Handbook of Sensory Physiology VolumeV/l Editorial Board H.Autrum R.Jung W.R. Loewenstein D.M.MacKay H.L.Teuber A uditory System Anatomy Physiology (Ear) By H.W.Ades A.Axelsson I.L.Baird G.v.Bekesy R.L.Boord C. B. G. Campbell O. Densert D. H. Eldredge H. Engstrom J.Fex J.M.Harrison O.W.Henson M.E.Howe S.Iurato A. Michelsen A. R. M011er R. R. Pfeiffer S. and I. Rauch E.A.G.Shaw J.Wersiill E.G. Wever Edited by Wolf D. Keidel and William D. Neff With 305 Figures Springer-Verlag Berlin Heidelberg New York 1974 Wolf D. Keidel I. Physiologisches Institut der Universitat 852 Erlangen, UniversitatsstraJ3e 17 (Germany) William D. Neff Indiana University, Center of Neural Sciences Psychology Building 320, Bloomington, Indiana 47401 (USA) ISBN-13: 978-3-642-65831-0 e-ISBN -13: 978-3-642-65829-7 DOl: 10.1007/978-3-642-65829-7 This work is subject to copyright. All rights are reserved, whether the whole or part of the material is concerned, specifically those of translation, reprinting, re-use of illustrations, broadcasting, reproduction by photocopying machine or similar means, and storage in data banks. Under § 54 of the German Copyright Law where copies are made for other than private use, a fee is payable to the publisher, the amount of the fee to be determined by agreement with the publisher. © by Springer-Verlag, Berlin' Heidelberg 1974. Library of Congress Catalog Card Number 74-415_ The use of general descriptive names, trade names, trade marks, etc. in this publication, even if the former are not especially identified, is not to be taken as a sign that such names, as under stood by the Trade Marks and Merchandise Marks Act, may accordingly be used freely by anyone. Typesetting, Softcover reprint of the hardcover 1s t edition 1974 Preface In planning The Handbook volumes on Audition, we, the editors, made the decision that there should be many authors, each writing about the work in the field that he knew best through his own research, rather than a few authors who would review areas of research with which they lacked first hand familiarity. For the purposes of the chapters on Audition, sensory physiology has been defined very broadly to include studies from the many disciplines that contribute to our understanding of the structures concerned with hearing and the processes that take place in these structures in man and in lower animals. A number of chapters on special topics have been included in order to present information that might not be covered by the usual chapters dealing with anatomical, physi ological and behavioral aspects of hearing. We wish to thank all authors of the volumes on Audition for the contributions that they have made. We feel confident that their efforts will also be appreciated by the many scientists and clinicians who will make use of the Handbook for many years to come. WOLF D. KEIDEL WILLIAM D. NEFF Erlangen Bloomington August 1974 Contents Chapter 1 Introduction. By G. v. BEKESY t. With 3 Figures. . . . . . . . 1 Chapter 2 Consideration of the Acoustic Stimulus. By R. R. PFEIFFER. With 19 Figures. . . . . . . . . . . . . . . . . . . . . . . . . 9 Chapter 3 Comparative Anatomy of the Middle Ear. By O. W. HENSON Jr. With 23 Figures. . . . . . . . . . . . . . . . . . . . . . . . . . . . 39 Chapter 4 The Morphology of the Middle Ear Muscles in Mammals. By O. DENSERT and J. WERSALL. With 12 Figures ................. 111 Chapter 5 Anatomy of the Inner Ear. By H. W. ADES and H. ENGSTROM. With 26 Figures. . . . . . . . . . . . . . . . . . . . . . . . . . . . 125 Chapter 6 Anatomical Features of the Inner Ear in Submammalian Vertebrates. By 1. L. BAffiD. With 18 Figures . . . . . . . . . . . . . . . . . . 159 Chapter 7 The Blood Supply of the Inner Ear of Mammals. By A. AXELSSON. With 36 Figures. . . . . . . . . . . . . . . . . . . . . . . . . 213 Chapter 8 Efferent Innervation ofthe Cochlea. By S. IURATO. With 11 Figures 261 Chapter 9 Anatomy of the Afferent Auditory Nervous System of Mammals. By J. M. HARRISON and M. E. HOWE. With 25 Figures . . . . . . . . . . . . . 283 Chapter 10 Central Auditory Pathways of Nonmammalian Vertebrates. By C. B. G. CAMPBELL and R. L. BOORD. With 4 Figures. . . . . . . . . . . . . 337 Chapter 11 Anatomy of the Descending Auditory System (Mammalian). By J. M. HARRISON and M. E. HOWE. With 10 Figures. . . . . . . . 363 Chapter 12 Hearing in Invertebrates. By A. MICHELSEN. With 18 Figures 389 Chapter 13 The Evolution of Vertebrate Hearing. By E. G. WEVER. With 14 Figures 423 Chapter 14 The External Ear. By E. A. G. SHAW. With 22 Figures . . . . 