The Evolutionary Biology of Hearing Douglas B. Webster Richard R. Fay Arthur N. Popper Editors

The Evolutionary Biology of Hearing

With 355 Illustrations, 2 in Full Color

Springer-Verlag New York Berlin Heidelberg London Paris Tokyo Hong Kong Barcelona Budapest Douglas B. Webster Richard R. Fay Department of Otorhinolaryngology Parm1y Hearing Institute Louisiana State University Medical Center and New Orleans, LA 70112, USA Loyola University of Chicago Chicago, IL 60626, USA Arthur N. Popper Department of Zoology University of Maryland College Park, MD 20742, USA

Cover Illustration: WIlliam N. Tavolga

Library of Congress Cataloging-in-Publication Data The evolutionary biology of hearing 1 Douglas B. Webster, Richard R. Fay, Arthur N. Popper, editors. p. cm. Based on a conference held at the Mote Marine Laboratory in Sarasota, Fla., May 20-24, 1990. Includes bibliographical references and index. ISBN-13:978-1-4612-7668-5 1. Ear-Evolution-Congresses. 2. Hearing-Congresses. 3. Physiology, Comparative-Congresses. I. Webster, Douglas B. II. Fay, Richard R. ill. Popper, Arthur N. [DNLM: 1. Ear-congresses. 2. Evolution-congresses. 3. Hearing• congresses. 4. Histology, Comparative-congresses. 5. Invertebrates-congresses 6. Physiology, Comparative• congresses. 7. Vertebrates-congresses. WV 270 E92 1990] QP460.EP96 1992 591.1 '825 - dc20 DNLM/DLC for Library of Congress 91-4805 CIP

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ISBN-13:978-1-4612-7668-5 e-ISBN-13: 978-1-4612-2784-7 DOl: 10.1007/978-1-4612-2784-7 This volume is dedicated to the memory of Professor Ernest Glen Wever (1902-1991), a pioneer in auditory research during much of the 20th century, and one of the few people who kept the flame of evolotionary biology alive in the hearing sciences. Without doubt, his ideas and work have had a major influence on all the chapters in this volume.

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Key to Photograph of Meeting Attendees

1. W. Tavo1ga 18. M. Miller 35. T. Lewis 52. W. Stebbins 2. A. Popper 19. K. Brandle 36. N. Schell art 53. E. