Auditory Sensitivity Provided by Self-tuned Critical Oscillations of Hair Cells
arXiv:physics/0003100 · doi:10.1073/pnas.97.7.3183
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 which 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 which depends on the elastic properties of the bundle. Simple variation of bundle geometry gives rise to hair cells with characteristic frequencies which 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 which 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 which carry less energy than the background noise.
11 pages, 6 figures, REVTEX
References in corpus (1)
Cited by in corpus (65)
- Optimal Dynamical Range of Excitable Networks at Criticality
- Are biological systems poised at criticality?
- Colloquium: Criticality and dynamical scaling in living systems
- Criticality in the brain: A synthesis of neurobiology, models and cognition
- Molecular motors robustly drive active gels to a critically connected state
- Physical Aspects of Axonemal Beating and Swimming
- The physics of hearing: fluid mechanics and the active process of the inner ear
- Dynamical and Statistical Criticality in a Model of Neural Tissue
- The Active Traveling Wave in the Cochlea
- Self-assembly of Active Colloidal Molecules with Dynamic Function
- Cellular organization by self-organization : mechanisms and models for Min protein dynamics
- From Physics to Biology by Extending Criticality and Symmetry Breakings
- The Cochlear Tuning Curve
- Fluctuation theorem and large deviation function for a solvable model of a molecular motor
- Two adaptation processes in auditory hair cells together can provide an active amplifier
- Control of a hair bundle's mechanosensory function by its mechanical load
- Perspectives on theory at the interface of physics and biology
- Universal Critical Behavior of Noisy Coupled Oscillators
- Dynamic Adaptive Computation: Tuning network states to task requirements
- Coexistence of critical sensitivity and subcritical specificity can yield optimal population coding
- Identification of Bifurcations from Observations of Noisy Biological Oscillators
- Bottom-up approach to torus bifurcation in neuron models
- Universal critical behavior of noisy coupled oscillators: A renormalization group study
- Signal integration enhances the dynamic range in neuronal systems
- Waves on Reissner's membrane: a mechanism for the propagation of otoacoustic emissions from the cochlea
- Oscillations in molecular motor assemblies
- Auditory power-law activation-avalanches exhibit a fundamental computational ground-state
- Dynamical phase transitions in the nonreciprocal Ising model
- A bifurcation integrates information from many noisy ion channels
- Mimicking the active cochlea with a fluid-coupled array of subwavelength Hopf resonators
- Cochlear-bone wave can yield a hearing sensation as well as otoacoustic emission
- Human pitch is pre-cortical: The essential role of the cochlear fluid
- Scaling law for the transient behavior of type-II neuron models
- Unidirectional mechanical amplification as a design principle for an active microphone
- Non-equilibrium systems have steady-state distributions and non-steady dynamics
- Nonequilibrium limit cycle oscillators: fluctuations in hair bundle dynamics
- Amplification in the auditory periphery: the effect of coupling tuning mechanisms
- Critical Waves and the Length Problem of Biology
- Sinusoidal-signal detection by active, noisy oscillators on the brink of self-oscillation
- Chimera states and frequency clustering in systems of coupled inner-ear hair cells
- Collective Effects in Models for Interacting Molecular Motors and Motor-Microtubule Mixtures
- Self-tuning to the Hopf bifurcation in fluctuating systems
- Learning with a network of competing synapses
- Violation of generalized fluctuation theorems in adaptively driven steady states: Applications to hair cell oscillations
- Noise-induced distortion of nonequilibrium oscillator mean limit cycle
- Self-tuning of threshold for a two-state system
- Coalescence of limit cycles in the presence of noise
- Frequency locking in auditory hair cells: Distinguishing between additive and parametric forcing
- Hair cells in the cochlea must tune resonant modes to the edge of instability without destabilizing collective modes
- Automated tuning of bifurcations via feedback
- Modeling cochlear two-tone suppression using a system of nonlinear oscillators with feed-forward coupling
- Molding the asymmetry of localized frequency-locking waves by a generalized forcing and implications to the inner ear
- Adaptive Scales of Spatial Integration and Response Latencies in a Critically-Balanced Model of the Primary Visual Cortex
- Self Tuned Criticality: Controlling a neuron near its bifurcation point via temporal correlations
- Multifrequency Forcing of a Hopf Oscillator Model of the Inner Ear
- Lattice ultrasensitivity amplifies signals in E. coli without fine-tuning
- Critical Dynamics and Cyclic Memory Retrieval in Non-reciprocal Hopfield Networks
- Treatise on Hearing: The Temporal Auditory Imaging Theory Inspired by Optics and Communication
- A simple mechanism for balancing at the border of instability with applications to persistent neural activity
- Active energy harvesting and work transduction by hair-cell bundles in bullfrog's inner ear
- Adaptation and Parameter Estimation in Systems with Unstable Target Dynamics and Nonlinear Parametrization
- Enhanced signal-to-noise ratios in frog hearing can be achieved through amplitude death
- Joint Spatio-Temporal Discretisation of Nonlinear Active Cochlear Models
- Driven response of time delay coupled limit cycle oscillators
- On Optimality in Auditory Information Processing