Cochlear Mechanisms: Structure, Function, and Models PDF
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Cochlear Mechanisms Structure, Function, and Models NAT O ASI Series Advanced Science Institutes Series A series presenting the results of activities sponsored by the NA-TO Science Committee, which aims at the dissemination of advanced scientific and technological knowledge, with a view to strengthening links between' scientific communities. The series is published by an international board of publishers in conjunction with the NATO Scientific Affairs Division A Life Sciences Plenum Publishing Corporation B Physics New York and London C Mathematical Kluwer Academic Publishers and Physical Sciences Dordrecht, Boston, and London o Behavioral and Social Sciences E Applied Sciences F Computer and Systems Sciences Springer-Verlag G Ecological Sciences Bertin, Heidelberg, New York, London, H Cell Biology Paris, and Tokyo Recent Volumes in this Series Volume 158-Biocompatibility of Co-Cr-Ni Alloys edited by Hartmut F. Hildebrand and Maxime Champy Volume 159-Biologically Based Methods for Cancer Risk Assessment edited by Curtis C. Travis Volume 160-Early Influences Shaping the Individual edited by Spyros Doxiadis Volume 161-Research in Congenital Hypothyroidism edited by F. Delange, D. A. Fisher, and D. Glinoer Volume 162-Nematode Identification and Expert System Technology edited by Renaud Fortuner Volume 163-Leishmaniasis: The Current Status and New Strategies for Control edited by D. T. Hart Volume 164-Cochlear Mechanisms: Structure, Function, and Models edited by J. P. Wilson and D. T. Kemp Series A: Life Sciences Cochlear Mechanisms Structure, Function, and Models Edited by J. P. Wilson University of Keele Keele, Staffordshire, United Kingdom and D. T. Kemp Institute of Otology and Laryngology London, United Kingdom Plenum Press New York and London Published in cooperation with NATO Scientific Affairs Division Proceedings of a NATO Advanced Research Workshop on Mechanics of Hearing, held July 3-8, 1988, at the University of Keele, Keele, Staffordshire, United Kingdom ISBN 978-1-4684-5642-4 ISBN 978-1-4684-5640-0 (eBook) 001 10.1007/978-1-4684-5640-0 Library of Congress Cataloging in Publication Data NATO Advanced Research Workshop on Mechanics of Hearing (1988: University of Keele) Cochlear mechanisms: structure, function, and models I edited by J. P. Wilson and D. T. Kemp. p. cm.-(NATO ASI series. Series A, Life sciences; v. 164) "Proceedings of a NATO Advanced Research Workshop on Mechanics of Hearing held July 3-8, 1988 at the University of Keele, Keele, Staffordshire, United Kingdom"-T.p. verso. "Published in cooperation with NATO Scientific Affairs Division." Includes bibliographies and indexes. ISBN 978-1-4684-5642-4 1. Cochlea-Congresses. 2. Hearing-Congresses. I. Wilson, John Patrick, 1935-. . II. Kemp, D. T. III. North Atlantic Treaty Organization. Scientific Af- fairs Division. IV. Title. V. Series. [DNLM: 1. Cochlea-congresses. WV 250 N279c 1988] QP461.N37 1988 599'.01825-dc19 DNLM/DLC 89-3760 for Library of Congress CIP © 1989 Plenum Press, New York Softcover reprint of the hardcover 1s t edition 1989 A Division of Plenum Publishing Corporation 233 Spring Street, New York, N.Y. 10013 All rights reserved No part of this book may be reproduced, stored in a retrieval system, or transmitted in any form or by any means, electronic, mechanical, photocopying, microfilming, recording, or otherwise, without written permission from the Publisher INTERNATIONAL ORGANIZING COMMITTEE E. de Boer, Amsterdam, The Netherlands P. Dallos, Evanston, Illinois, USA A. J. Hudspeth, San Francisco, California, USA D. T. Kemp, London, United Kingdom J. P. Wilson, Keele, Staffordshire, United Kingdom E. de Boer, D.T. Kemp and J.P. Wilson PREFACE Great advances have been made in understanding hearing in recent years. In particular, the mechanical function of the cochlea has become the focus of intense interest. This started in one direction, with the discovery of otoacoustic emissions in 1978, which required active mechanical amplification processes, as first postulated by Gold in 1948. Direct evidence for the role of this mechanism in sharpening-up the otherwise poor, basilar membrane