Timing of cochlear feedback: spatial and temporal representation of a tone across the basilar membrane

Nilsen, K. E.; Russell, Ian J.

doi:10.1038/10197

Cited by 58 publications

(38 citation statements)

References 37 publications

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“…Tone-evoked BM displacements can be measured through the interaction of light within the laser diode and reflections from the surface of the BM. Measurements at up to 15 different locations across the width of the BM were made from nine animals in response to the CF of the recording site (22). Tones of varying sound pressure level (SPL), expressed in dB (dB relative to 2 ϫ 10 Ϫ5 Pa), were used in the experiments.…”

Section: Amplification Of Bm Vibrations Is Greatest In the Organ Of Cmentioning

confidence: 99%

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The spatial and temporal representation of a tone on the guinea pig basilar membrane

Nilsen

Russell

2000

Proc. Natl. Acad. Sci. U.S.A.

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In the mammalian cochlea, the basilar membrane's (BM) mechanical responses are amplified, and frequency tuning is sharpened through active feedback from the electromotile outer hair cells (OHCs). To be effective, OHC feedback must be delivered to the correct region of the BM and introduced at the appropriate time in each cycle of BM displacement. To investigate when OHCs contribute to cochlear amplification, a laser-diode interferometer was used to measure tone-evoked BM displacements in the basal turn of the guinea pig cochlea. Measurements were made at multiple sites across the width of the BM, which are tuned to the same characteristic frequency (CF). In response to CF tones, the largest displacements occur in the OHC region and phase lead those measured beneath the outer pillar cells and adjacent to the spiral ligament by about 90°. Postmortem, responses beneath the OHCs are reduced by up to 65 dB, and all regions across the width of the BM move in unison. We suggest that OHCs amplify BM responses to CF tones when the BM is moving at maximum velocity. In regions of the BM where OHCs contribute to its motion, the responses are compressive and nonlinear. We measured the distribution of nonlinear compressive vibrations along the length of the BM in response to a single frequency tone and estimated that OHC amplification is restricted to a 1.25-to 1.40-mm length of BM centered on the CF place.cochlear amplifier ͉ outer hair cell ͉ frequency selectivity ͉ laser-diode interferometry v on Békésy (1) discovered that sound-induced stapes movement causes a wave of basilar membrane (BM) displacement to travel from the base of the cochlea to the apex because of a pressure difference set up across the cochlear partition. The length of the BM is graded in stiffness, and the cochlear partition can be modeled as a series of weakly coupled sections, each section comprised of a rigid mass connected to the sides of the cochlea by springs that decrease in stiffness toward the apex (2). The BM will resonate when the mechanical impedance caused by the stiffness of the springs cancels that caused by the mass of the section (1). At a point just basal to the resonant place, a peak of displacement will occur on the BM. At a point just apical to the resonant place, the BM impedance is insufficient to maintain a pressure difference across the cochlear partition, and the traveling wave dies out. The location of the displacement peak depends on stimulus frequency, so that each segment of the BM is tuned to a characteristic frequency (CF). von Békésy measured BM movement under postmortem conditions and found that the mechanical responses were broadly tuned and insensitive. Subsequent measurements made from sensitive cochleae in vivo have revealed that, in fact, BM displacement responses are sharply tuned and very sensitive at low sound-pressure levels (3-6).Contributions from the electromotile outer hair cells (OHCs) (7-10) appear to be essential for cochlear sensitivity and frequency tuning (11,12). Many current models of cochlear functi...

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Section: Amplification Of Bm Vibrations Is Greatest In the Organ Of Cmentioning

confidence: 99%

“…The basal turn of the cochlea was exposed in guinea pigs that were under deep neuroleptanalgesia, and an opening was made in the scala tympani (22) (Fig. 1c).…”

Section: Amplification Of Bm Vibrations Is Greatest In the Organ Of Cmentioning

confidence: 99%

The spatial and temporal representation of a tone on the guinea pig basilar membrane

Nilsen

Russell

2000

Proc. Natl. Acad. Sci. U.S.A.

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“…Both monophasic (18) and multiphasic (19) responses have been reported in the basal turn of the guinea pig cochlea. Whereas the BM is accessible at the base, the TM and organ of Corti (OC) are not.…”

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confidence: 99%

Evidence of tectorial membrane radial motion in a propagating mode of a complex cochlear model

Cai

Shoelson

Chadwick

2004

Proc. Natl. Acad. Sci. U.S.A.

