Multiple-Timescale Dynamics Underlying Spontaneous Oscillations of Saccular Hair Bundles

Roongthumskul, Yuttana; Fredrickson-Hemsing, Lea; Kao, Albert; Bozovic, Dolores

doi:10.1016/j.bpj.2011.06.027

Cited by 36 publications

(64 citation statements)

References 30 publications

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“…Both electrical and mechanical stimuli could hence trasiently affect the internal calcium levels. Our experimental findings are consistent with the numerical simulations by Roongthumskul et al [9], which propose a calcium-dependent stiffness element.…”

Section: Discussionsupporting

confidence: 82%

Effects of Electrical and Mechanical Overstimulus on Spontaneous Oscillations in Hair Bundles

Kao¹,

Strimbu²,

Bozovic³

et al. 2011

AIP Conference Proceedings

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Abstract. Spontaneous oscillations constitute one of the manifestations of the active process operant in hair cells and provides a sensitive probe for their internal dynamics. The influx of ions into the stereocilia can be modulated by applying an electrical current across the epithelium and has been previously shown to strongly affect the oscillatory profiles. We applied strong transient stimuli and demonstrated that they can induce a transition from the oscillatory to the quiescent state, an effect that can last over several seconds post stimulus cessation. The dynamics of recovery to the oscillatory state was found to be dependent on the amplitude and the duration of the stimulus. Similar dynamics were observed after high-amplitude mechanical stimulus, which mimics the effects of loud sound on an individual bundle.

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Section: Discussionsupporting

confidence: 82%

Effects of Electrical and Mechanical Overstimulus on Spontaneous Oscillations in Hair Bundles

Kao¹,

Strimbu²,

Bozovic³

et al. 2011

AIP Conference Proceedings

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“…Even the simple model presented here exhibits very complex behavior in the region where the head and tail of the fish overlap (SI Appendix). Additional complexities arise from the effects of noise and the interplay between multiple adaptation mechanisms (11,20,27).…”

Section: Discussionmentioning

confidence: 99%

The diverse effects of mechanical loading on active hair bundles

Maoiléidigh

Nicola

Hudspeth

2012

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

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Hair cells in the auditory, vestibular, and lateral-line systems of vertebrates receive inputs through a remarkable variety of accessory structures that impose complex mechanical loads on the mechanoreceptive hair bundles. Although the physiological and morphological properties of the hair bundles in each organ are specialized for detecting the relevant inputs, we propose that the mechanical load on the bundles also adjusts their responsiveness to external signals. We use a parsimonious description of active hair-bundle motility to show how the mechanical environment can regulate a bundle's innate behavior and response to input. We find that an unloaded hair bundle can behave very differently from one subjected to a mechanical load. Depending on how it is loaded, a hair bundle can function as a switch, active oscillator, quiescent resonator, or low-pass filter. Moreover, a bundle displays a sharply tuned, nonlinear, and sensitive response for some loading conditions and an untuned or weakly tuned, linear, and insensitive response under other circumstances. Our simple characterization of active hair-bundle motility explains qualitatively most of the observed features of bundle motion from different organs and organisms. The predictions stemming from this description provide insight into the operation of hair bundles in a variety of contexts.auditory system | hair cell | Hopf bifurcation | transduction | vestibular system A s the mechanosensitive organelle of a hair cell, the hair bundle detects acceleration in the vestibular system, sound in the auditory system, and fluid flow in the lateral-line system. Stimulation of any of these organs results in hair-bundle deflection and the consequent generation of an electrical signal by the hair cell (1). The hair bundle is more than a passive detector, however, for it can mechanically amplify an external input (2). Moreover, an active hair bundle can be tuned to specific frequencies, can oscillate spontaneously, and can exhibit a nonlinear response to external forcing. In contrast, a passive bundle is untuned, quiescent, and linear (2-6).The mechanical load imposed upon a hair bundle, which varies greatly depending on the receptor organ, might be expected to adjust the bundle's performance. In the mammalian cochlea, the hair bundles of outer hair cells are sensitive to the displacement of the overlying tectorial membrane to which they are attached. In contrast, the hair bundles of inner hair cells in the same organ are free of accessory structures but are deflected by fluid flow. Linear acceleration is detected in the utricle and saccule by hair bundles loaded with calcareous aggregates, the otoconia, embedded in an otolithic membrane. These hair bundles are deflected by the inertial force owing to the mass of the otoconia. The semicircular canals, the sensory organs for angular acceleration, contain groups of hair bundles encased in a gelatinous cupula. Head rotation induces within the canals a fluid flow that the bundles detect. The organization of hair bundles in late...

