SPRINGER HANDBOOK OF AUDITORY RESEARCH. Series Editors: Richard R. Fay and Arthur N. Popper. Springer Science+ Business Media, LLC

Transcription

1 SPRINGER HANDBOOK OF AUDITORY RESEARCH Series Editors: Richard R. Fay and Arthur N. Popper Springer Science+ Business Media, LLC

2 SPRINGER HANDBOOK OF AUDITORY RESEARCH Volume I: The Mammalian Auditory Pathway: Neuroanatomy Edited by Douglas B. Webster, Arthur N. Popper, and Richard R. Fay Volume 2: The Mammalian Auditory Pathway: Neurophysiology Edited by Arthur N. Popper and Richard R. Fay Volume 3: Human Psychophysics Edited by William Yost, Arthur N. Popper, and Richard R. Fay Volume 4: Comparative Hearing: Mammals Edited by Richard R. Fay and Arthur N. Popper Volume 5: Hearing by Bats Edited by Arthur N. Popper and Richard R. Fay Volume 6: Auditory Computation Edited by Harold L. Hawkins, Teresa A. McMullen, Arthur N. Popper, and Richard R. Fay Volume 7: Clinical Aspects of Hearing Edited by Thomas R. Van De Water, Arthur N. Popper, and Richard R. Fay Volume 8: The Cochlea Edited by Peter Dallos, Arthur N. Popper, and Richard R. Fay Volume 9: Development of the Auditory System Edited by Edwin WRubel, Arthur N. Popper, and Richard R. Fay Volume 10: Comparative Hearing: Insects Edited by Ronald Hoy, Arthur N. Popper, and Richard R. Fay Volume II: Comparative Hearing: Fish and Amphibians Edited by Richard R. Fay and Arthur N. Popper Volume 12: Hearing by Whales and Dolphins Edited by Whitlow W.L. Au, Arthur N. Popper, and Richard R. Fay Volume 13: Comparative Hearing: Birds and Reptiles Edited by Robert Dooling, Arthur N. Popper, and Richard R. Fay Volume 14: Genetics and Auditory Disorders Edited by Bronya J.B. Keats, Arthur N. Popper, and Richard R. Fay Volume 15: Integrative Functions in the Mammalian Auditory Pathway Edited by Donata Oertel, Richard R. Fay, and Arthur N. Popper Volume 16: Acoustic Communication Edited by Andrea Simmons, Arthur N. Popper, and Richard R. Fay Volume 17: Compression: From Cochlea to Cochlear Implants Edited by Sid P. Bacon, Richard R. Fay, and Arthur N. Popper Volume 18: Speech Processing in the Auditory System Edited by Steven Greenberg, William Ainsworth, Arthur N. Popper, and Richard R. Fay Volume 19: The Vestibular System Edited by Stephen M. Highstein, Richard R. Fay, and Arthur N. Popper Volume 20: Cochlear Implants: Auditory Prostheses and Electric Hearing Edited by Fan-Gang Zeng, Arthur N. Popper, and Richard R. Fay Volume 21 : Plasticity of the Auditory System Edited by Thomas N. Parks, Edwin W Rubel, and Richard N. Popper Continued after index

3 Geoffrey A. Manley Arthur N. Popper Richard R. Fay Editors Evolution of the Vertebrate Auditory System With 101 illustrations, Springer

4 Geoffrey A. Manley Lehrstuhl flir Zoologie Technische Universitaet Muenchen Garching, Gennany Arthur N. Popper Department of Biology University of Maryland College Park, MD , USA Richard R. Fay Department of Psychology and Parmly Hearing Institute Loyola University of Chicago Chicago, IL 60626, USA Series Editors: Richard R. Fay and Arthur N. Popper Cover illustration: Modified after Manley 2000c (see Chapter I, Fig. 5), 2000 Wiley-VCH Verlag GmbH and used with permission. ISBN ISBN (ebook) DOI / Printed on acid-free paper Springer Science+Business Media New York Originally published by Springer-Verlag New York in 2004 Softcover reprint of the hardcover I st edition 2004 All rights reserved. This work may not be translated or copied in whole or in part without the wrirten permission of the publisher Springer Science+Business Media, LLC except for brief excerpts in connection with reviews or scholarly analysis. Use in connection with any form of information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter developed is forbidden. The use in this publication of trade names, trademarks, service marks, and similar tenns, even if they are not identified as such, is not to be taken as an expression of opinion as to whether or not they are subject to proprietary rights SPIN (HA) SPIN (SA) springeronline.com