tuning properties, was provided in 1982; and in 1983, motility was shown in outer hair cells. In parallel, an immense amount of work has been done on the electrophysiology of hair cells, following the first intracellular recordings in 1977. Over a longer time scale, models of basilar membrane motion have been developed and refined, and recently much effort has been put into incorporating active mechanisms and non-linear processes. It seemed an opportune time to bring together the leading workers in these various areas, to take stock of the whole field and to stimulate further progress. This book represents the proceedings of a NATO ARW on the Mechanics of Hearing held at the University of Keele, 3-8 July, 1988. The conception of the meeting owes much to earlier meetings held in Boston in 1985 (Peripheral Auditory Mechallisms, Eds. J.B. Allen, J.L. Hall, A. Hubbard, S.T. Neely and A. Tubis, Springer-Verlag, Berlin, 1986) and Delft in 1983 (Mechanics of Hearing, Eds. E. de Boer and M.A. Viergever, Delft University Press, 1983) and also London in 1980 (Nonlinear and Active Mechanical Processes in the Cochlea, Eds. D.T. Kemp and S.D. Anderson, Hearing Research, 2 (3/4». In this meeting, however, we have departed from previous practice by omitting middle ear measurements. This was necessitated by the very rapid and exciting growth in the field of micro mechanics and hair cell motility. Furthermore, to broaden the understanding of this field, it appeared advantageous to introduce some of the recent ultrastructural findings. The editors received much encouraging feedback during the meeting, both from modellers and morphologists, that this had been a popular and fruitful decision. In addition to the main papers we have included extra material as "comments", either sent in beforehand, presented as posters, or written up during the meeting. The edited discussions are also included, and, in a much less heavily edited form, the two main discussion sessions, which by default, have not necessarily been approved by the authors concerned. We were fortunate in having so many of the pioneer workers in this field, present at the workshop, and in addition, two eminent scientists from other fields, who had interesting contributions to make. Professor Thomas Gold, FRS, the cosmologist and astronomer, had made predictions about active feedback mechanisms within the cochlea, forty years ago, and it was intriguing to hear about auditory resear:ch of that era, and to wonder how different the development of hearing might have been if his vii viii Preface attempts at that time, to measure spontaneous otoacoustic emissions, had been successful; and Sir James Lighthill, FRS, who was able to relate, as guest of honour at the dinner, some of the background to the earlier meetings, particularly that at Delft for which he was on the organising committee. As chairman of the modelling discussion session, he showed how his expertise in fluid dynamics can be applied to energy flow problems within the cochlea. The editors would like to thank the members of the International Organising Committee for many useful suggestions which have helped shape the meeting, the Chairmen of Sessions, and the members of the Local Organising Committee who contributed so much to the smooth running of the meeting. These are all named following the list ,of participants. We would also like to thank NATO for so generously supporting the workshop in administrative costs, and in providing accommodation and travel support for participants who needed it. Plans were made at the end, to hold another workshop in 1990, probably in the US Mid West. J.P. Wilson and D.T. Kemp October, 1988 CONTENTS 1. Hair Cell Ultrastructure ........................................... . Structural organization of the mammalian auditory hair cells in relation to micromechanics . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3 D. J. Lim, Y. Hanamure, and Y. Ohashi Observations on the cytoskeleton and related structures of mammalian cochlear hair cells. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 11 C. M. Hackney and D. N. Furness A comparative study of actin filaments in cochlear hair cells: outer hair cells in the apex of the guinea pig cochlea contain a unique ultrastructural feature. