Putting ion channels to work: Mechanoelectrical transduction, adaptation, and amplification by hair cells

Hudspeth, A. J.; Choe, Yong Kyung; Mehta, Ashesh D.; Martin, Pascal

doi:10.1073/pnas.97.22.11765

Cited by 241 publications

(210 citation statements)

References 73 publications

(82 reference statements)

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“…The influence of gating currents was not explicitly considered in the original Hodgkin-Huxley (HH) model [1]. In 1975 Hodgkin [31] and, independently, Adrian [32], firstly inquired theoretically into the influence of the ion channel density on the velocity of the action potential propagation along the squid giant axon by taking into consideration the gating currents of sodium ion channels (via an effective capacitance loading caused by ion channels, see also [33]). Remarkably, they found an optimal ion channel density for which the signal velocity is maximal [31,32,[34][35][36].…”

Section: Introductionmentioning

confidence: 99%

Capacitance fluctuations causing channel noise reduction in stochastic Hodgkin–Huxley systems

2006

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Voltage-dependent ion channels determine the electric properties of axonal cell membranes. They not only allow the passage of ions through the cell membrane, but also contribute to an additional charging of the cell membrane resulting in the so-called capacitance loading. The switching of the channel gates between an open and a closed configuration is intrinsically related to the movement of gating charge within the cell membrane. At the beginning of an action potential, the transient gating current is opposite to the direction of the current of sodium ions through the membrane. Therefore, the excitability is expected to become reduced due to the influence of a gating current. Our stochastic Hodgkin-Huxley-like modeling takes into account both the channel noise-i.e. the fluctuations of the number of open ion channels-and the capacitance fluctuations that result from the dynamics of the gating charge. We investigate the spiking dynamics of membrane patches of a variable size and analyze the statistics of the spontaneous spiking. As a main result, we find that the gating currents yield a drastic reduction of the spontaneous spiking rate for sufficiently large ion channel clusters. Consequently, this demonstrates a prominent mechanism for channel noise reduction.

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Section: Introductionmentioning

confidence: 99%

Capacitance fluctuations causing channel noise reduction in stochastic Hodgkin–Huxley systems

2006

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“…This result therefore adds to the evidence that active hair-bundle motility constitutes the active process, at least in the ears of nonmammalian tetrapods (reviewed in refs. [13][14][15]. Bundle motility displays all four hallmarks of the aural active process.…”

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confidence: 99%

Hair-bundle movements elicited by transepithelial electrical stimulation of hair cells in the sacculus of the bullfrog

Bozovic

Hudspeth

2003

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

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Electrically evoked otoacoustic emission is a manifestation of reverse transduction by the inner ear. We present evidence for a single-cell correlate of this phenomenon, hair-bundle movement driven by transepithelial electrical stimulation of the frog's sacculus. Responses could be observed at stimulus frequencies up to 1 kHz, an order of magnitude higher than the organ's natural range of sensitivity to acceleration or sound. Measurements at highstimulus frequencies and pharmacological treatments allow us to distinguish two mechanisms that mediate the electrical responses: myosin-based adaptation and Ca 2؉ -dependent reclosure of transduction channels. These mechanisms also participate in the active process that amplifies and tunes the mechanical responses of this receptor organ. Transient application of the channel blocker gentamicin demonstrated the crucial role of mechanoelectrical transduction channels in the rapid responses to electrical stimulation. A model for electrically driven bundle motion that incorporates the negative stiffness of the hair bundle as well as its two mechanisms of motility captures the essential features of the measured responses.

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“…Hair cells, the nonneural, epithelial mechanoreceptors in vertebrate ears, achieve this sensitivity actively. These cells respond to mechanical stimuli by cell body contractions [mammalian outer hair cells (2,(4)(5)(6)] or active hair bundle twitches [lower tetrapod hair cells (3,7,8)], which, in turn, assist the minute motions induced by sound. The result is a positive mechanical feedback.…”

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confidence: 99%

Motion generation by Drosophila mechanosensory neurons

Göpfert

Robert

2003

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

162

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In Drosophila melanogaster, hearing is supported by mechanosensory neurons transducing sound-induced vibrations of the antenna. It is shown here that these neurons additionally generate motions that mechanically drive the antenna and tune it to relevant sounds. Motion generation in the Drosophila auditory system is betrayed by the auditory mechanics; the antenna of the fly nonlinearly alters its tuning as stimulus intensity declines and oscillates spontaneously in the absence of sound. The susceptibility of auditory motion generation to mechanosensory mutations shows that motion is generated by mechanosensory neurons. Motion generation depends on molecular components of the mechanosensory transduction machinery (NompA, NompC, Btv, and TilB), apparently involving mechanical activity of ciliated dendrites and microtubule-dependent motors. Hence, in analogy to vertebrate hair cells, the mechanosensory neurons of the fly serve dual, transducing, and actuating roles, documenting a striking functional parallel between the vertebrate cochlea and the ears of Drosophila.

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Putting ion channels to work: Mechanoelectrical transduction, adaptation, and amplification by hair cells

Cited by 241 publications

References 73 publications

Capacitance fluctuations causing channel noise reduction in stochastic Hodgkin–Huxley systems

Capacitance fluctuations causing channel noise reduction in stochastic Hodgkin–Huxley systems

Hair-bundle movements elicited by transepithelial electrical stimulation of hair cells in the sacculus of the bullfrog

Motion generation by Drosophila mechanosensory neurons

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