455 Chapter 15 Function of the Middle Ear. By A. R. MOLLER. With 19 Figures 491 Chapter 16 The Acoustic Middle Ear Muscle Reflex. By A. R. MOLLER. With 13 Figures 519 Chapter 17 Inner Ear - Cochlear Mechanics and Cochlear Potentials. By D. H. ELDREDGE. With 9 Figures . . . . . . . . . . . . . . . . . . . . 549 Chapter 18 Neural Excitatory Processes of the Inner Ear. By J. FEX. With 10 Figures 585 Chapter 19 Physico-Chemical Properties of the Inner Ear Especially Ionic Transport. By S. and 1. RAUCH. With 13 Figures. . . . . . . . . . . . . . . . 647 Author Index 683 Subject Index 708 List of Contributors ADES, Harlow W., Department of Electrical Engineering, Bioacoustics Research Laboratory, University of Illinois, Urbana, Illinois 61801, USA AXELSSON, Alf, University of Washington, Department of Otolaryngology, BB 1165 RL·30, Seattle, Washington 98195, USA BAIRD, Irwin, Department of Anatomy, The Milton S. Hershey Medical Center, Pennsylvania State University, Hershey, Pennsylvania 17033, USA t BEKEs¥, Georg von, Laboratory of Sensory Sciences, University of Hawaii, Honolulu, Hawaii 96822, USA BOORD, Robert, Department of Biological Sciences, University of Delaware, Newark, Delaware 19711, USA CAMPBELL, C. B. G., Department of Neurological Surgery, University of Virginia, Charlottes· ville, Virginia 22901, USA DENSERT, Ove, Department of Otolarynology, Karolinska Sjukhuset, S·10401 Stockholm 60, Sweden ELDREDGE, Donald H., Central Institute for the Deaf, 818 South Euclid, St. Louis, Missouri 63110, USA ENGSTROM, Hans, Department of Oto.Rhino-Laryngology, Uppsala University, University Hospital, S-75014 Uppsala, Sweden FEX, Jargen, Laboratory of Neuro-otolaryngology, National Institute of Neurological Diseases and Stroke, National Institutes of Health, Bethesda, Maryland 20014, USA HARRISON, J. M., Department of Psychology, Boston University, Boston, Massachusetts 02215, USA HENSON, Jr., Odell, W., The University of North Carolina at Chapel Hill, Division of Health Affairs, Department of Anatomy, 306 Mac Nider, Chapel Hill, North Carolina 27514, USA HOWE, M. E., New England Regional Primate Research Center, Harvard Medical School, Southborough, Massachusetts, USA IURATO, Salvatore, Cattedra di Bioacustica dell' Universita di Bari, Policlinico, 70124 Bari, Italia MICHELSEN, Axel, Institute of Biology, Odense Universitet, 5000 Odense, Denmark MOLLER, Aage R., Fysiologiska Institutionen II, Karolinska Institutet, 10401 Stockholm 60, Sweden PFEIFFER, Russel R., Department of Electrical Engineering and Physiology and Biophysics, The Washington University, St. Louis, Missouri 63130, USA RAUCH, S. and 1., 3011 Bern, ZeughausstraBe 20, Switzerland SHAW, Edgar A. G., Acoustic Section, Division of Physics, National Research Council Canada, Ottawa, Ontario KIA OR6, Canada WERSALL, Jan, Department of E. N. T., Huddinge sjukhus, 14186 Huddinge, Sweden WEVER, E. G., Auditory Research Laboratories, Princeton University, Princeton, New Jersey 08540, USA Chapter 1 Introduction GEORG VON BEKESY t, Honolulu, Hawaii (USA) With 3 Figures Contents Historical Background of Research in Hearing . . . 1 Impact of Physical and Telephone Engineering Concepts on Research in Hearing . 3 The Impact of Instrumentation on Hearing Research 5 The Data Explosion . 6 References . . . . . . . . . . . . . . . . . . . 7 Since scientific progress is not a continuous flow, the best time to write a handbook is when the number of findings reaches a maximum and the newer experiments show a certain redundancy. VON HELMHOLTZ'S (1863) book on hearing is a classical example of a book published at the right time. But so also is the handbook published by BETHE and BERGMANN (1928). Perhaps the publisher of these three volumes is correct in his judgment that we have reached such a maximum and tha,t now is the correct time to summarize the data. This is a brave enterprise of the publisher, the editors, and the authors; their efforts will be highly apprecia ted by the coming generation. The material in the two volumes on audition will form the platform from which new advances can be made, as was the case with the books of VON HELMHOLTZ and BETHE and BERGMANN. In engineering and the exact sciences, a new handbook would mean essentially the addition of some new facts to the already acquired ones. Unfortunately, this is not so in the field of hearing. Hearing research at the moment is a complicated interaction between physics, anatomy, physiology, and psychology. We cannot separate certain variables to the degree that