5 This book is dedicated to our families. GM: Many thanks to Christine for putting up with all the work involved in preparing this book for publication. ANP: This volume is dedicated to the ladies in my life-my wife Helen, my daughters Michelle and Melissa, and my late mother Evelyn. Helen and our girls have provided infinite love, support, guidance, tolerance, and understanding during my career. My mother, a consummate teacher, was the ultimate role model for an aspiring professor. RRF: I dedicate this volume to my wife Catherine who has imagined and made possible our life, and the lives of our two children, Christian and Amanda, in spite of my academic career.

6 Series Preface The Springer Handbook of Auditory Research presents a series of comprehensive and synthetic reviews of the fundamental topics in modem auditory research. The volumes are aimed at all individuals with interests in hearing research including advanced graduate students, postdoctoral researchers, and clinical investigators. The volumes are intended to introduce new investigators to important aspects of hearing science and to help established investigators to better understand the fundamental theories and data in fields of hearing that they may not normally follow closely. Each volume presents a particular topic comprehensively, and each serves as a synthetic overview and guide to the literature. As such, the chapters present neither exhaustive data reviews nor original research that has not yet appeared in peer-reviewed journals. The volumes focus on topics that have developed a solid data and conceptual foundation rather than on those for which a literature is only beginning to develop. New research areas will be covered on a timely basis in the series as they begin to mature. Each volume in the series consists of a few substantial chapters on a particular topic. In some cases, the topics will be ones of traditional interest for which there is a substantial body of data and theory, such as auditory neuroanatomy (Vol. 1) and neurophysiology (Vol. 2). Other volumes in the series deal with topics that have begun to mature more recently, such as development, plasticity, and computational models of neural processing. In many cases, the series editors are joined by a co-editor having special expertise in the topic of the volume. RICHARD R. FAY, Chicago, Illinois ARTHUR N. POPPER, College Park, Maryland Vll

7 Volume Preface One of the defining characteristics of vertebrate organisms is that they carry three paired, major sense organs in the head, the nasal epithelia, the eyes, and the ears. These sense organs of the head region are protected by being partially or almost completely enclosed within elements of the skull. This enclosure means that even in fossil vertebrates, some information concerning the size and structure of the major sense organs can be obtained, even though soft tissues are very rarely preserved during fossilization. During the evolution of vertebrates, these sense organs underwent changes associated with changes in lifestyle (for example, the transition from water to land living) but also with developments that led to improvements in the performance of the organs as interfaces to the outside world. This book is concerned with the evolution of one of these organs, the ear, and, to a lesser extent, the brain pathways associated with the processing of the auditory information supplied by the ears. In Chapter I, Manley and Clack provide a framework for understanding the evolutionary relationships between the various lineages of vertebrates, without which it is impossible to understand the changes that have occurred over evolutionary time. In spite of current disagreements regarding the exact status and relationships and even the nomenclature of some vertebrate groups, this systematic framework is adhered to throughout the book, to avoid confusion. Manley and Clack also provide an overview of the subsequent chapters, to help the reader better integrate the information provided for each of the major groups of vertebrates. Here, the emphasis is on the amniotes, the reptiles, birds, and mammals, since these lineages show not only the greatest variety of structural arrangements but also the largest and most complex inner ears. When biologists speak of the "design" of a structure in an organism, they are referring to the result of selection pressures, sometimes over very long periods of time, that have shaped the morphology and the function of that structure. These selection pressures are, in the special case of sense organs, hugely influenced by the physical and chemical nature of the stimuli to be perceived. In the present case, the stimuli are sound-pressure waves in the media water and! or air. As is generally the case for sensory organs, selection pressures existed for attaining very high sensitivities, in other words for the detection of extremely IX

