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Davis—1961 Revisited: Signal Transmission in the Cochlear Hair Cell-Nerve Junction

Davis—1961 Revisited: Signal Transmission in the Cochlear Hair Cell-Nerve Junction Abstract • In 1961, Hallowell Davis proposed the occurrence of the following general sequence of interrelated events in sense organs, in response to specific sensory inputs: (1) the generation of receptor potentials in the sensory cells; (2) chemical transmission across the synapses between hair cells and afferent dendrites; and (3) the triggering of postsynaptic generator potentials capable of eliciting the actual nerve action potentials. Although at the time of his writing there was no evidence for this hypothesis in the auditory organ, there is now good support for the occurrence of all three events and for their general importance in the sensory transduction process. (Arch Otolaryngol 101:528-535, 1975) References 1. Davis H: Some principles of sensory receptor action . Physiol Rev 41:391-416, 1961. 2. Eccles JS: Neuron physiology—Introduction , in Field J (ed): Handbook of Physiology . Washington, American Physiological Society, 1959, chap 2. 3. Drischel H: Das Neuronale Gedächtnis , in Scharf JH (ed): Informatik : Leipzig, JA Barth, 1972, pp 325-354. 4. Békésy G von: DC resting potentials inside the cochlear partition . J Acoust Soc Am 25:770-785, 1953. 5. Békésy G von: Shearing microphonics produced by vibrations near the inner and outer hair cells . J Acoust Soc Am 25:786-790, 1953.Crossref 6. Hilding AD: The tectorial membrane in the theory of hearing . Ann Otol Rhinol Laryngol 62:757-769,1953. 7. Tonndorf J: Shearing motion in scala media of cochlear models . J Acoust Soc Am 32:238-244, 1969.Crossref 8. Lowenstein 0, Wersäll J: A functional interpretation of the electron microscopic structure of the sensory hairs in the crista of the elasmobranch, Raja clavata, in terms of directional sensitivity . Nature 184:1807-1810, 1959.Crossref 9. Flock A: Sensory tranduction in hair cells , in Lowenstein WR (ed): Handbook of Sensory Physiology, Vol 1, Principles of Receptor Physiology . Berlin, Springer Verlag, 1971, pp 396-441. 10. Friedman J: La cytologie de l'oreille an microscope electrique . Triangle 6:74, 1963. 11. Dallos P, Billone MC, Durrant JD, et al: Cochlear inner and outer hair cells: Functional differences . Science 177:356-358, 1972.Crossref 12. Zwislocki JJ, Sokolich WG: Velocity and displacement responses in auditory-nerve fibers . Science 182:64-66, 1973.Crossref 13. Lim DJ: Fine morphology of the tectorial membrane; its relationship to the organ of Corti . Arch Otolaryngol 96:199-215, 1972.Crossref 14. Flock A: Lateral line organs and amphibian hearing organs . J Acoust Soc Am 54:440, 1973. 15. Harris GG, Frishkopf L, Flock A: Receptor potentials in the hair cells of mudpuppy lateral line . J Acoust Soc Am 45:300-301, 1969.Crossref 16. Harris GG, Frishkopf L, Flock A: Receptor potentials from hair cells of the lateral line . Science 167:76-79, 1970.Crossref 17. Békésy G von: DC potentials and energy balance of the cochlear partition . J Acoust Soc Am 23:574-582, 1951. 18. Engström H, Ades HW, Hawkins JE Jr: Structure and functions of the sensory hairs of the inner ears . J Acoust Soc Am 34:1356-1363, 1962.Crossref 19. Hilman DE, Lewis ER: Morphological basis for a mechanical linkage in otolithic receptor transduction in the frog . Science 174:416-419, 1971.Crossref 20. Kimura RS: Hairs of the cochlear sensory cells and their attachment to the tectorial membrane . Acta Otolaryngol 61:55-72, 1966.Crossref 21. Spoendlin H: The organization of the cochlear receptor , in Ruedi L (ed): Advances in Oto Rhino Laryngology , Basel, Karger, 1966, vol 13. 22. Tonndorf J: Invited discussion to session 1 , in Sachs MB (ed): Physiology of the Auditory System . Baltimore, National Education Consultants, 1971, pp 69-75. 23. Wever EG, Bray C: Action currents in the auditory nerve in response to acoustic stimulation . Proc Natl Acad Sci USA 16:344-450, 1930.Crossref 24. Davis H: in Stevens SS, Davis H (eds): Hearing . New York, John Wiley & Sons Inc, 1938, pp 310-355. 25. Davis H: Mechanism of excitation of auditory nerve impulses , in Rasmussen GL, Windle WF (eds): Neural Mechanisms of the Auditory and Vestibular Systems . Springfield Ill, Charles C Thomas, Publisher, 1960. 26. Dallos P: The Auditory Periphery . New York, Academic Press, 1973, pp 218-464. 