is possible in physics. Furthermore, our measurements are not so precise, and the range of validity is not so well defined. Therefore, we often have to modify our earlier findings in light of the new, at least in the range of validity. In this way, a new handbook in the field of hearing is almost always a reevaluation of all the known facts. It is this balancing of one finding against another that makes modern handbook writing difficult. Historical Background of Research in Hearing The main basic problem in hearing today is almost exactly the same as it was a century ago. Perhaps it can be illustrated best by an experiment. If we have a 2 G. VON BEKESY: Introduction speaker in a normal living room and we listen to him monaurally or binaurally first from a distance of one meter and then from three meters, we notice hardly any difference except for a small drop in loudness at the greater distance. But if we have two identical microphones, one placed one meter away from the speaker and the second three meters away, then the recordings show two different sound pressure patterns over time as illustrated in Fig. 1. There is a small time delay for the lower trace which was recorded from the more distant microphone. It is difficult to understand how such different stimuli as the sound patterns in the upper and lower traces can produce the same sensations. Much research was done to find the reasons why this is possible. We inherited from the last century three basic experiments. One was done by SAVART (1840), one by OHM (1843; 1844), and one by SEEBECK (1841, 1843, 1844a, b). All three experiments were repeated over and over again and proved to be correct. In recent years, the validity range was also precisely determined. SAVART found that the pitch of a tone, with or without overtones, is determined with the precision of 10% in two cycles. Since resonators or small band pass filters have to accumulate energy to produce a frequency analysis, the ear cannot possibly consist of such frequency analyzers, since two cycles do not permit the necessary accumulation of energy. Therefore, the short onset and offset time of pitch discrimination of the ear contradicts the resonance theories of hearing. The above experiment is so simple that it did not become controversial and, therefore, it is seldom quoted. OHM introduced the FOURIER analysis into the field of hearing, showing that li>uch a complicated pressure pattern as speech can be represented as the sum of many sinusoidal tones. Since sinusoidal electric currents could be easily measured, OHM'S law became the basis of modern telecommunication planning. When com bined with the fact that phase differences between two tones cannot be detected Fig. 1. Section of,a recording of speech by two condenser microphones, one, I m away from the speaker (upper recording) and, another, 3 m away (lower recording); both of them in the median plane of the head and spoken toward the direction of the microphones. There is a small time delay between the two recordings as a result of the traveling time of the s01md waves; but, otherwise, they would be similar if there would be no sound reflections from the wall of the ordinary living room. The problem of hearing research is that listening monaurally or binau· rally to both sounds, which show such a strong difference in the oscillographic recording, we are unable to detect by hearing a difference except the change in loudness in agreement with the distance increase Impact of Physical and Telephone Engineering Concepts on Research in Hearing 3 with a single ear and, therefore, phase measurements can be omitted, OHM'S law made possible a quantitative description of communication systems. It was known, however, that OHM'S law is not valid in all situations. A FOURIER analysis of a complex tone overemphasizes the steady state and is of little use for transients. SEE:aECK found that for speech and for certain complex sounds which show a definite periodicity, the ear hears tones which do not show in the FOURIER analysis of these complex sounds. In other words, the ear does not do a long-term frequency analysis; its analysis is made in a few cycles. All three of these basic experiments indicate that oscillographic recordings, as shown in Fig. 1, are not good speech extractors. Impact of Physical and Telephone Engineering Concepts on Research in Hearing Assuming that, during the evolution of the animal kingdom, the most efficient system always survived, it seems probable that the laws of physics were followed to build up