Cochlear transduction: an integrative model and review

A model for cochlear transduction is presented that is based on considerations of the cell biology of its receptor cells, particularly the mechanisms of transmitter release at recepto-neural synapses. Two new interrelated hypotheses on the functional organization of the organ of Corti result from these considerations, one dealing with the possibility of electrotonic interaction between inner and outer hair cells and the other with a possible contributing source to acoustic emissions of cochlear origin that results from vesicular membrane turnover.

[1]  B. Bohne Anatomical Correlates of a Temporary Shift in the Threshold of Hearing , 1973 .

[2]  W. Dougherty,et al.  Neonatal development of circadian rhythm in "synaptic" ribbon numbers in the rat pinealocyte. , 1980, The American journal of anatomy.

[3]  J. Brawer The role of the arcuate nucleus in the brain‐pituitary‐gonad axis , 1971, The Journal of comparative neurology.

[4]  T. Furukawa,et al.  Adaptive rundown of excitatory post‐synaptic potentials at synapses between hair cells and eight nerve fibres in the goldfish. , 1978, The Journal of physiology.

[5]  J. Theron,et al.  Microfilaments, the smooth endoplasmic reticulum and synaptic ribbon fields in the pinealocytes of the baboon (Papio ursinus). , 1979, The American journal of anatomy.

[6]  H. Davis,et al.  Exploration of Cochlear Potentials in Guinea Pig with a Microelectrode , 1954 .

[7]  J. P. Wilson,et al.  Evidence for a cochlear origin for acoustic re-emissions, threshold fine-structure and tonal tinnitus , 1980, Hearing Research.

[8]  H. Wagner Darkness-induced reduction of the number of synaptic ribbons in fish retina. , 1973, Nature: New biology.

[9]  T. Iu Study of synaptic transmission between photoreceptor and horizontal cell by electric stimulations of the retina , 1968 .

[10]  R. Szamier Enzymatic digestion of presynaptic structures in electroreceptors of elasmobranchs. , 1974, The American journal of anatomy.

[11]  S. Schaeffer,et al.  Ultrastructural analysis of functional changes in the synaptic endings of turtle cone cells. , 1976, Cold Spring Harbor symposia on quantitative biology.

[12]  Inner and outer hair cells, differential uptake of horseradish peroxidase: a preliminary report. , 1977 .

[13]  T. Furukawa,et al.  Quantal analysis of the size of excitatory post‐synaptic potentials at synapses between hair cells and afferent nerve fibres in goldfish. , 1978, The Journal of physiology.

[14]  D O Kim,et al.  Cochlear mechanics: nonlinear behavior in two-tone responses as reflected in cochlear-nerve-fiber responses and in ear-canal sound pressure. , 1980, The Journal of the Acoustical Society of America.

[15]  G. Bredberg,et al.  Scanning Electron Microscopy of the Normal and Pathologically Altered Organ of Corti , 1972 .

[16]  F. Sjöstrand,et al.  Structure of the nerve endings on the external hair cells of the guinea pig cochlea as studied by serial sections. , 1961, Journal of ultrastructure research.

[17]  C. Fernández,et al.  DEVELOPMENT OF MAMMALIAN ENDOCOCHLEAR POTENTIAL. , 1963, The Journal of experimental zoology.

[18]  C. Geisler Model of crossed olivocochlear bundle effects. , 1974, The Journal of the Acoustical Society of America.

[19]  D. T. Kemp,et al.  Observations on the Generator Mechanism of Stimulus Frequency Acoustic Emissions — Two Tone Suppression , 1980 .

[20]  D. C. Teas,et al.  Effects of electrical current applied to cochlear partition on discharges in individual auditory-nerve fibers. II. Interaction of electrical polarization and acoustic stimulation. , 1970, The Journal of the Acoustical Society of America.

[21]  D Bodian,et al.  Synapses involving auditory nerve fibers in primate cochlea. , 1978, Proceedings of the National Academy of Sciences of the United States of America.

[22]  C. Nicholson,et al.  Calcium and potassium changes in extracellular microenvironment of cat cerebellar cortex. , 1978, Journal of neurophysiology.

[23]  W. T. Peake,et al.  Intracellular electric responses to sound in a vertebrate cochlea , 1974, Nature.

[24]  M. Blaustein,et al.  Synaptic vesicle recycling in synaptosomes in vitro , 1976, Nature.

