Auditory sensitivity provided by self-tuned critical oscillations of hair cells

Abstract

We introduce the concept of self-tuned criticality as a general mechanism for signal detection in sensory systems. In the case of hearing, we argue that active amplification of faint sounds is provided by a dynamical system that is maintained at the threshold of an oscillatory instability. This concept can account for the exquisite sensitivity of the auditory system and its wide dynamic range as well as its capacity to respond selectively to different frequencies. A specific model of sound detection by the hair cells of the inner ear is discussed. We show that a collection of motor proteins within a hair bundle can generate oscillations at a frequency that depends on the elastic properties of the bundle. Simple variation of bundle geometry gives rise to hair cells with characteristic frequencies that span the range of audibility. Tension-gated transduction channels, which primarily serve to detect the motion of a hair bundle, also tune each cell by admitting ions that regulate the motor protein activity. By controlling the bundle's propensity to oscillate, this feedback automatically maintains the system in the operating regime where it is most sensitive to sinusoidal stimuli. The model explains how hair cells can detect sounds that carry less energy than the background noise. Detecting the sounds of the outside world imposes stringent demands on the design of the inner ear, where the transduction of acoustic stimuli to electrical signals takes place (1). Each of the hair cells within the cochlea, which act as mechanosensors, must be responsive to a particular frequency component of the auditory input. Moreover, these sensors need the utmost sensitivity, because the weakest audible sounds impart an energy, per cycle of oscillation, which is no greater than that of thermal noise (2). At the same time, they must operate over a wide range of volumes, responding and adapting to intensities that vary by many orders of magnitude. Clearly, some form of nonlinear amplification is necessary in sound detection. The familiar resonant gain of a passive elastic system is far from sufficient for the required demands because of the heavy viscous damping at microscopic scales (3). Instead, the cochlea has developed active amplificatory processes, whose precise nature remains to be discovered.There is strong evidence that the cochlea contains forcegenerating dynamical systems that are capable of executing oscillations of a characteristic frequency (4-10). In general, such a system exhibits a Hopf bifurcation (11): as the value of a control parameter is varied, the behavior abruptly changes from a quiescent state to self-sustained oscillations. When the system is in the immediate vicinity of the bifurcation, it can act as a nonlinear amplifier for sinusoidal stimuli close to the characteristic frequency. That such a phenomenon might occur in hearing was first proposed by Gold (3) more than 50 years ago. The idea was recently revived by Choe, Magnasco, and Hudspeth (12) in the context of a specific model of the hair cell. No gene...

Actin cytoskeleton of chemotactic amoebae operates close to the onset of oscillations

“…Many biological systems have been demonstrated to operate at the border of an instability (36). For example, there is evidence that the exceptional auditory sensitivity of the cochlea relies on a forcegenerating dynamical system, which is maintained at the threshold of a Hopf bifurcation (37). Under such conditions, the system can act as a precisely tuned nonlinear amplifier for stimuli close to its intrinsic frequency.…”

Power gain exhibited by motile mechanosensory neurons in Drosophila ears

“…It suggests that the fly is controlling the amplificatory gain by adjusting the neural energy contribution. If this energy adjustment serves to stabilize the system at the verge of an oscillatory instability, it will maximize the ear's sensitivity to external disturbances imposed by sound (26,27). Evidence suggests that vertebrate hair cells and also the cochlear mechanics operate near such a critical point, a Hopf bifurcation (13,(26)(27)(28)(29), and the fly's auditory neurons and mechanics may do so as well.…”

“…Evidence suggests that vertebrate hair cells and also the cochlear mechanics operate near such a critical point, a Hopf bifurcation (13,(26)(27)(28)(29), and the fly's auditory neurons and mechanics may do so as well. By linking nonlinearities, noisy twitches, self-sustained oscillations, and undamping in a mechanistic way (26)(27)(28), such critical adjustment of amplification and the underlying concept of self-tuned criticality (27) might explain the vast biophysical parallels between the ears of vertebrates and flies, which, along with multiple molecular parallels (e.g., refs. 19 and 30-33), recommend Drosophila for the study of hearing.…”

Coding of Sounds in the Auditory System and Its Relevance to Signal Processing and Coding in Cochlear Implants

“…The exact way in which the active mechanism works is complex and is still not fully understood. For recent reviews, the reader is referred to (6)(7)(8)(9).…”