8 x 'Volume Preface small signal strengths even in the presence of noise and competing signals from various sources. In Chapter 2, Lewis and Fay discuss some of the important ecological and physical factors that would have been omnipresent throughout the history of vertebrate evolution and must have had an impact on the evolution of vertebrate hearing. They conclude that in addition to having acoustic transducers, the sine qua non for any auditory system to function in such a world is the ability to isolate signals from their individual sources. Furthermore, this quintessential task must be achieved largely by neural computation, and this requirement establishes essential constraints on the acoustic transducers, on the signalprocessing structures associated with them, and on the brain itself. In the appendix at the end of the book, Lewis provides a physical-mathematical framework for understanding the nature of the stimulus and the resulting constraints that operated during ear evolution. These constraints were responsible for molding the form and function of vertebrate inner ears to those we see today. The sensory cells that sub serve the function of hearing are among the oldest of cell types, with possible forerunners among chordate ancestors and perhaps even other invertebrate organisms. Thus "hair" cells not only are found in the inner ear, but also are the typical sensory cell of fish and amphibian lateral-line organs. In fact, they are the primary sensory cells used by vertebrates for the detection of mechanical signals from external sources. Since mechanoreceptive organs can have their stimuli filtered by accessory structures and be required to provide information on different aspects of the stimuli (acceleration, velocity, displacement), it is not surprising to find that selection pressures have greatly influenced the characteristics of such accessory structures. In parallel, however, we find modifications to hair cell structure and function that are large enough to justify the recognition of different types of hair cells. In Chapter 3, Coffin et al. describe the variety of hair cell types in different vertebrates and provide us with a framework for classifying them and understanding the functional background for hair cell specialization. It is clear that the sense of hearing in vertebrates arose well before the origin of sensory organs especially dedicated to that sense. In fact, the rich acoustic world of fishes is testimony to the fact that fishes, which form by far the largest group among vertebrates (more than 50% of species), have created a very useful hearing system by utilizing preexisting sensory epithelia of the vestibular part of the inner ear. Since these animals not only live in water but also have a body largely made up of water, acoustic signals from the environment have no difficulty in penetrating their tissues and are thus not attenuated at the water-to-body interface. The only requirement for them to be able to detect acoustic stimuli is that relative motion at the sensory epithelium be produced, and this is only possible at an impedance transition such as from water to a dense inner-ear otolith or at the boundary between tissue and the fish's air bladder. It is thus evident that in fishes, sound detection is based on the use of sensory epithelia that are also used to detect linear acceleration, and there must be some kind of compromise in the organs' sensitivities to these different stimuli. In Chapter 4,