[25]  P. Hamrick,et al.  Ion transport in guinea pig cochlea. I. Potassium and sodium transport. , 1978, Acta oto-laryngologica.

[26]  L. Barajas,et al.  Cupular secretion by Xenopus laevis line organs: autoradiographic evidence for incorporation of 3H-glucose and 35S-sulfate. , 1980, American Journal of Anatomy.

[27]  A. Hudspeth,et al.  Sensitivity, polarity, and conductance change in the response of vertebrate hair cells to controlled mechanical stimuli. , 1977, Proceedings of the National Academy of Sciences of the United States of America.

[28]  D. Kemp Stimulated acoustic emissions from within the human auditory system. , 1978, The Journal of the Acoustical Society of America.

[29]  T. Konishi,et al.  The Temporal Relationship Between Motion of the Basilar Membrane and Initiation of Nerve Impulses in the Auditory Nerve Fibers , 1973 .

[30]  P. Siekevitz,et al.  Purification from black widow spider venom of a protein factor causing the depletion of synaptic vesicles at neuromuscular junctions , 1976, The Journal of cell biology.

[31]  A. J. Hudspeth,et al.  Stereocilia mediate transduction in vertebrate hair cells , 1979 .

[32]  H. Spoendlin Neuroanatomy of the Cochlea , 1974 .

[33]  W. A. Hagins,et al.  Signal Transmission along Retinal Rods and the Origin of the Electroretinographic a-Wave , 1969, Nature.

[34]  J. P. Wilson,et al.  Model for cochlear echoes and tinnitus based on an observed electrical correlate , 1980, Hearing Research.

[35]  H. Spoendlin The organization of the cochlear receptor. , 1966, Fortschritte der Hals-Nasen-Ohrenheilkunde.

[36]  C. Devigne,et al.  Significance of presynaptic formations in early stages of cochlear synaptogenesis , 1979, Neuroscience Letters.

[37]  K. Yanagisawa,et al.  Potentials of outer hair cells and their membrane properties in cationic environments , 1980, Hearing Research.

[38]  S. Schaeffer,et al.  Membrane recycling in the cone cell endings of the turtle retina , 1978, The Journal of cell biology.

[39]  A. Flock,et al.  Studies on the sensory hairs of receptor cells in the inner ear. , 1977, Acta oto-laryngologica.

[40]  J. J. Zwislocki,et al.  Velocity and Displacement Responses in Auditory-Nerve Fibers , 1973, Science.

[41]  Alexander Joseph Book reviewDischarge patterns of single fibers in the cat's auditory nerve: Nelson Yuan-Sheng Kiang, with the assistance of Takeshi Watanabe, Eleanor C. Thomas and Louise F. Clark: Research Monograph no. 35. Cambridge, Mass., The M.I.T. Press, 1965 , 1967 .

[42]  T. Reese,et al.  EVIDENCE FOR RECYCLING OF SYNAPTIC VESICLE MEMBRANE DURING TRANSMITTER RELEASE AT THE FROG NEUROMUSCULAR JUNCTION , 1973, The Journal of cell biology.

[43]  A. Flock,et al.  Actin filaments in sensory hairs of inner ear receptor cells , 1977, The Journal of cell biology.

[44]  P. A. Lynn,et al.  Cochlear innervation, signal processing, and their relation to auditory time-intensity effects. , 1970, The Journal of the Acoustical Society of America.

[45]  Y. Katsuki,et al.  Electrical potentials of the subtectorial space in the guinea pig cochlea. , 1977, The Japanese journal of physiology.

[46]  A. J. Duvall,et al.  Delineation of Cochlear Glycogen by Electron Microscopy , 1976, The Annals of otology, rhinology, and laryngology.

[47]  T. Reese,et al.  Freeze‐fracture studies on the synapses in the organ of corti , 1977, The Journal of comparative neurology.

[48]  J. Fex,et al.  Neural Excitatory Processes of the Inner Ear , 1974 .

[49]  T. Konishi,et al.  Summating Potential with Electrical Stimulation of Crossed Olivocochlear Bundles , 1971, Science.

[50]  B. Engström,et al.  Structure of the hairs on cochlear sensory cells , 1978, Hearing Research.

[51]  M. Sanders Handbook of Sensory Physiology , 1975 .