27. Honrubia V, Ward PH: Properties of the summating potentials of the guinea pig's cochlea . J Acoust Soc Am 45:1443-1450, 1969.Crossref 28. Strelioff D: A computer simulation of the generation and distribution of cochlear potentials . J Acoust Soc Am 54:620-629, 1973.Crossref 29. Adrian ED, Bronk DW, Phillips G: The nervous origin of the Wever and Bray effect . J Physiol 7:28-30, 1931. 30. Tasaki I, Davis H, Eldredge DH: Exploration of cochlear potentials with a microelectrode . J Acoust Soc Am 26:765-773, 1954.Crossref 31. Tasaki I, Davis H, Legouix JP: The space-time pattern of the cochlear microphonics (guinea pig) as recorded by differential electrodes . J Acoust Soc Am 24:502-518, 1952.Crossref 32. Zwislocki JJ: The nature of auditory stimuli and their attenuation. ONR Symposium Report ACR-1, 182-190, 1955. 33. Dallos P: Comments on the differential-electrode technique . J Acoust Soc Am 45:99-1007, 1969. 34. Békésy G von: DC resting potentials inside the cochlear partition . J Acoust Soc Am 24:72-76, 1952.Crossref 35. Davis H: Initiation of nerve impulses in the cochlea and other mechano-receptors , in Bullock TH (ed): Physiological Triggers and Discontinuous Rate Process . Washington, DC, American Physiological Society, 1956, pp 60-71. 36. Weiss TF, Peake WT, Sohmer HS: Intracochlear potential recorded with micropipets: III. Relation of cochlear microphonic potential to stapes velocity . J Acoust Soc Am 50:602-615, 1971.Crossref 37. Goto T: Experimental studies of the intracellular negative potential of the organ of Corti in the various conditions . Jap J Otolaryngol 76:82-107, 1973. 38. de Vries HL: Brownian motion and the transmission of energy in the cochlea . J Acoust Soc Am 24:527-533, 1952.Crossref 39. Furukawa I, Ishii Y, Matsuura S: An analysis of microphonic potentials of the sacculus of golfish . Jap J Physiol 22:602-616, 1972. 40. Woolsey CN, Walzl EM: Topical projections of nerve fibers from local regions of the cochlea to the cerebral cortex of cat . Bull Hopkins Hosp 71:315-344, 1930. 41. Smith CA, Sjöstrand FS: Asynaptic structure in the hair cells of the guinea pig cochlea . J Ultrastruct Res 5:184-192, 1961.Crossref 42. de Robertis E: Histophysiologische Aspekte der Signalübermittlung im Nervensystem: die Rolle der synaptischen Bläschen . Triangle 5:76-89, 1961. 43. Churchill JA, Schuknecht HF, Doran R: Acetylcholinesterase activity in the cochlea . Laryngoscope 66:1-15, 1958. 44. Schuknecht HF, Churchill JA, Doran R: The localization of acetylcholinesterase in the cochlea . Arch Otolaryngol 69:549-559, 1959.Crossref 45. Axelrod J: Noradrenaline: Fate and control of its biosynthesis . Science 173:598-606,1971.Crossref 46. Axelrod J: Neurotransmitters . Sci Am 239:58-71, 1974.Crossref 47. Nachmansohn D: Proteins in excitable membranes . Science 168:1059-1066, 1970.Crossref 48. Neumann E, Nachmansohn D, Katchalsky A: An attempt at an integral interpretation of nerve excitability . Proc Natl Acad Sci USA 70:727-731, 1973.Crossref 49. Thornhill RA: The effect of catecholamine precursors and related drugs on the morphology of the synaptic bar in the vestibular epithelia of the frog, Rana temporaria . Comp Gen Pharmacol 3:89-97, 1972.Crossref 50. Osborne MP, Thornhill RA: The effect of monamine depleting drugs upon the synaptic bars in the inner ear of the bullfrog (Rana catesbeiana) . Z Zellforsch Mikrosk Anat 127:347-355, 1972.Crossref 51. Flock A: Neurobiology of hair cells and their synapse , in Zwicker E, Terhardt E (eds): Facts and Models in Hearing . Berlin, Springer Verlag, 1974, pp 37-42. 52. Lowry BL, Godfrey DA, Carter JA, et al: Quantitative distribution of alleged transmitter amino acids in the cochlear nucleus . J Acoust Soc Am ( (Fall suppl) ):19, 1974. 53. Davis H, Fernandez C, McAudiffe DR: The excitatory process in the cochlea . Proc Natl Acad Sci USA 36:580-587, 1950.Crossref 54. Dallos P, Schoeny ZG, Cheatham MA: Cochlear summating potentials: Composition . Science 170:641-644, 1970.Crossref 55. Dallos P: Summating potentials in the cochlea , in Sachs MS (ed): Physiology of the Auditory System . Baltimore, National Education Consultants Inc, 1971, pp 57-67. 56. Dallos P, Cheatham MA: Generator potentials: Are they identifiable from gross cochlear recordings? J Acoust Soc Am ( (Fall suppl) ):10, 1974. 57. Stevens SS: On the psychophysical law . Psychol Rev 64:153-181, 1957.Crossref 58. Stevens SS: Neural events and the psychophysical law . Science 170:1043-1050, 1970.Crossref http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Archives of Otolaryngology American Medical Association