9 Volume Preface xi Ladich and Popper describe how fishes achieved this compromise, which organs are involved, and the constraints imposed by the requirement to retain vestibular responses. Together with comparative studies of form and function in a variety of modem vertebrate groups, the study of fossil organisms is the most direct source of information as to which changes occurred when over evolutionary time. The transition to land during the development of the first land vertebrates (the labyrinthodont amphibians) greatly changed the selection pressures that operated on the various major sense organs. The nasal epithelium was moistened and could continue to operate with few changes. The eye required little more than a change in the optical properties of the lens to accommodate the fact that the air-corneal interface provided much more refraction of light than a water-corneal interface. Similarly, the largest acoustic problem for the inner ear was to overcome the huge impedance mismatch between air and body tissues. Or at least, that was the thinking that influenced the interpretation of the fossil story for many years. In Chapter 5, Clack and Allin have gathered together a wealth of data from vertebrate fossils, providing a detailed interpretation as to what can be read out concerning the status of the inner ear and especially any special bony connections between it and the outside world. These authors indicate that tympanic middle ears as we know them were not characteristic of the earliest land vertebrates, but in fact arose quite late in their evolution, many millions of years after the origin of the amphibians. This implies not only that important initiating impulses were missing, but also that the early amphibians and, indeed, early reptiles were well served by the inner ear without a tympanic middle ear. Certainly the early land vertebrates had large heads, short necks, and short limbs, implying that in fact the head was in close or often direct contact with the ground and that sound and vibrational stimuli from the substrate thus had no problem influencing the inner ear. Clack and Allin demonstrate that tympanic middle ears have arisen a number of times independently in different lineages, a crucial finding that makes it possible to understand the great variety of inner-ear structures and the parallel developments that they show. Before tympanic middle ears arose, the land vertebrates had already diversified into a number of different lineages. Existing alongside the amphibians, several lineages had arisen from the stem reptiles, the lepidosaurs, the archosaurs, and the mammal-like reptiles that later gave rise to the mammals. The lack of a tympanic middle ear as we now know it probably meant that during those periods of time, selection pressures for the development of larger and more complex inner-ear hearing epithelia were missing or weak. It is apparent that, while the amniote descendants of the stem reptiles all inherited a rather simple hearing papilla largely supported by the basilar membrane, the ancestors of modem amphibians developed two separate epithelia. As Smotherman and Narins describe in Chapter 6, it is possible, perhaps even probable, that strictly speaking, neither of these epithelia is homologous with the basilar papilla of amniotes (in spite of one of them bearing the same name). Nonetheless, as

10 xii Volume Preface these authors also point out, all of these epithelia originate during ontogeny from one common epithelium with the vestibular sensory patches. The long history of the amphibians since the development of a tympanic middle ear was obviously accompanied by the evolution of different papillar specializations in different amphibian groups. In the anuran amphibians, these papillae are well enough developed, though small, to support sophisticated acoustic communication behaviors. In the lepidosaurs, especially the lizards, the hearing papilla remained relatively simple and evolution led only in one group-the geckos-to acoustic communication. In the apparent absence of strong selection pressures for the maintenance of a particular size and development of the inner-ear hearing epithelium, the various lineages of the lizards demonstrate a remarkable degree of structural variety. In Chapter 7, Manley describes the lizard hearing organ and shows that in spite of this great structural variety, the function of the ear as seen at the level of the auditory nerve is much less variable. This can be attributed to a situation of neutral evolution, where in the absence of strong selection pressures, structural configurations can drift, provided that a basic degree of functional integrity is maintained. The huge variety of structural configurations seen in the lizard basilar papilla are thus not accompanied by any documented differences in behavior. Nonetheless, the structural variety does result in some functional differences that provide a window into the ear, helping to understand the function of variable components such as that of the enigmatic tectorial membrane. Those who know the structure of the archosaur (birds and Crocodilia) inner ears will not find it surprising that crocodiles and their relatives are the closest living relatives of the birds. These organisms elongated and elaborated on the ancestral stem-reptile inner ear and have large numbers of hair cells in their auditory epithelia. These have been strongly specialized into two groups, where the extreme forms differ greatly in morphology and innervation pattern. As Gleich et al. describe in Chapter 8, these specializations parallel to a remarkable degree those observed in mammalian inner ears. This suggests that in this lineage, and completely independently from the mammals, two hair cell populations that are placed neurally and abneurally on the papilla developed that are, respectively, specialized for signal detection and for signal amplification. There is no doubt that this specialization is responsible for the exquisite hearing ability of these animals and for their extensive use of acoustic signals in behavior. The treatment of the mammals has been placed at the end of the animal-group series only out of tradition. It should not be assumed that this is a series of continuously increasing quality of hearing. Indeed, in some respects, as for example in frequency selectivity, the mammalian ear has a poorer performance than many nonmammalian ears. What sets mammalian ears apart is something different. During the evolution of mammals, but of no other group, the independent development of a tympanic middle ear occurred at the same time as the improvement of the jaw joints. Mammals have a secondary jaw joint. This fortuitous coincidence meant that the mammals were able to incorporate redun-

