Abstract
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.
Highlights
The auditory system exhibits extraordinary sensitivity and temporal resolution
We focus our theoretical and experimental studies on that regime, as it is consistent with the occurrence of spontaneous otoacoustic emissions in vivo, a phenomenon that is ubiquitous across vertebrate species
As chaotic oscillators are a subclass of nonlinear systems that exhibit extreme sensitivity to initial conditions[22], we propose that chaos leads to both high sensitivity and rapid response to mechanical perturbation that characterize hair bundle dynamics
Summary
The auditory system exhibits extraordinary sensitivity and temporal resolution. It is capable of detecting sounds that induce motion in the Å regime, below that of the stochastic noise levels of the surrounding fluid[1]. Dynamics of the auditory response have been modeled using the normal form equation for Hopf bifurcations[15,16] This simple differential equation accounts for many experimentally observed phenomena, including the sensitivity and frequency selectivity of hearing exhibited by many species. A second issue with proximity to criticality is the phenomenon of critical slowing down: near the bifurcation, a system would exhibit a slow response, which seems inconsistent with the high temporal resolution that characterizes hearing This second objection is not resolved by the inclusion of homeostasis or feedback. As chaotic oscillators are a subclass of nonlinear systems that exhibit extreme sensitivity to initial conditions[22], we propose that chaos leads to both high sensitivity and rapid response to mechanical perturbation that characterize hair bundle dynamics
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