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“…To minimize its effects on the dynamical response of the bundle to sinusoidal stimulation, the homeostatic mechanism operates slowly. Because experimental manipulations have been shown to affect adaptation, homeostatic feedback is applied to the models' adaptation mechanisms, although other choices are possible (31)(32)(33). Additional motivation for the homeostatic mechanisms is provided in Discussion.…”

Section: Resultsmentioning

confidence: 99%

“…Multiple timescales have been seen in the dynamics of hair bundle motion (31,48). However, delays in a bundle's return to spontaneous oscillations were reported to depend on the duration rather than on the magnitude of the force steps, possibly because large force steps were used (48).…”

Section: Discussionmentioning

confidence: 99%

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Homeostatic enhancement of sensory transduction

Milewski

Maoiléidigh

Salvi

et al. 2017

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

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Our sense of hearing boasts exquisite sensitivity, precise frequency discrimination, and a broad dynamic range. Experiments and modeling imply, however, that the auditory system achieves this performance for only a narrow range of parameter values. Small changes in these values could compromise hair cells' ability to detect stimuli. We propose that, rather than exerting tight control over parameters, the auditory system uses a homeostatic mechanism that increases the robustness of its operation to variation in parameter values. To slowly adjust the response to sinusoidal stimulation, the homeostatic mechanism feeds back a rectified version of the hair bundle's displacement to its adaptation process. When homeostasis is enforced, the range of parameter values for which the sensitivity, tuning sharpness, and dynamic range exceed specified thresholds can increase by more than an order of magnitude. Signatures in the hair cell's behavior provide a means to determine through experiment whether such a mechanism operates in the auditory system. Robustness of function through homeostasis may be ensured in any system through mechanisms similar to those that we describe here.hair cell | hearing | nonlinear dynamics | oscillation | robustness B iological systems are subject to developmental variation and environmental fluctuations. Homeostatic mechanisms nonetheless ensure that most individuals function well under a variety of conditions. For example, homeotherms maintain an internal body temperature within a few degrees of a set point thanks to mechanisms such as sweating, panting, shivering, and redirecting blood flow. Many organisms regulate blood pressure by changing blood-vessel diameter or by adjusting heart rate or stroke volume. How homeostasis occurs remains an open question in many contexts, particularly when the system in question operates near a transition between two distinct behaviors, as has been suggested in gene expression, neuronal networks, and flocking (1-4). Here, we seek the general principles underlying homeostatic mechanisms by studying a specific system whose high level of performance derives from operating near a dynamical transition. We propose a strategy that increases the robustness of sensory transduction to parameter variation.Within the range of human hearing, a trained ear can distinguish tones that differ in frequency by only 0.1% (5). The softest sounds that we can detect carry energies of the same magnitude as thermal fluctuations (6-9). We can, however, process sounds that convey a trillionfold more power (10). To achieve these specifications, the auditory system uses a set of active elements poised on the brink of self-oscillation (11). The presence of these self-oscillatory elements is evidenced by measurable sounds, termed spontaneous otoacoustic emissions, generated by our ears (8). It is unclear, however, how the auditory system maintains proximity to the boundary of spontaneous oscillation.Within the cochlea, hair cells transduce sound-induced vibrations into electrical signals, w...

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Multiple-Timescale Dynamics Underlying Spontaneous Oscillations of Saccular Hair Bundles

Cited by 36 publications

References 30 publications

Effects of Electrical and Mechanical Overstimulus on Spontaneous Oscillations in Hair Bundles

Effects of Electrical and Mechanical Overstimulus on Spontaneous Oscillations in Hair Bundles

The diverse effects of mechanical loading on active hair bundles

Homeostatic enhancement of sensory transduction

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