being reduced a small amount by negative feedback from OHC length changes (Ren and Nuttall, 2001; Rhode, 2007; Versteegh and van der Heijden, 2012). At frequencies considerably below the OHC membrane-time-constant corner frequency, the phase of OHC motility is 90° from the phase for producing positive or negative feedback (Fig. 2A, double-arrow-up vs. X).
Power Dissipation in the Cochlea Can Enhance Frequency Selectivity
2019, Biophysical Journal