Physical basis of two-tone interference in hearing

Jülicher, Frank; Andor, Daniel; Duke, Thomas

doi:10.1073/pnas.151257898

Cited by 81 publications

(74 citation statements)

References 27 publications

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“…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.…”

Section: Discussionmentioning

confidence: 99%

Power gain exhibited by motile mechanosensory neurons in Drosophila ears

Göpfert

Humphris²,

Albert³

et al. 2004

Proc. Natl. Acad. Sci. U.S.A.

120

137

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In insects and vertebrates alike, hearing is assisted by the motility of mechanosensory cells. Much like pushing a swing augments its swing, this cellular motility is thought to actively augment vibrations inside the ear, thus amplifying the ear's mechanical input. Power gain is the hallmark of such active amplification, yet whether and how much energy motile mechanosensory cells contribute within intact auditory systems has remained uncertain. Here, we assess the mechanical energy provided by motile mechanosensory neurons in the antennal hearing organs of Drosophila melanogaster by analyzing the fluctuations of the sound receiver to which these neurons connect. By using dead WT flies and live mutants (tilB 2 , btv 5P1 , and nompA 2 ) with defective neurons as a background, we show that the intact, motile neurons do exhibit power gain. In WT flies, the neurons lift the receiver's mean total energy by 19 zJ, which corresponds to 4.6 times the energy of the receiver's Brownian motion. Larger energy contributions (200 zJ) associate with self-sustained oscillations, suggesting that the neurons adjust their energy expenditure to optimize the receiver's sensitivity to sound. We conclude that motile mechanosensory cells provide active amplification; in Drosophila, mechanical energy contributed by these cells boosts the vibrations that enter the ear.cochlear amplifier ͉ hearing ͉ auditory mechanics ͉ cell mobility ͉ hair cell T he cochlear amplifier is the dominant unifying concept in cochlear mechanics (1). The concept assumes that the cochlea is endowed with a biological energy source that amplifies the ear's input by pumping mechanical energy into the vibrations inside the ear (1-6). The validity of the concept is supported by the mechanics of the cochlea and its mechanosensory cells. Hair cells, the cochlear mechanosensory cells, provide a source of mechanical energy. In addition to transducing mechanical vibrations into electrical responses, some hair cells are equipped with molecular motors that convert metabolic or electrical energy into mechanical energy, resulting in active movements of the cells (1, 3-7). These cellular movements, in turn, exert positive feedback on the cochlear mechanics. By nonlinearly undamping the cochlear resonances as the stimulus intensity declines, this feedback selectively improves the ear's sensitivity to small vibrations induced by faint sound (1, 3-6). Notably, this hair cell-based feedback occasionally becomes unstable, leading to self-sustained feedback oscillations within the cochlear duct. Such self-sustained feedback oscillations may account for the ear's ability to generate spontaneous otoacoustic emissions, i.e., to spontaneously emit sound (8, 9).Collectively, the hair cells' motility, the cochlea's nonlinearity, and the ear's spontaneous otoacoustic emissions document the presence of hair cell-based mechanical feedback inside the cochlear duct. Yet, whether this feedback brings about power gain by expending biological energy, as assumed by the concept of the cochlear ampli...

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Section: Discussionmentioning

confidence: 99%

Power gain exhibited by motile mechanosensory neurons in Drosophila ears

Göpfert

Humphris²,

Albert³

et al. 2004

Proc. Natl. Acad. Sci. U.S.A.

120

137

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“…The six features that characterize the ear's active process are signatures of any dynamical system operating near a Hopf bifurcation (17,18,38). That active hair-bundle motility displays those properties therefore does not preclude the possibility that the ear contains oscillators in addition to hair bundles.…”

Section: Scaling Of Responses With Stimulationmentioning

confidence: 99%

Compressive nonlinearity in the hair bundle's active response to mechanical stimulation

Martin

Hudspeth

2001

Proc. Natl. Acad. Sci. U.S.A.

178

133

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The auditory system's ability to interpret sounds over a wide range of amplitudes rests on the nonlinear responsiveness of the ear. Whether measured by basilar-membrane vibration, nerve-fiber activity, or perceived loudness, the ear is most sensitive to small signals and grows progressively less responsive as stimulation becomes stronger. Seeking a correlate of this behavior at the level of mechanoelectrical transduction, we examined the responses of hair bundles to direct mechanical stimulation. As reported by the motion of an attached glass fiber, an active hair bundle from the bullfrog's sacculus oscillates spontaneously. Sinusoidal movement of the fiber's base by as little as ؎1 nm, corresponding to the application at the bundle's top of a force of ؎0.3 pN, causes detectable phase-locking of the bundle's oscillations to the stimulus. Although entrainment increases as the stimulus grows, the amplitude of the hair-bundle movement does not rise until phaselocking is nearly complete. A bundle is most sensitive to stimulation at its frequency of spontaneous oscillation. Far from that frequency, the sensitivity of an active hair bundle resembles that of a passive bundle. Over most of its range, an active hair bundle's response grows as the one-third power of the stimulus amplitude; the bundle's sensitivity declines accordingly in proportion to the negative two-thirds power of the excitation. This scaling behavior, also found in the response of the mammalian basilar membrane to sound, signals the operation of an amplificatory process at the brink of an oscillatory instability, a Hopf bifurcation.H earing operates over a remarkably broad dynamic range.The faintest sounds we can sense impart to the ear an amount of energy per cycle of oscillation comparable to thermal energy (1). At the other extreme, the ear endures urban, industrial, and military noise that represents sound pressures 6 orders of magnitude greater than threshold! To accommodate such diverse stimuli, the ear's responsiveness must be nonlinear. The common use of decibels, a logarithmic metric, for the intensity of sound reflects this fact. Nonlinear compression of responsiveness is evident throughout the ear's transduction process. The perceived loudness, the firing rate of auditory-nerve axons, and the basilar-membrane vibration in the cochlea all grow more gradually than the input signal. In the chinchilla's cochlea, for example, sound-pressure levels ranging over 120 dB are represented as basilar-membrane vibrations spanning but 2 orders of magnitude (ref. 2; reviewed in ref.3). The basilar membrane's responsiveness, defined as the increase in amplitude of vibration evoked by an increment in soundpressure level, is greatest for threshold stimuli and then declines progressively at moderate to intense levels.The nonlinearity of aural responsiveness is associated closely with the ear's great sensitivity, sharp frequency selectivity, and ability to generate otoacoustic emissions. These four characteristics of hearing result from an active process that ...