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 21 L. Carlisle, P. R. Thorne, G. Zajic, R. A. Altschuler, and J. Schacht The lateral walls of inner and outer hair cells 29 A. Forge Tip-link organization in relation to the structure and orientation of stereo villar bundles. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 37 J. O. Pickles, M. P. Osborne, S. D. Com is, C. Koppl, O. Gleich, J. Brix, andG. A. Manley 2. Micromechanical measurements and models 45 Hair cell mechanics controls the dynamic behaviour of the lateral line cupula...... ..... ... .... . ... ... . . ... . ......... .... . . . . . . . . .. 47 S. M. van Netten and A. B. A. Kroese Aminoglycoside antibiotics and lectins cause irreversible increases in the stiffness of cochlear hair-cell stereocilia. . . . . . . . . . . . . . . . . . . . . . . .. 57 G. P. Richardson, I. J. Russell, R. Wasserkort, and M. Hans Mechanical analysis of hair cell microstructure and motility. . . . . . . . . . . . . .. 67 C. R. Steele, .C. R. Steele and D. H. Jen A model for bidirectional transduction in outer hair cells. . . . . . . . . . . . . . . .. 75 S. T. Neely A three-degree-of-freedom active micro mechanical model of the cochlear partition . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 83 K. L. Jones and D. O. Kim Outer hair cells possess acetylcholine receptors and produce motile responses in the organ of Corti ........................................ 93 H. P. Zenner, G. Reuter, P. K. Plinkert, U. Zimmermann, and A. Gitter ix x Contents Mechano-electrical transduction in turtle hafr cells . . . . . . . . . . . . . . . . . . . . . .. 99 R. Fettiplace and A. C. Crawford Transducer motor coupling in cochlear outer hair cells ............ . . . . . .. 107 J. F. Ashmore, Structure of the cortical cytoskeleton in outer hair cells from the guinea pig organ of corti. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 115 M. C. Hol/ey and J. F. Ashmore Gating compliance, a reduction in hair-bundle stiffness associated with the gating of transduction channels in hair cells from the bullfrog's sacculus ........................................... 117 A. J. Hudspeth, W. M. Roberts, and J. Howard Simultaneous recording of fluctuations of hair-bundle defection and intracellular voltage in saccular hair cells ....................... 125 W. Denk and W. W. Webb Micromechanical movements of chick sensory hair bundles to sinusoidal stimuli. . . . . . . . . . . . . . . .• . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 135 J. C. Saunders and Y. M. Szymko Micromechanical basis of high-frequency tuning in the bobtail lizard. . . . . .. 143 G. A. Manley, C. Koppl, and G. K. Yates Mechanical coupling between inner and outer hair cells in the mammalian cochlea . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 153 D. C. Mountain and A. R. Cody 3. Electrophysiological Measurements .................................. 161 Phase reversal of ohc response at high sound intensities . . . . . . . . . . . . . . . . .. 163 J. J. Zwislocki and R. L. Smith Outer hair cell receptor current and its effect on cochlear mechanics. . . . . .. 169 R. B. Patuzzi, G. K. Yates, and B. M. Johnstone Saturation of receptor currents accounts for two-tone suppression . . . . . . . .. 177 G. K. Yates, C. D. Geisler, R. B. Patuzzi, and B. M. Johnstone Components of the membrane current in guinea pig inner hair cells. . . . . . .. 189 C. J. Kros and A. C. Crawford Cochlear nonlinearities reflected in inner hair cell responses ............. " 197 P. Dal/os and M. A. Cheetham Asymmetries in motile responses of outer hair cells in simulated in vivo conditions ................................................. " 205 B. N. Evans, P. Dal/os, and R. Hal/worth Round window cochlear microphonic and atrophy of short and middle stereocilia on outer hair cells in hydropic cochleas in guinea pigs 207 K. C. Horner, Y. Cazals, and A. Guilhaume Postnatal developement of the cochlea in horseshoe bats 217 M. Vater and R. Riibsamen On the origin of interspecific differences in auditory susceptibility . . . . . . . .. 225 L. Decory, A. Guilhaume, A. Dancer, and J.-M. Aran
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