maximal efficiency. Therefore, we expect that the physical laws served as guidelines to the evolution of the structures and functions of the middle and inner ear. The sensitivity of the ear is so great that we know nature has outdone man in our attempts to build sound transmission systems based on these same physical laws. For example, to obtain maximum sensitivity in hearing, none of the sound energy hitting the eardrum should be reflected but should be transmitted in its full amount to the inner part of the ear, the cochlea. THEVENIN (1883) has shown that maximum sensitivity can be obtained by means of a mechanical trans former which provides a proper matching between the relatively soft air of the middle ear and the much harder fluid of the inner ear. THEVENIN'S theorem, which is so widely used by man in telephone engineering, also helps to explain the struc tures and functions that nature has provided for the middle ear. It is relatively easy to measure the electrical activity inside the cochlea and the energy of this activity for a given part of the cochlea. It turned out that the energy activity inside the cochlea produced by a tone is very much higher than the energy of the tone which is absorbed by the eardrum. Therefore, in the inner ear we do not have a passive system but something like an amplifier. ]'rom telephone engineer ing, it is known that it is of no use to amplify indefinitely because every amplifier also produces noise. This holds for the human ear where the cochlea has a blood supply with pulse waves resulting from the streaming of the fluid in the capillaries. One of the most important technical concepts, therefore, became the so-called signal-to-noise ratio. Nature applied this concept by reducing the sensitivity of the ear for the lower frequency range where noise is introduced by the circulatory system. One of the principles which had a tremendous impact on hearing research was the Fourier analysis. The Fourier analysis, as mentioned above, showed that any complex sound can 1:>e considered as a sum of sinusoidal sounds. Since the ear does perform to a certairi degree exactly that type of analysis, application of Fourier analysis became one of the most successful tools in hearing and speech research. Pitch discrimination seemed to be simply explained by assuming for every fre- 4 G. VON BEKESY: Introduction quency a certain resonator which produced sensations only in that frequency dominion. However, there were two difficulties. One was that no proper resonator could be found inside the cochlea. Most of the tissue in the cochlea is either too soft or too hard to function as a resonator. The other difficulty was that there is a well established law in telephone engineering that a filter with a given frequency band width needs given onset and offset times. This difficulty was already known a century ago, long before it was possible to formulate it mathematically. It is the short onset time of the perception of speech which makes it unlikely that resona tors inside the inner ear determine pitch perception. In this case, the application of Fourier analysis was not successful. But there are other principles, like the feedback principle in the auditory system, which are only beginning to be developed and which will contribute to the further understanding of cochlea activity. Pattern recognition similar to that found in vision certainly plays a great role in the field of hearing; but, it will take a long time before it can be evaluated. In vision, it is already clear that the visual sensations are produced mainly by edges in the brightness distribution and not by the brightness itself. The importance of similar phenomena in the auditory system is only beginning to be investigated. Compared with machines, one of the most surprising features of sense organs is the tremendous range of physical events to which a given sense organ is sensitive. , , , I 2 A 100 B I I 50 ", I ,,, I I " 50 I " I 40 I 40 " I I 30 " I I " I I ' Q) 20 I CQ ) 30 "" '' "uV0 I I I .uV.. I l," I .-~ 10 E o .£;. Q) .. : :.§ 20 0 5 01 J ..S! 4 / :3 10 2 2 3 4 5 10 :3 4 5 10 logarithmic scale logarithmic scale Fig. 2. A log-log scale representation of results invites extrapolation. In a linear log scale representation, the results shown by the solid line could hardly be extrapolated, as shown in the Drawing A. If we repeat the drawing again (the solid line showing the experimental data) on the log.log scale, it seems to extrapolate and make the assumptions that this extrapolation is significant