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“…It is a key feature of active hearing organs that the nonlinearities of the system together with an inherent reciprocity of force transmission must lead to the generation of distortion products [5]. In the case of the mosquito ear this means that, even when stimulated with only two tones f 1 and f 2 (representing, for example, male and female flight tones), the antennal displacement response will display peaks at a set of mathematically predicted additional frequencies, i.e., distortion products.…”

Section: Current Biologymentioning

confidence: 99%

“…No engineered system has yet been designed that could understand distorted speech in a noisy and reverberating environment with multiple speakers. That our auditory system achieves this feat is testament to its remarkable performance.On the other hand, an engineer could argue that the auditory system's performance is objectively poor, even in animals with sensitive hearing: at the very first step, during the mechanoelectrical transduction in the inner ear, external sounds are distorted, or even completely suppressed, while new tones are generated by the ear itself [5]. Forward and backward masking, illusory percepts of nonexistent tones (such as the Zwicker illusion [6]), perceptual merging of separate auditory streams, the precedence effect suppressing the perception of echoes that has been demonstrated in insects and vertebrates [7,8] (and which some blind people can unsuppress), auditory hallucinations, and a frustrating inability to distinguish between distinct phonemes of a foreign language -all of these phenomena indicate that evolution has not shaped the auditory system as an objective detector of acoustical reality.…”

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confidence: 99%

Comparative Aspects of Hearing in Vertebrates and Insects with Antennal Ears

Albert¹,

Kozlov

2016

Current Biology

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The evolution of hearing in terrestrial animals has resulted in remarkable adaptations enabling exquisitely sensitive sound detection by the ear and sophisticated sound analysis by the brain. In this review, we examine several such characteristics, using examples from insects and vertebrates. We focus on two strong and interdependent forces that have been shaping the auditory systems across taxa: the physical environment of auditory transducers on the small, subcellular scale, and the sensory-ecological environment within which hearing happens, on a larger, evolutionary scale. We briefly discuss acoustical feature selectivity and invariance in the central auditory system, highlighting a major difference between insects and vertebrates as well as a major similarity. Through such comparisons within a sensory ecological framework, we aim to emphasize general principles underlying acute sensitivity to airborne sounds.Introduction Auditory physiology offers a distinctive perspective on the interaction between a sensory system and its environment. On the one hand, auditory systems in vertebrates and insects with sensitive hearing are capable of remarkable performances on multiple levels, both within the sensory periphery where the minute energies associated with sound are converted into electrical signals, as well as within higher-order brain areas where complex natural stimuli such as human speech are processed. For example, displacements caused by acoustical stimuli in the inner ear at the threshold of hearing are sub-nanometer and comparable to the distance between atoms in molecules [1]. Furthermore, thermal fluctuations in the ear's mechanotransduction apparatus not only are significant, but also can be larger than the faintest audible signals, making signal detection a challenging task [2]. Ascending the sensory hierarchy, one encounters other marvels of evolution, such as the ability of individual neurons to encode -using millisecond-long action potentials -inter-aural time differences of only about ten microseconds, and to use this information to localize the source of the sound [3,4]. No engineered system has yet been designed that could understand distorted speech in a noisy and reverberating environment with multiple speakers. That our auditory system achieves this feat is testament to its remarkable performance.On the other hand, an engineer could argue that the auditory system's performance is objectively poor, even in animals with sensitive hearing: at the very first step, during the mechanoelectrical transduction in the inner ear, external sounds are distorted, or even completely suppressed, while new tones are generated by the ear itself [5]. Forward and backward masking, illusory percepts of nonexistent tones (such as the Zwicker illusion [6]), perceptual merging of separate auditory streams, the precedence effect suppressing the perception of echoes that has been demonstrated in insects and vertebrates [7,8] (and which some blind people can unsuppress), auditory hallucinations, and a frustrating inab...

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Physical basis of two-tone interference in hearing

Cited by 81 publications

References 27 publications

Power gain exhibited by motile mechanosensory neurons in Drosophila ears

Power gain exhibited by motile mechanosensory neurons in Drosophila ears

Compressive nonlinearity in the hair bundle's active response to mechanical stimulation

Comparative Aspects of Hearing in Vertebrates and Insects with Antennal Ears

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