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The auditory and vestibular systems exhibit remarkable sensitivity of detection, responding to deflections on the order of angstroms, even in the presence of biological noise. The auditory system exhibits high temporal acuity and frequency selectivity, allowing us to make sense of the acoustic world around us. As the acoustic signals of interest span many orders of magnitude in both amplitude and frequency, this system relies heavily on nonlinearities and power-law scaling. The vestibular system, which detects ground-borne vibrations and creates the sense of balance, exhibits highly sensitive, broadband detection. It likewise requires high temporal acuity so as to allow us to maintain balance while in motion. The behavior of these sensory systems has been extensively studied in the context of dynamical systems theory, with many empirical phenomena described by critical dynamics. Other phenomena have been explained by systems in the chaotic regime, where weak perturbations drastically impact the future state of the system. Using a Hopf oscillator as a simple numerical model for a sensory element in these systems, we explore the intersection of the two types of dynamical phenomena. We identify the relative tradeoffs between different detection metrics, and propose that, for both types of sensory systems, the instabilities giving rise to chaotic dynamics improve signal detection.

The remarkable signal-detection capabilities of the auditory and vestibular systems have been studied for decades. Much of the conceptual framework that arose from this research has suggested that these sensory systems rest on the verge of instability, near a Hopf bifurcation, in order to explain the detection specifications. However, this paradigm contains several unresolved issues. Critical systems are not robust to stochastic fluctuations or imprecise tuning of the system parameters. Further, a system poised at criticality exhibits a phenomenon known in dynamical systems theory ascritical slowing down, where the response time diverges as the system approaches the critical point. An alternative description of these sensory systems is based on the notion of chaotic dynamics, where the instabilities inherent to the dynamics produce high temporal acuity and sensitivity to weak signals, even in the presence of noise. This alternative description resolves the issues that arise in the criticality picture. We review the conceptual framework and experimental evidence that supports the use of chaos for signal detection by these systems, and propose future validation experiments.

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 dynamicsin 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.