A Micromechanical Contribution to Cochlear Tuning and Tonotopic Organization

Holton, Thomas; Hudspeth, A. J.

doi:10.1126/science.6623089

Cited by 125 publications

(40 citation statements)

References 21 publications

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“…Systematic variation of stereovillar height is known to be correlated with the tonotopic organization of hair cells (e.g., in the alligator lizard, Holton and Hudspeth, 1983). Our data in the starling and the pigeon show an increase of stereovillar height from about 3 pm near the base up to more than 10 pm at the apex, without systematic variation over the width of the papilla (Fig.…”

Section: Resultssupporting

confidence: 59%

Quantitative morphological analysis of the sensory epithelium of the starling and pigeon basilar papilla

Gleich

Manley

1988

Hearing Research

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Several features of bird basilar papilla morphology were quantitatively studied in the starling and the pigcon in order to attempt a structure-function correlation. We confirmed and quantified several findings from earlier studies, but also obtained results contradictory to previous reports. The greatest discrepancies concerned the pattern of hair cell orientation. By including the results from other investigations, we describe a 'typical' aviau basilar papilla and on this basis the specializations within individual species.These morphological specializations are discussed in the context of the available physiological data.Bird; Basilar papilla; Morphology; Hair cell; Stereovilli One approach to elucidating basic mechanisms of vertebrate hearing is the comparative investigation of the different types of hearing organs that developed during vertebrate evolution. A knowledge of the morphological substrate is a prerequisite to the ~te~retation of physiolo~c~ results. The number of physiological and anatomical studies of the bird's auditory system has increased greatly over the last 10 years. After early descriptions of the avian inner ear by Retzius (1884) and Held (19X), a detailed comparative investigation of the gross anatomy of different avian cochleae was published by Schwartzkopff and Winter (1960). Studies of fine and ultr~t~ctur~ features and innervation patterns of the basilar papilla of a variety of avian species followed (Takasaka and Smith, 1971;Rosenhall, 1971;Hirokawa, 1978;Tanaka and Smith, 1978; Firbas and Mtiller, 1983;Tilney and Saunders, 1983;Chandler, 1984; &ring et al., 1985;Smith et al., 1985;Counter Correspondence to: Geoffrey A. Manley, Institut ftir Zoologie der Technischen Universit&t Miinchen, Lichtenbergstrasse 4, 8046 Garching, F.R.G. and Tsao, 1986;Tilney et al., 1987). ~thou~ these studies provide a lot of detailed information, most of them are qualitative, making direct comparisons of different species difficult. Starting from this data base, we investigated the auditory epithelia of the starling and the pigeon and quantified a number of gradients over the width and length of the papillae. These results allow objective comparisons of specific morphological features between species, and thus lay the foundation for a structure-function analysis. Material and MethodsThe cochleae of adult starlings (Sturnas u~~g~r~s) and pigeons (C~~~~~~ &via dom.) were the focus of this detailed study. One adult budgerigar (Melopsittucus undulutus) and one adult chicken (Gallus gallus dom.) basilar papilla were also investigated, but not in detail. Starlings, pigeons and one budgerigar were anesthetized by injection of a 6% solution of Na-Pentobarbital into the pectoral muscle (100 mg per kg body weight). The birds were either fixed by transcardial perfusion immediately after sufficient anesthesia (normally within 10 mm; pigeons and budgerigar) or, following a neurophysiological ex-0378-5955/88/~3.50 8 1988 Elsevier Science Publishers B.V. (Biorne~~ Division)

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Section: Resultssupporting

confidence: 59%

Quantitative morphological analysis of the sensory epithelium of the starling and pigeon basilar papilla

Gleich

Manley

1988

Hearing Research

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“…A simple morphological gradient along the basilar membrane would endow the ear with the ability to analyze a wide range of frequencies. Experimentally, it is well established that the height of hair bundles progressively increases along the cochlea, and that concurrently the characteristic frequency of the hair cells declines (19,35). Our proposition that the kinocilium might play an active role in nonmammalian vertebrate hair cells suggests experiments that study the motility of the kinocilium and its potential for generating oscillations.…”