[52]  S. Schacher,et al.  Synaptic activity of frog retinal photoreceptors. A peroxidase uptake study , 1976, The Journal of cell biology.

[53]  T. Konishi,et al.  The temporal relationship between basilar membrane motion and nerve impulse initiation in auditory nerve fibers of guinea pigs. , 1978, The Japanese journal of physiology.

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

[55]  Juergen Tonndorf,et al.  Dual Origin of the Cochlear Microphonics Inner and Outer Hair Cells , 1972, The Annals of otology, rhinology, and laryngology.

[56]  W. Saunders,et al.  Structural Pattern of the Organ of Corti. , 1967 .

[57]  J. Desmedt,et al.  Ionic mechanism of the efferent olivo‐cochlear inhibition studied by cochlear perfusion in the cat. , 1975, The Journal of physiology.

[58]  C. Rovainen,et al.  Structure and chemistry of glucose-producing cells in meningeal tissue of the lamprey. , 1971, Brain research.

[59]  J J Zwislocki,et al.  Phase opposition between inner and outer hair cells and auditory sound analysis. , 1975, Audiology : official organ of the International Society of Audiology.

[60]  J. Nadol Reciprocal Synapses at the Base of Outer Hair Cells in the Organ of Corti of Man , 1981, The Annals of otology, rhinology, and laryngology.

[61]  D. T. Kemp,et al.  Properties of the generator of stimulated acoustic emissions , 1980, Hearing Research.

[62]  L. Illis,et al.  Enlargement of Spinal Cord Synapses after Repetitive Stimulation of a Single Posterior Root , 1969, Nature.

[63]  T. Reese,et al.  Intercellular junctions in the reticular lamina of the organ of Corti , 1976 .

[64]  D. Lim Fine morphology of the tectorial membrane. Its relationship to the organ of Corti. , 1972, Archives of otolaryngology.

[65]  J. Zwislocki,et al.  Neuro-Mechanical Frequency Analysis in the Cochlea , 1974 .

[66]  R. Fettiplace,et al.  The frequency selectivity of auditory nerve fibres and hair cells in the cochlea of the turtle , 1980, The Journal of physiology.

[67]  H. Ades,et al.  Effect of high-intensity noise on inner ear sensory epithelia. , 1960, Acta oto-laryngologica. Supplementum.

[68]  W. P. Hurlbut,et al.  Vesicle hypothesis of the release of quanta of acetylcholine. , 1980, Physiological Reviews.

[69]  H Ripps,et al.  Peroxidase uptake by photoreceptor terminals of the skate retina , 1976, The Journal of cell biology.

[70]  J. P. Wilson,et al.  The Combination Tone, 2f1 – f2, in Psychophysics and Ear-Canal Recording , 1980 .

[71]  E. Pannese,et al.  Intercellular junctions in the organ of Corti as revealed by freeze fracturing. , 1976, Acta oto-laryngologica.

[72]  R. Thalmann Recent refinements of quantitative microchemical analysis of tissues and cells of the inner ear. , 1972, Acta oto-laryngologica.

[73]  K. Jahnke,et al.  The fine structure of freeze-fractured intercellular junctions in the guinea pig inner ear. , 1975, Acta oto-laryngologica. Supplementum.

[74]  J. Raynauld,et al.  Goldfish retina: a correlate between cone activity and morphology of the horizontal cell in clone pedicules. , 1979, Science.

[75]  Role of inner and outer hair cells in neural excitation. , 1976, Transactions. Section on Otolaryngology. American Academy of Ophthalmology and Otolaryngology.

[76]  M. Magalhães,et al.  ELECTRON MICROSCOPE RADIOAUTOGRAPHIC STUDY OF GLYCOGEN SYNTHESIS IN THE RABBIT RETINA , 1970, The Journal of cell biology.

[77]  R. Kimura,et al.  The ultrastructure of the organ of Corti. , 1975, International review of cytology.

[78]  R. Kelly,et al.  Biochemistry of neurotransmitter release. , 1979, Annual review of neuroscience.

[79]  A. Kronester-frei The effect of changes in endolymphatic ion concentrations on the tectorial membrane , 1979, Hearing Research.

[80]  A. J. Duvall,et al.  Cochlear Transport of Horseradish Peroxidase , 1972, The Annals of otology, rhinology, and laryngology.

[81]  A. J. Hudspeth,et al.  Ionic basis of the receptor potential in a vertebrate hair cell , 1979, Nature.