11 Volume Preface xiii dant jaw-joint bones into their middle-ear ossicular chain. Much later in evolution, when mammals were able to move toward acquiring the ability to perceive higher frequencies of sounds (above, say, 10 khz), it turned out that, quite unplanned, as it were, this kind of middle ear was much better at transmitting high frequencies than was the second-order lever system used by all the nonmammalian groups. Thus one of the features characterizing the mammalian hearing organ-the perception of very high frequencies-was not primarily a result of any specialization of the hearing epithelium, but a result of the firstorder lever system of the middle ear. Hair cell specializations, such as specialized active processes, almost certainly developed later, together with a sometimes dramatic papillar elongation. As noted above, the mammalian inner ear shows hair cell specializations that are in parallel to those of birds. In mammals, the huge amount of data available on structure and function make it clear that the inner hair cells on the neural side of the papilla or organ of Corti are the signal detectors, and the outer hair cells are the signal manipulators and amplifiers. The evolutionary story behind the ears of the various mammals, some highly specialized, is told by Vater et al. in Chapter 9. Most of the information transduced by the inner ear is transformed into neural signals that travel along afferent nerve fibers to the first neural processing station in the brain stem, the cochlear nucleus. From this nuclear complex, the neural information is passed to higher and higher centers of the auditory pathway that are often specialized to process certain aspects of the sound stimulus. During vertebrate evolution, the brain enlarged, often to a very great extent and independently in different lineages. During this enlargement, however, the basic structure of the auditory pathway remained very similar and recognizable in all lineages while specific neural centers sometimes became very large. Groupspecific differences are seen, and differences in the pattern of the processing of neural information are sometimes quite large even within one group of vertebrates. In Chapter 10, Grothe et al. present an overview of the evolution of this pathway in the brain and examine the question as to whether we can detect clear evolutionary trends in the organization and function of the afferent auditory pathway. Thanks to a huge research effort over the last 50 years or so, we are now in a position to much better understand what happened to middle- and inner-ear structure during evolutionary processes that lasted more than 400 million years. This book attempts to organize these facts into a coherent pattern and make this area of scientific knowledge accessible to those who are interested. As Manley outlines in the summary in Chapter 11, we have made huge strides in integrating large amounts of data. Nonetheless, many exciting questions, some of them very fundamental to understanding the hearing processes, are still open for the devoted investigator. The editors hope that this book will be an inspiration for young colleagues to tackle these problems in the near future. As with most other volumes in the Springer Handbook of Auditory Research (SHAR) series, the readers of many chapters in this volume will benefit from reading chapters in earlier volumes. Thus, sensory hair cells were also discussed

12 xiv "olurne Preface in several chapters in The Cochlea (volume 8) and chapters by Hoy and others in Comparative Hearing: Insects (volume 10). Hearing by fishes and amphibians was discussed in detail in volume 11 (Comparative Hearing: Fish and Amphibians), while hearing in reptiles and birds was the topic of Comparative Hearing: Birds and Reptiles (volume 13). Mammalian hearing has been the subject of chapters in many volumes in the SHAR series, but most notably, for the context of the current volume, in Comparative Hearing in Mammals (volume 4) and Hearing by Bats (volume 5). Finally, the structure and function of the central nervous system was first dealt with in volume 1 of this series, The Mammalian Auditory Pathway: Neuroanatomy, and volume 2, The Mammalian Auditory Pathway: Neurophysiology, and in the more recent overview in volume 15, Integrative Functions in the Mammalian Auditory Pathway. September, 2003 GEOFFREY A. MANLEY, Garching, Germany ARTHUR N. POPPER, College Park, Maryland RICHARD R. FAY, Chicago, Illinois