Davis—1961 Revisited: Signal Transmission in the Cochlear Hair Cell-Nerve Junction

Archives of Otolaryngology , Volume 101 (9) – Sep 1, 1975

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References (69)

Publisher
American Medical Association
Copyright
Copyright © 1975 American Medical Association. All Rights Reserved.
ISSN
0003-9977
DOI
10.1001/archotol.1975.00780380006002
Publisher site
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Abstract

Abstract • In 1961, Hallowell Davis proposed the occurrence of the following general sequence of interrelated events in sense organs, in response to specific sensory inputs: (1) the generation of receptor potentials in the sensory cells; (2) chemical transmission across the synapses between hair cells and afferent dendrites; and (3) the triggering of postsynaptic generator potentials capable of eliciting the actual nerve action potentials. Although at the time of his writing there was no evidence for this hypothesis in the auditory organ, there is now good support for the occurrence of all three events and for their general importance in the sensory transduction process. (Arch Otolaryngol 101:528-535, 1975) References 1. Davis H: Some principles of sensory receptor action . Physiol Rev 41:391-416, 1961. 2. Eccles JS: Neuron physiology—Introduction , in Field J (ed): Handbook of Physiology . Washington, American Physiological Society, 1959, chap 2. 3. Drischel H: Das Neuronale Gedächtnis , in Scharf JH (ed): Informatik : Leipzig, JA Barth, 1972, pp 325-354. 4. Békésy G von: DC resting potentials inside the cochlear partition . J Acoust Soc Am 25:770-785, 1953. 5. Békésy G von: Shearing microphonics produced by vibrations near the inner and outer hair cells . J Acoust Soc Am 25:786-790, 1953.Crossref 6. Hilding AD: The tectorial membrane in the theory of hearing . Ann Otol Rhinol Laryngol 62:757-769,1953. 7. Tonndorf J: Shearing motion in scala media of cochlear models . J Acoust Soc Am 32:238-244, 1969.Crossref 8. Lowenstein 0, Wersäll J: A functional interpretation of the electron microscopic structure of the sensory hairs in the crista of the elasmobranch, Raja clavata, in terms of directional sensitivity . Nature 184:1807-1810, 1959.Crossref 9. Flock A: Sensory tranduction in hair cells , in Lowenstein WR (ed): Handbook of Sensory Physiology, Vol 1, Principles of Receptor Physiology . Berlin, Springer Verlag, 1971, pp 396-441. 10. Friedman J: La cytologie de l'oreille an microscope electrique . Triangle 6:74, 1963. 11. Dallos P, Billone MC, Durrant JD, et al: Cochlear inner and outer hair cells: Functional differences . Science 177:356-358, 1972.Crossref 12. Zwislocki JJ, Sokolich WG: Velocity and displacement responses in auditory-nerve fibers . Science 182:64-66, 1973.Crossref 13. Lim DJ: Fine morphology of the tectorial membrane; its relationship to the organ of Corti . Arch Otolaryngol 96:199-215, 1972.Crossref 14. Flock A: Lateral line organs and amphibian hearing organs . J Acoust Soc Am 54:440, 1973. 15. Harris GG, Frishkopf L, Flock A: Receptor potentials in the hair cells of mudpuppy lateral line . J Acoust Soc Am 45:300-301, 1969.Crossref 16. Harris GG, Frishkopf L, Flock A: Receptor potentials from hair cells of the lateral line . Science 167:76-79, 1970.Crossref 17. Békésy G von: DC potentials and energy balance of the cochlear partition . J Acoust Soc Am 23:574-582, 1951. 18. Engström H, Ades HW, Hawkins JE Jr: Structure and functions of the sensory hairs of the inner ears . J Acoust Soc Am 34:1356-1363, 1962.Crossref 19. Hilman DE, Lewis ER: Morphological basis for a mechanical linkage in otolithic receptor transduction in the frog . Science 174:416-419, 1971.Crossref 20. Kimura RS: Hairs of the cochlear sensory cells and their attachment to the tectorial membrane . Acta Otolaryngol 61:55-72, 1966.Crossref 21. Spoendlin H: The organization of the cochlear receptor , in Ruedi L (ed): Advances in Oto Rhino Laryngology , Basel, Karger, 1966, vol 13. 22. Tonndorf J: Invited discussion to session 1 , in Sachs MB (ed): Physiology of the Auditory System . Baltimore, National Education Consultants, 1971, pp 69-75. 23. Wever EG, Bray C: Action currents in the auditory nerve in response to acoustic stimulation . Proc Natl Acad Sci USA 16:344-450, 1930.Crossref 24. Davis H: in Stevens SS, Davis H (eds): Hearing . New York, John Wiley & Sons Inc, 1938, pp 310-355. 25. Davis H: Mechanism of excitation of auditory nerve impulses , in Rasmussen GL, Windle WF (eds): Neural Mechanisms of the Auditory and Vestibular Systems . Springfield Ill, Charles C Thomas, Publisher, 1960. 26. Dallos P: The Auditory Periphery . New York, Academic Press, 1973, pp 218-464. 27. Honrubia V, Ward PH: Properties of the summating potentials of the guinea pig's cochlea . J Acoust Soc Am 45:1443-1450, 1969.Crossref 28. Strelioff D: A computer simulation of the generation and distribution of cochlear potentials . J Acoust Soc Am 54:620-629, 1973.Crossref 29. Adrian ED, Bronk DW, Phillips G: The nervous origin of the Wever and Bray effect . J Physiol 7:28-30, 1931. 30. Tasaki I, Davis H, Eldredge DH: Exploration of cochlear potentials with a microelectrode . J Acoust Soc Am 26:765-773, 1954.Crossref 31. Tasaki I, Davis H, Legouix JP: The space-time pattern of the cochlear microphonics (guinea pig) as recorded by differential electrodes . J Acoust Soc Am 24:502-518, 1952.Crossref 32. Zwislocki JJ: The nature of auditory stimuli and their attenuation. ONR Symposium Report ACR-1, 182-190, 1955. 33. Dallos P: Comments on the differential-electrode technique . J Acoust Soc Am 45:99-1007, 1969. 34. Békésy G von: DC resting potentials inside the cochlear partition . J Acoust Soc Am 24:72-76, 1952.Crossref 35. Davis H: Initiation of nerve impulses in the cochlea and other mechano-receptors , in Bullock TH (ed): Physiological Triggers and Discontinuous Rate Process . Washington, DC, American Physiological Society, 1956, pp 60-71. 36. Weiss TF, Peake WT, Sohmer HS: Intracochlear potential recorded with micropipets: III. Relation of cochlear microphonic potential to stapes velocity . J Acoust Soc Am 50:602-615, 1971.Crossref 37. Goto T: Experimental studies of the intracellular negative potential of the organ of Corti in the various conditions . Jap J Otolaryngol 76:82-107, 1973. 38. de Vries HL: Brownian motion and the transmission of energy in the cochlea . J Acoust Soc Am 24:527-533, 1952.Crossref 39. Furukawa I, Ishii Y, Matsuura S: An analysis of microphonic potentials of the sacculus of golfish . Jap J Physiol 22:602-616, 1972. 40. Woolsey CN, Walzl EM: Topical projections of nerve fibers from local regions of the cochlea to the cerebral cortex of cat . Bull Hopkins Hosp 71:315-344, 1930. 41. Smith CA, Sjöstrand FS: Asynaptic structure in the hair cells of the guinea pig cochlea . J Ultrastruct Res 5:184-192, 1961.Crossref 42. de Robertis E: Histophysiologische Aspekte der Signalübermittlung im Nervensystem: die Rolle der synaptischen Bläschen . Triangle 5:76-89, 1961. 43. Churchill JA, Schuknecht HF, Doran R: Acetylcholinesterase activity in the cochlea . Laryngoscope 66:1-15, 1958. 44. Schuknecht HF, Churchill JA, Doran R: The localization of acetylcholinesterase in the cochlea . Arch Otolaryngol 69:549-559, 1959.Crossref 45. Axelrod J: Noradrenaline: Fate and control of its biosynthesis . Science 173:598-606,1971.Crossref 46. Axelrod J: Neurotransmitters . Sci Am 239:58-71, 1974.Crossref 47. Nachmansohn D: Proteins in excitable membranes . Science 168:1059-1066, 1970.Crossref 48. Neumann E, Nachmansohn D, Katchalsky A: An attempt at an integral interpretation of nerve excitability . Proc Natl Acad Sci USA 70:727-731, 1973.Crossref 49. Thornhill RA: The effect of catecholamine precursors and related drugs on the morphology of the synaptic bar in the vestibular epithelia of the frog, Rana temporaria . Comp Gen Pharmacol 3:89-97, 1972.Crossref 50. Osborne MP, Thornhill RA: The effect of monamine depleting drugs upon the synaptic bars in the inner ear of the bullfrog (Rana catesbeiana) . Z Zellforsch Mikrosk Anat 127:347-355, 1972.Crossref 51. Flock A: Neurobiology of hair cells and their synapse , in Zwicker E, Terhardt E (eds): Facts and Models in Hearing . Berlin, Springer Verlag, 1974, pp 37-42. 52. Lowry BL, Godfrey DA, Carter JA, et al: Quantitative distribution of alleged transmitter amino acids in the cochlear nucleus . J Acoust Soc Am ( (Fall suppl) ):19, 1974. 53. Davis H, Fernandez C, McAudiffe DR: The excitatory process in the cochlea . Proc Natl Acad Sci USA 36:580-587, 1950.Crossref 54. Dallos P, Schoeny ZG, Cheatham MA: Cochlear summating potentials: Composition . Science 170:641-644, 1970.Crossref 55. Dallos P: Summating potentials in the cochlea , in Sachs MS (ed): Physiology of the Auditory System . Baltimore, National Education Consultants Inc, 1971, pp 57-67. 56. Dallos P, Cheatham MA: Generator potentials: Are they identifiable from gross cochlear recordings? J Acoust Soc Am ( (Fall suppl) ):10, 1974. 57. Stevens SS: On the psychophysical law . Psychol Rev 64:153-181, 1957.Crossref 58. Stevens SS: Neural events and the psychophysical law . Science 170:1043-1050, 1970.Crossref

Journal

Archives of OtolaryngologyAmerican Medical Association

Published: Sep 1, 1975

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