Vestibular Drop Attacks and Meniere's Disease as Results of Otolithic Membrane Damage-A Numerical Model.

Meniere's disease (MD) is a condition of the inner ear with symptoms affecting both vestibular and hearing functions. Some patients with MD experience vestibular drop attacks (VDAs), which are violent falls caused by spurious vestibular signals from the utricle and/or saccule. Recent surgical work has shown that patients who experience VDAs also show disrupted utricular otolithic membranes. The objective of this study is to determine if otolithic membrane damage alone is sufficient to induce spurious vestibular signals, thus potentially eliciting VDAs and the vestibular dysfunction seen in patients with MD. We use a previously developed numerical model to describe the nonlinear dynamics of an array of active, elastically coupled hair cells. We then reduce the coupling strength of a selected region of the membrane to model the effects of tissue damage. As we reduce the coupling strength, we observe large and abrupt spikes in hair bundle position. As bundle displacements from the equilibrium position have been shown to lead to depolarization of the hair-cell soma and hence trigger neural activity, this spontaneous activity could elicit false detection of a vestibular signal. The results of this numerical model suggest that otolithic membrane damage alone may be sufficient to induce VDAs and the vestibular dysfunction seen in patients with MD. Future experimental work is needed to confirm these results in vitro.

Chimera states and frequency clustering in systems of coupled inner-ear hair cells.

Coupled hair cells of the auditory and vestibular systems perform the crucial task of converting the energy of sound waves and ground-borne vibrations into ionic currents. We mechanically couple groups of living, active hair cells with artificial membranes, thus mimicking in vitro the coupled dynamical system. We identify chimera states and frequency clustering in the dynamics of these coupled nonlinear, autonomous oscillators. We find that these dynamical states can be reproduced by our numerical model with heterogeneity of the parameters. Furthermore, we find that this model is most sensitive to external signals when poised at the onset of synchronization, where chimera and cluster states are likely to form. We, therefore, propose that the partial synchronization in our experimental system is a manifestation of a system poised at the verge of synchronization with optimal sensitivity.

Dynamics of Mechanically Coupled Hair-Cell Bundles of the Inner Ear.

The high sensitivity and effective frequency discrimination of sound detection performed by the auditory system rely on the dynamics of a system of hair cells. In the inner ear, these acoustic receptors are primarily attached to an overlying structure that provides mechanical coupling between the hair bundles. Although the dynamics of individual hair bundles has been extensively investigated, the influence of mechanical coupling on the motility of the system of bundles remains underdetermined. We developed a technique of mechanically coupling two active hair bundles, enabling us to probe the dynamics of the coupled system experimentally. We demonstrated that the coupling could enhance the coherence of hair bundles' spontaneous oscillation, as well as their phase-locked response to sinusoidal stimuli, at the calcium concentration in the surrounding fluid near the physiological level. The empirical data were consistent with numerical results from a model of two coupled nonisochronous oscillators, each displaying a supercritical Hopf bifurcation. The model revealed that a weak coupling can poise the system of unstable oscillators closer to the bifurcation by a shift in the critical point. In addition, the dynamics of strongly coupled oscillators far from criticality suggested that individual hair bundles may be regarded as nonisochronous oscillators. An optimal degree of nonisochronicity was required for the observed tuning behavior in the coherence of autonomous motion of the coupled system.

Chaotic Dynamics Enhance the Sensitivity of Inner Ear Hair Cells.

Hair cells of the auditory and vestibular systems are capable of detecting sounds that induce sub-nanometer vibrations of the hair bundle, below the stochastic noise levels of the surrounding fluid. Furthermore, the auditory system exhibits a highly rapid response time, in the sub-millisecond regime. We propose that chaotic dynamics enhance the sensitivity and temporal resolution of the hair bundle response, and we provide experimental and theoretical evidence for this effect. We use the Kolmogorov entropy to measure the degree of chaos in the system and the transfer entropy to quantify the amount of stimulus information captured by the detector. By varying the viscosity and ionic composition of the surrounding fluid, we are able to experimentally modulate the degree of chaos observed in the hair bundle dynamics in vitro. We consistently find that the hair bundle is most sensitive to a stimulus of small amplitude when it is poised in the weakly chaotic regime. Further, we show that the response time to a force step decreases with increasing levels of chaos. These results agree well with our numerical simulations of a chaotic Hopf oscillator and suggest that chaos may be responsible for the high sensitivity and rapid temporal response of hair cells.

Noise-induced chaos and signal detection by the nonisochronous Hopf oscillator.

The Hopf oscillator has been shown to capture many phenomena of the auditory and vestibular systems. These systems exhibit remarkable temporal resolution and sensitivity to weak signals, as they are able to detect sounds that induce motion in the angstrom regime. In the present work, we find the analytic response function of a nonisochronous Hopf oscillator to a step stimulus and show that the system is most sensitive in the regime where noise induces chaotic dynamics. We show that this regime also provides a faster response and enhanced temporal resolution. Thus, the system can detect a very brief, low-amplitude pulse. Finally, we subject the oscillator to periodic delta-function forcing, mimicking a spike train, and find the exact analytic expressions for the stroboscopic maps. Using these maps, we find a period-doubling cascade to chaos with increasing force strength.

Chaotic Dynamics of Inner Ear Hair Cells.

Experimental records of active bundle motility are used to demonstrate the presence of a low-dimensional chaotic attractor in hair cell dynamics. Dimensionality tests from dynamic systems theory are applied to estimate the number of independent variables sufficient for modelling the hair cell response. Poincaré maps are constructed to observe a quasiperiodic transition from chaos to order with increasing amplitudes of mechanical forcing. The onset of this transition is accompanied by a reduction of Kolmogorov entropy in the system and an increase in transfer entropy between the stimulus and the hair bundle, indicative of signal detection. A simple theoretical model is used to describe the observed chaotic dynamics. The model exhibits an enhancement of sensitivity to weak stimuli when the system is poised in the chaotic regime. We propose that chaos may play a role in the hair cell's ability to detect low-amplitude sounds.