13 Contents Series Preface Volume Preface Contributors vii ix xvii Chapter 1 Chapter 2 An Outline of the Evolution of Vertebrate Hearing Organs.... GEOFFREY A. MANLEY AND JENNIFER A. CLACK Environmental Variables and the Fundamental Nature of Hearing EDWIN R. LEWIS AND RICHARD R. FAY Chapter 3 Evolution of Sensory Hair Cells ALLISON COFFIN, MATTHEW KELLEY, GEOFFREY A. MANLEY, AND ARTHUR N. POPPER Chapter 4 Parallel Evolution in Fish Hearing Organs FRIEDRICH LADICH AND ARTHUR N. POPPER Chapter 5 The Evolution of Single- and Multiple-Ossicle Ears in Fishes and Tetrapods JENNIFER A. CLACK AND EDGAR ALLIN Chapter 6 Evolution of the Amphibian Ear MICHAEL SMOTHERMAN AND PETER NARINS Chapter 7 The Lizard Basilar Papilla and Its Evolution GEOFFREY A. MANLEY Chapter 8 Hearing Organ Evolution and Specialization: Archosaurs OTTO GLEICH, FRANZ PETER FISCHER, CHRISTINE KOPPL, AND GEOFFREY A. MANLEY xv

14 XVl Contents Chapter 9 Chapter 10 Chapter 11 Hearing Organ Evolution and Specialization: Early and Later Mammals MARIANNE VATER, JIN MENG, AND RICHARD C. Fox The Evolution of Central Pathways and Their Neural Processing Patterns BENEDIKT GROTHE, CATHERINE E. CARR, JOHN H. CASSEDAY, BERND FRITZSCH, AND CHRISTINE KOPPL Advances and Perspectives in the Study of the Evolution of the Vertebrate Auditory System GEOFFREY A. MANLEY Appendix: Useful Concepts from Circuit Theory EDWIN R. LEWIS Index

15 Contributors EDGAR ALLIN Chicago College of Osteopathic Medicine, Midwestern University, Downers Grove, IL 60515, USA CATHERINE E. CARR Department of Biology, University of Maryland, College Park, MD 20742, USA JOHN H. CASSEDA Y Department of Psychology, University of Washington, Seattle, WA 98195, USA JENNIFER A. CLACK University Museum of Zoology, Cambridge, CB2 3EJ, England ALLISON COFFIN Department of Biology, University of Maryland, College Park, MD 20742, USA RICHARD R. FAY Department of Psychology and Parmly Hearing Institute, Loyola University of Chicago, Chicago, IL 60626, USA FRANZ PETER FISCHER Lehrstuhl fur Zoologie, Technische Universitaet Muenchen, Garching, Germany RICHARD C. FOX Laboratory for Vertebrate Paleontology, Department of Biological Sciences, University of Alberta, Edmonton, Alberta T6G 2E9, Canada BERND FRITZSCH Creighton University, Department of Biomedical Sciences, Omaha, Nebraska 68178, USA xvii

16 XVlll Contributors OTTO GLEICH ENT-Department, Universitat Regensburg, Regensburg, Germany BENEDIKT GROTHE Max-Planck-Institut fur Neurobiologie, D Martinsried, Germany MATTHEW KELLEY National Institute on Deafness and Other Communication Disorders, National Institutes of Health, Rockville, MD, 20850, USA CHRISTINE KOPPL Lehrstuhl fur Zoologie, Technische Universitaet Muenchen, Garching, Germany FRIEDRICH LADICH Institute of Zoology, University of Vienna, A-1090 Vienna, Austria EDWIN R. LEWIS Department of Electrical Engineering and Computer Science, University of California-Berkeley, Berkeley, CA 94720, USA GEOFFREY A. MANLEY Lehrstuhl fur Zoologie, Technische Universitaet Muenchen, Garching, Germany JlN MENG Division of Paleontology, American Museum of Natural History, New York, NY 10024, USA PETER NARINS Department of Physiological Science, University of California-Los Angeles, Los Angeles, CA 90095, USA ARTHUR N. POPPER Department of Biology and Neuroscience and Cognitive Science Program, University of Maryland, College Park, MD 20742, USA MICHAEL SMOTHERMAN Department of Physiological Science, University of California-Los Angeles, Los Angeles, CA 90095, USA MARIANNE V A TER Department of Biochemistry and Biology, University of Potsdam, Potsdam, Germany