Section: Figmentioning

confidence: 70%

Auditory sensitivity provided by self-tuned critical oscillations of hair cells

Camalet

Duke

Jülicher

et al. 2000

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

373

372

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We introduce the concept of self-tuned criticality as a general mechanism for signal detection in sensory systems. In the case of hearing, we argue that active amplification of faint sounds is provided by a dynamical system that is maintained at the threshold of an oscillatory instability. This concept can account for the exquisite sensitivity of the auditory system and its wide dynamic range as well as its capacity to respond selectively to different frequencies. A specific model of sound detection by the hair cells of the inner ear is discussed. We show that a collection of motor proteins within a hair bundle can generate oscillations at a frequency that depends on the elastic properties of the bundle. Simple variation of bundle geometry gives rise to hair cells with characteristic frequencies that span the range of audibility. Tension-gated transduction channels, which primarily serve to detect the motion of a hair bundle, also tune each cell by admitting ions that regulate the motor protein activity. By controlling the bundle's propensity to oscillate, this feedback automatically maintains the system in the operating regime where it is most sensitive to sinusoidal stimuli. The model explains how hair cells can detect sounds that carry less energy than the background noise. Detecting the sounds of the outside world imposes stringent demands on the design of the inner ear, where the transduction of acoustic stimuli to electrical signals takes place (1). Each of the hair cells within the cochlea, which act as mechanosensors, must be responsive to a particular frequency component of the auditory input. Moreover, these sensors need the utmost sensitivity, because the weakest audible sounds impart an energy, per cycle of oscillation, which is no greater than that of thermal noise (2). At the same time, they must operate over a wide range of volumes, responding and adapting to intensities that vary by many orders of magnitude. Clearly, some form of nonlinear amplification is necessary in sound detection. The familiar resonant gain of a passive elastic system is far from sufficient for the required demands because of the heavy viscous damping at microscopic scales (3). Instead, the cochlea has developed active amplificatory processes, whose precise nature remains to be discovered.There is strong evidence that the cochlea contains forcegenerating dynamical systems that are capable of executing oscillations of a characteristic frequency (4-10). In general, such a system exhibits a Hopf bifurcation (11): as the value of a control parameter is varied, the behavior abruptly changes from a quiescent state to self-sustained oscillations. When the system is in the immediate vicinity of the bifurcation, it can act as a nonlinear amplifier for sinusoidal stimuli close to the characteristic frequency. That such a phenomenon might occur in hearing was first proposed by Gold (3) more than 50 years ago. The idea was recently revived by Choe, Magnasco, and Hudspeth (12) in the context of a specific model of the hair cell. No gene...

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“…Because the specialization of the protein prestin for electromotility is thought to be unique to mammals (Franchini and Elgoyhen, 2006) and has been shown not to occur in at least some reptiles (He et al, 2003), tectorial hair cells probably contribute to the active process through active hair-bundle motility. In the lepidosaurian cochlea, acoustic stimuli produce a pressure difference across the basilar membrane that rocks the basilar papilla back and forth about a hinge along the neural edge of the structure (Frishkopf and DeRosier, 1983;Holton and Hudspeth, 1983;Aranyosi and Freeman, 2005). In the gecko's cochlea, such a motion would be expected to deflect the hair bundles of tectorial hair cells and thus to excite them.…”

Section: Two Classes Of Hair Cellsmentioning

confidence: 99%

The Structural and Functional Differentiation of Hair Cells in a Lizard's Basilar Papilla Suggests an Operational Principle of Amniote Cochleas

Chiappe¹,

Kozlov²,

Hudspeth³

2007

J. Neurosci.

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The hair cells in the mammalian cochlea are of two distinct types. Inner hair cells are responsible for transducing mechanical stimuli into electrical responses, which they forward to the brain through a copious afferent innervation. Outer hair cells, which are thought to mediate the active process that sensitizes and tunes the cochlea, possess a negligible afferent innervation. For every inner hair cell, there are approximately three outer hair cells, so only one-quarter of the hair cells directly deliver information to the CNS. Although this is a surprising feature for a sensory system, the occurrence of a similar innervation pattern in birds and crocodilians suggests that the arrangement has an adaptive value. Using a lizard with highly developed hearing, the tokay gecko, we demonstrate in the present study that the same principle operates in a third major group of terrestrial animals. We propose that the differentiation of hair cells into signaling and amplifying classes reflects incompatible strategies for the optimization of mechanoelectrical transduction and of an active process based on active hair-bundle motility.

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A Micromechanical Contribution to Cochlear Tuning and Tonotopic Organization

Cited by 125 publications

References 21 publications

Quantitative morphological analysis of the sensory epithelium of the starling and pigeon basilar papilla

Quantitative morphological analysis of the sensory epithelium of the starling and pigeon basilar papilla

Auditory sensitivity provided by self-tuned critical oscillations of hair cells

The Structural and Functional Differentiation of Hair Cells in a Lizard's Basilar Papilla Suggests an Operational Principle of Amniote Cochleas

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