[82]  H. Baumann,et al.  Turnover of the plasma membrane of mammalian cells. , 1979, Life sciences.

[83]  Presynaptic bodies in outer hair cells of the chinchilla organ of Corti , 1981, Brain Research.

[84]  D. Mountain,et al.  Changes in endolymphatic potential and crossed olivocochlear bundle stimulation alter cochlear mechanics. , 1980, Science.

[85]  M J Mulroy,et al.  The organization of actin filaments in the stereocilia of cochlear hair cells , 1980, The Journal of cell biology.

[86]  J J Zwislocki,et al.  Tectorial membrane: a possible effect on frequency analysis in the cochlea. , 1979, Science.

[87]  A. Nuttall,et al.  Electrical potentials and fluid boundaries within the organ of Corti. , 1974, The Journal of the Acoustical Society of America.

[88]  D Strelioff A computer simulation of the generation and distribution of cochlear potentials. , 1973, The Journal of the Acoustical Society of America.

[89]  A. Sans,et al.  Morphological changes in afferent vestibular hair cell synapses during the postnatal development of the cat , 1979, Journal of neurocytology.

[90]  B. Christensen,et al.  A quantitative analysis of ultrastructural changes induced by electrical stimulation of identified spinal cord axons in the larval lamprey , 1980, Journal of neurocytology.

[91]  L. Tauc,et al.  Are vesicles necessary for release of acetylcholine at cholinergic synapses? , 1979, Biochemical pharmacology.

[92]  P. Dallos,et al.  Bioelectric correlates of kanamycin intoxication. , 1974, Audiology : official organ of the International Society of Audiology.

[93]  P Gouras,et al.  Horizontal cells in cat retina with independent dendritic systems. , 1975, Science.

[94]  A. Salt,et al.  Effects of noise on cochlear potentials and endolymph potassium concentration recorded with potassium-selective electrodes , 1979, Hearing Research.

[95]  H. Zimmermann Vesicle recycling and transmitter release , 1979, Neuroscience.

[96]  M. Magalhães,et al.  The rabbit retina Müller cell. A fine structural and cytochemical study. , 1972, Journal of ultrastructure research.

[97]  A. Flock Electron probe determination of relative ion distribution in the inner ear. , 1977, Acta oto-laryngologica.

[98]  G. Manley,et al.  The Electrophysiological Profile of the Organ of Corti , 1980 .

[99]  T. Furukawa,et al.  Synaptic delay and time course of postsynaptic potentials at the junction between hair cells and eighth nerve fibers in the goldfish. , 1972, The Japanese journal of physiology.

[100]  S. Schacher,et al.  Uptake of horseradish peroxidase by frog photoreceptor synapses in the dark and the light , 1974, Nature.

[101]  C. Fernández,et al.  Postnatal development of endocochlear potential and stria vascularis in the cat. , 1974, Acta oto-laryngologica.

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

[103]  D. Morest,et al.  Receptor synapses without synaptic ribbons in the cochlea of the cat. , 1975, Proceedings of the National Academy of Sciences of the United States of America.

[104]  R B Szamier,et al.  Special cutaneous receptor organs of fish: IV. Ampullary organs of the nonelectric catfish, Kryptopterus , 1969, Journal of morphology.

[105]  I. Tasaki,et al.  Modification of cochlear microphonics and action potentials by KC1 solution and by direct currents. , 1952, Journal of neurophysiology.

[106]  H. Davis Transmission and transduction in the cochlea , 1958 .

[107]  N. Kiang,et al.  Effects of electric stimulation of the crossed olivocochlear bundle on single auditory-nerve fibers in the cat. , 1970, The Journal of the Acoustical Society of America.

[108]  H. Engström,et al.  THE NORMAL ORGAN OF CORTI , 1973 .

[109]  B. Katz,et al.  Tetrodotoxin‐resistant electric activity in presynaptic terminals , 1969, The Journal of physiology.

[110]  R. Kimura,et al.  Hairs of the cochlear sensory cells and their attachment to the tectorial membrane. , 1966, Acta oto-laryngologica.

[111]  H. Wagner,et al.  Light-dependent plasticity of the morphology of horizontal cell terminals in cone pedicles of fish retinas , 1980, Journal of neurocytology.