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Knowledge of vibratory patterns in the cochlea is crucial to understanding the stimulation of mechanosensory cells. Experiments to determine the motion of the cochlear partition and surrounding fluid are extremely challenging. As a result, the motion data are incomplete and often contradictory. The bending mechanism of hair bundles, thought to be related to the shear motion and endolymphatic flow between the tectorial membrane (TM) and reticular lamina (RL), is controversial. We, therefore, extend the frequency range of our previous hybrid analytical-finite-element approach to model the basal as well as apical regions of the guinea pig cochlea. We solve the fluid-solid interaction eigenvalue problem for the axial wavenumber, fluid pressure, and vibratory relative motions of the cochlear partition as a function of frequency. A simple monophasic vibratory mode of the basilar membrane is found at both ends of the cochlea. However, this simple movement is associated with a complex frequency-dependent relative deformation between the TM and the RL. We provide evidence of a radial component of TM motion that is out of phase with the RL and that facilitates the bending of outer hair cell stereocilia at appropriate frequencies at both the cochlear base and apex.A dynamic fluid-structure interaction occurs when the cochlea is stimulated by environmental sounds. This interaction elicits a transverse wave on the cochlear partition (CP), which travels from the base to the apex of the spiral-shaped hearing organ. Details of the vibratory mode shape of this traveling wave are directly related to the bending of hair bundles and, therefore, are very important to the understanding of the stimulation of inner hair cells (IHCs) and outer hair cells (OHCs), which lies at the very core of hearing transduction (1, 2). The tectorial membrane (TM) radial resonance is thought to be one potential bending mechanism of the stereocilia. The origin and evolution of ideas concerning the radial motion of the TM is discussed fully in Zwislocki's recent monograph (3). In short, new ideas were needed to resolve discrepancies in both amplitude and phase of the tuning of mechanical, neural, and cellular responses. TM radial motion, consequently, was incorporated in mathematical models of cochlear micromechanics by using the lumped-parameter approach (1, 3-9). Although indirect evidence inferred from frequency tuning of otoacoustic emissions (10, 11) and cochlear microphonics (12) lent support to the idea of radial TM motion, direct evidence awaited the measurements of Gummer et al. (13) and Hemmert et al. (14). These latter findings contrast those of Ulfendahl et al. (15), who reported almost no radial motion of the TM. Preliminary observations of TM motion in the hemicochlea preparation also do not yet show a significant TM radial motion (16,17). It seems that the local excitation in that preparation has difficulty in exciting a significantly propagating mode, which could affect the TM motion.Another controversy involves the transverse mode shape...

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“…We assume that the maximal displacements of the basilar membrane for two cells ͑two CFs͒ are the same and equal to the displacement considered in the first set of figures. The level of the basilar membrane maximal displacement was chosen at 1 nm, which corresponds to about 30-40 dB SPL ͑e.g., Nilsen and Russell, 1999;Fridberger et al, 2004͒. According to Eq.…”

Section: Resultsmentioning

confidence: 99%

Outer hair cell active force generation in the cochlear environment

Liao

Feng

Popel

et al. 2007

The Journal of the Acoustical Society of America

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Outer hair cells are critical to the amplification and frequency selectivity of the mammalian ear acting via a fine mechanism called the cochlear amplifier, which is especially effective in the high-frequency region of the cochlea. How this mechanism works under physiological conditions and how these cells overcome the viscous (mechanical) and electrical (membrane) filtering has yet to be fully understood. Outer hair cells are electromotile, and they are strategically located in the cochlea to generate an active force amplifying basilar membrane vibration. To investigate the mechanism of this cell's active force production under physiological conditions, a model that takes into account the mechanical, electrical, and mechanoelectrical properties of the cell wall (membrane) and cochlear environment is proposed. It is shown that, despite the mechanical and electrical filtering, the cell is capable of generating a frequency-tuned force with a maximal value of about 40 pN. It is also found that the force per unit basilar membrane displacement stays essentially the same (40 pNnm) for the entire linear range of the basilar membrane responses, including sound pressure levels close to hearing threshold. Our findings can provide a better understanding of the outer hair cell's role in the cochlear amplifier.

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Timing of cochlear feedback: spatial and temporal representation of a tone across the basilar membrane

Cited by 58 publications

References 37 publications

The spatial and temporal representation of a tone on the guinea pig basilar membrane

The spatial and temporal representation of a tone on the guinea pig basilar membrane

Evidence of tectorial membrane radial motion in a propagating mode of a complex cochlear model

Outer hair cell active force generation in the cochlear environment

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