Dynamics of Freely Oscillating and Coupled Hair Cell Bundles under Mechanical Deflection

Fredrickson-Hemsing, Lea; Strimbu, C. Elliott; Roongthumskul, Yuttana; Bozovic, Dolores

doi:10.1016/j.bpj.2012.03.017

Cited by 25 publications

(25 citation statements)

References 35 publications

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“…4C-E). In agreement with published observations (26,27), entrainment was frequency-dependent for a range of stimulus forces. A map of vector strength computed across a range of stimulus forces and frequencies disclosed a phase-locked region that depended on load stiffness.…”

Section: Response To Sinusoidal Stimulationsupporting

confidence: 92%

Control of a hair bundle’s mechanosensory function by its mechanical load

Salvi

Maoiléidigh

Fabella

et al. 2015

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

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Hair cells, the sensory receptors of the internal ear, subserve different functions in various receptor organs: they detect oscillatory stimuli in the auditory system, but transduce constant and step stimuli in the vestibular and lateral-line systems. We show that a hair cell's function can be controlled experimentally by adjusting its mechanical load. By making bundles from a single organ operate as any of four distinct types of signal detector, we demonstrate that altering only a few key parameters can fundamentally change a sensory cell's role. The motions of a single hair bundle can resemble those of a bundle from the amphibian vestibular system, the reptilian auditory system, or the mammalian auditory system, demonstrating an essential similarity of bundles across species and receptor organs.auditory system | dynamical system | hair cell | Hopf bifurcation | vestibular system T he hair bundles of vertebrates are mechanosensory organelles responsible for detecting sounds in the auditory system, linear and angular accelerations in the vestibular system, and water movements and pressure gradients in the lateral-line system of fishes and amphibians (1, 2). In each instance an appropriate stimulus deflects the bundles, depolarizing the hair cells from which they emerge (3). Hair bundles are not simply passive detectors, however, for they actively amplify their responses to mechanical stimulation (4, 5). Hair-bundle motility contributes to an active process that endows the auditory system with the ability to detect stimuli with energies near that of thermal fluctuations (6), to distinguish tones that differ by less than 0.2% in frequency (7), and to accommodate inputs varying over a millionfold range in amplitude (4,(8)(9)(10)(11).Auditory, vestibular, and lateral-line organs respond to distinct patterns of mechanical input. The mechanical properties and environments of hair bundles differ correspondingly between different organisms, among receptor organs, and with the tonotopic position along individual auditory organs (12-15). A mathematical model predicts that the response of a hair bundle is regulated both by its intrinsic mechanical characteristics and by its mechanical load (16). Motivated by this proposition, we investigated how the load stiffness and constant force imposed on a bundle control its dynamics and response to external perturbations. ResultsMapping the Hair Bundle's Experimental State Diagram. The hair bundle's state diagram characterizes its behavior for different combinations of two control parameters: load stiffness, or force per unit displacement, and constant force. These control parameters describe the mechanical load imposed on a hair bundle within a sensory organ. A theoretical model of hair-bundle dynamics predicts the qualitative structure of the state diagram ( Fig. 1 A-C). To test this prediction experimentally, we varied the mechanical load imposed on an individual hair bundle and monitored its displacement. The load was delivered to an individual hair bundle by attaching the tip o...

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Section: Response To Sinusoidal Stimulationsupporting

confidence: 92%

Control of a hair bundle’s mechanosensory function by its mechanical load

Salvi

Maoiléidigh

Fabella

et al. 2015

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

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“…Owing to the effects of adaptation, offsets in the positive direction typically do not fully suppress active motility unless very large deflections are imposed [20]. Before full suppression is reached, a number of hair bundles display a transition from spontaneous limit cycle oscillation to spiking, in which they undergo rapid excursions in the negative direction.…”

Section: Resultsmentioning

confidence: 99%

Phase-locked spiking of inner ear hair cells and the driven noisy Adler equation

Shlomovitz

Roongthumskul

et al. 2014

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The inner ear constitutes a remarkably sensitive mechanical detector. This detection occurs in a noisy and highly viscous environment, as the sensory cells—the hair cells—are immersed in a fluid-filled compartment and operate at room or higher temperatures. We model the active motility of hair cell bundles of the vestibular system with the Adler equation, which describes the phase degree of freedom of bundle motion. We explore both analytically and numerically the response of the system to external signals, in the presence of white noise. The theoretical model predicts that hair bundles poised in the quiescent regime can exhibit sporadic spikes—sudden excursions in the position of the bundle. In this spiking regime, the system exhibits stochastic resonance, with the spiking rate peaking at an optimal level of noise. Upon the application of a very weak signal, the spikes occur at a preferential phase of the stimulus cycle. We compare the theoretical predictions of our model to experimental measurements obtained in vitro from individual hair cells. Finally, we show that an array of uncoupled hair cells could provide a sensitive detector that encodes the frequency of the applied signal.

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“…For example, under some conditions hair bundles leap from quiescence to largeamplitude oscillations, the hallmark of a subcritical Hopf bifurcation 150,200 . Still more complex patterns, such as runs of oscillation punctuated by periods of inactivity, reflect bifurcations of a higher order 164 .…”

Section: Impact Of the Hopf Bifurcation On Hearingmentioning

confidence: 99%

Integrating the active process of hair cells with cochlear function

2014

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Uniquely among human senses, hearing is not simply a passive response to stimulation. Our auditory system is instead enhanced by an active process in cochlear hair cells that amplifies acoustic signals several hundred-fold, sharpens frequency selectivity and broadens the ear's dynamic range. Active motility of the mechanoreceptive hair bundles underlies the active process in amphibians and some reptiles; in mammals, this mechanism operates in conjunction with prestin-based somatic motility. Both individual hair bundles and the cochlea as a whole operate near a dynamical instability, the Hopf bifurcation, which accounts for the cardinal features of the active process.

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Dynamics of Freely Oscillating and Coupled Hair Cell Bundles under Mechanical Deflection

Cited by 25 publications

References 35 publications

Control of a hair bundle’s mechanosensory function by its mechanical load

Control of a hair bundle’s mechanosensory function by its mechanical load

Phase-locked spiking of inner ear hair cells and the driven noisy Adler equation

Integrating the active process of hair cells with cochlear function

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