[112]  F. Sjöstrand,et al.  A synaptic structure in the hair cells of the guinea pig cochlea , 1961 .

[113]  R. Perkins,et al.  A study of cochlear innervation patterns in cats and rats with the Golgi method and Nomarski optics , 1975, The Journal of comparative neurology.

[114]  H. Spoendlin Innervation patterns in the organ of corti of the cat. , 1969, Acta oto-laryngologica.

[115]  A. R. Freeman,et al.  Stimulation-Dependent Alterations in Peroxidase Uptake at Lobster Neuromuscular Junctions , 1971, Science.

[116]  C. Geisler Letter: Hypothesis on the function of the crossed olivocochlear bundle. , 1974, The Journal of the Acoustical Society of America.

[117]  D. C. Teas,et al.  Electrophysiological Studies on the Spatial Distribution of the Crossed Olivocochlear Bundle along the Guinea Pig Cochlea , 1970 .

[118]  Effects of electrical current applied to cochlear partition on discharges in individual auditory-nerve fibers. I. Prolonged direct-current polarization. , 1970, The Journal of the Acoustical Society of America.

[119]  A M MULLINGER,et al.  The fine structure of ampullary electric receptors in Amiurus , 1964, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[120]  A. J. Goldstein,et al.  XXXIII Separation of the Organ of Corti into its Component Cells , 1967, The Annals of otology, rhinology, and laryngology.

[121]  H. W. Lissmann,et al.  Organization of ampullary electric receptors in Gymnotidae (Pisces) , 1968, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[122]  P Dallos,et al.  Production of cochlear potentials by inner and outer hair cells. , 1976, The Journal of the Acoustical Society of America.

[123]  Alec N. Salt,et al.  Effects of exposure to noise on ion movement in guinea pig cochlea , 1979, Hearing Research.

[124]  Duck O. Kim,et al.  An Active Cochlear Model with Negative Damping in the Partition: Comparison with Rhode’s Ante- and Post-Mortem Observations , 1980 .

[125]  A. Møller,et al.  Some dualistic properties of the cochlear microphonic , 1980, Hearing Research.

[126]  T. Furukawa,et al.  Quantal nature of transmission at the synapse between hair cells and eighth nerve fibers. , 1971, The Japanese journal of physiology.

[127]  A. Hudspeth,et al.  Passive signal propagation and membrane properties in median photoreceptors of the giant barnacle , 1977, The Journal of physiology.

[128]  T. Hoshino Attachment of the inner sensory cell hairs to the tectorial membrane. A scanning electron microscopic study. , 1976, ORL; journal for oto-rhino-laryngology and its related specialties.

[129]  T. Konishi,et al.  Effects of the electrical stimulation of the crossed olivocochlear bundle on cochlear potentials recorded with intracochlear electrodes in guinea pigs. , 1971, The Journal of the Acoustical Society of America.

[130]  V Honrubia,et al.  Neural transduction in Xenopus laevis lateral line system. , 1978, Journal of neurophysiology.

[131]  T. Reese,et al.  Regional specialization of the hair cell plasmalemma in the organ of corti , 1977, The Anatomical record.

[132]  G. Manley Cochlear frequency sharpening-a new synthesis. , 1978, Acta oto-laryngologica.

[133]  H. Ades,et al.  Anatomy of the Inner Ear , 1974 .

[134]  J. Nadol Intercellular Fluid Pathways in the Organ of Corti of Cat and Man , 1979, Annals of Otology, Rhinology and Laryngology.

[135]  W. T. Peake,et al.  Cochlear responses to condensation and rarefaction clicks. , 1962, Biophysical journal.

[136]  R. A. Schmiedt,et al.  Inferred response polarities of cochlear hair cells. , 1976, The Journal of the Acoustical Society of America.

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

[138]  A. Mauro,et al.  TURNOVER OF TRANSMITTER AND SYNAPTIC VESICLES AT THE FROG NEUROMUSCULAR JUNCTION , 1973, The Journal of cell biology.

[139]  A. H. Bunt Enzymatic digestion of synaptic ribbons in amphibian retinal photoreceptors. , 1971, Brain research.

[140]  R. Fettiplace,et al.  The coding of sound pressure and frequency in cochlear hair cells of the terrapin , 1978, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[141]  P M Sellick,et al.  Intracellular studies of hair cells in the mammalian cochlea. , 1978, The Journal of physiology.