A fast motile response in guinea‐pig outer hair cells: the cellular basis of the cochlear amplifier.

1. Outer hair cells from the cochlea of the guinea‐pig were isolated and their motile properties studied in short‐term culture by the whole‐cell variant of the patch recording technique. 2. Cells elongated and shortened when subjected to voltage steps. Cells from both high‐ and low‐frequency regions of the cochlea responded with an elongation when hyperpolarized and a shortening when depolarized. The longitudinal motion of the cell was measured by a differential photosensor capable of responding to motion frequencies 0‐40 kHz. 3. Under voltage clamp the length change of the cell was graded with command voltage over a range +/‐ 2 microns (approximately 4% of the length) for cells from the apical turns of the cochlea. The mean sensitivity of the movement was 2.11 nm/pA injected current, or 19.8 nm/mV membrane polarization. 4. The kinetics of the cell length change during a voltage step were measured. Stimulated at their basal end, cells from the apical (low‐frequency) cochlear turns responded with a latency of between 120 and 255 microseconds. The cells thereafter elongated exponentially by a process which could be characterized by three time constants, one with value 240 microseconds, and a second in the range 1.3‐2.8 ms. A third time constant with a value 20‐40 ms characterized a slower component which may represent osmotic changes. 5. Consistent with the linearity shown to voltage steps, sinusoidal stimulation of the cell generated movements which could be measured at frequencies above 1 kHz. The phase of the movement relative to the stimulus continued to grow with frequency, suggesting the presence of an absolute delay in the response of about 200 microseconds. 6. The electrically stimulated movements were insensitive to the ionic composition of the cell, manipulated by dialysis from the patch pipette. The responses occurred when the major cation was K+ or Na+ in the pipette. Loading the cell with ATP‐free solutions or calcium buffers did not inhibit the response. 7. It is concluded that interaction between actin and myosin, although present in the cell, is unlikely to account for the cell motility. Instead, it is proposed that outer hair cell motility is associated with structures in the cell cortex. The implications for cochlear mechanics of such force generation in outer hair cells are discussed.

[1]  Review Paper: Hair Cells, Receptors with a Motor Capacity? , 1938 .

[2]  H. Davis,et al.  A model for transducer action in the cochlea. , 1965, Cold Spring Harbor symposia on quantitative biology.

[3]  C D Geisler,et al.  Model of the displacement between opposing points on the tectorial membrane and reticular lamina. , 1967, The Journal of the Acoustical Society of America.

[4]  C. Nicholson Electric current flow in excitable cells J. J. B. Jack, D. Noble &R. W. Tsien Clarendon Press, Oxford (1975). 502 pp., £18.00 , 1976, Neuroscience.

[5]  J. Pringle The Croonian Lecture, 1977 - Stretch activation of muscle: function and mechanism , 1978, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[6]  D. Lim,et al.  Cochlear anatomy related to cochlear micromechanics. A review. , 1980, The Journal of the Acoustical Society of America.

[7]  J. Allen,et al.  Cochlear micromechanics--a physical model of transduction. , 1980, The Journal of the Acoustical Society of America.

[8]  A. Luff,et al.  Dynamic properties of the inferior rectus, extensor digitorum longus, diaphragm and soleus muscles of the mouse. , 1981, The Journal of physiology.

[9]  Anthony W. Gummer,et al.  Direct measurement of basilar membrane stiffness in the guinea pig , 1981 .

[10]  K. Iwasa,et al.  Rapid pressure changes and surface displacements in the squid giant axon associated with production of action potentials. , 1982, The Japanese journal of physiology.

[11]  P Dallos,et al.  Intracellular recordings from cochlear outer hair cells. , 1982, Science.

[12]  S M Khanna,et al.  Basilar membrane tuning in the cat cochlea. , 1982, Science.

[13]  S Inoué,et al.  Acrosomal reaction of Thyone sperm. II. The kinetics and possible mechanism of acrosomal process elongation , 1982, The Journal of cell biology.

[14]  Y. Goldman,et al.  Relaxation of muscle fibres by photolysis of caged ATP , 1982, Nature.

[15]  B. M. Johnstone,et al.  Measurement of basilar membrane motion in the guinea pig using the Mössbauer technique. , 1982, The Journal of the Acoustical Society of America.

[16]  Hallowell Davis,et al.  An active process in cochlear mechanics , 1983, Hearing Research.

[17]  K L Magleby,et al.  Calcium dependence of open and shut interval distributions from calcium‐activated potassium channels in cultured rat muscle. , 1983, The Journal of physiology.

[18]  A. Nuttall,et al.  The temperature dependency of neural and hair cell responses evoked by high frequencies. , 1983, The Journal of the Acoustical Society of America.

[19]  E de Boer No sharpening? a challenge for cochlear mechanics. , 1983, The Journal of the Acoustical Society of America.

[20]  A. Flock,et al.  Stiffness of sensory-cell hair bundles in the isolated guinea pig cochlea , 1984, Hearing Research.

[21]  M. Charles Liberman,et al.  Single-neuron labeling and chronic cochlear pathology. II. Stereocilia damage and alterations of spontaneous discharge rates , 1984, Hearing Research.

[22]  A. Nuttall,et al.  Efferent control of cochlear inner hair cell responses in the guinea‐pig. , 1984, The Journal of physiology.

[23]  S. Terakawa Potential‐dependent variations of the intracellular pressure in the intracellularly perfused squid giant axon. , 1985, The Journal of physiology.

[24]  P Dallos,et al.  Response characteristics of mammalian cochlear hair cells , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[25]  C E Miller Structural implications of basilar membrane compliance measurements. , 1985, The Journal of the Acoustical Society of America.

[26]  I. Russell,et al.  Outer hair cells in the mammalian cochlea and noise-induced hearing loss , 1985, Nature.

[27]  A. Flock,et al.  Ultrastructural morphology of enzyme-dissociated cochlear sensory cells. , 1985, Acta oto-laryngologica.

[28]  The Cellular Physiology of Isolated Outer Hair Cells: Implications for Cochlear Frequency Selectivity , 1986 .

[29]  V. Torre,et al.  Incorporation of calcium buffers into salamander retinal rods: a rejection of the calcium hypothesis of phototransduction. , 1986, The Journal of physiology.

[30]  I. J. Russell,et al.  The responses of inner and outer hair cells in the basal turn of the guinea-pig cochlea and in the mouse cochlea grown in vitro , 1986, Hearing Research.

[31]  C. Daniel Geisler,et al.  A model of the effect of outer hair cell motility on cochlear vibrations , 1986, Hearing Research.

[32]  S. Neely,et al.  A model for active elements in cochlear biomechanics. , 1986, The Journal of the Acoustical Society of America.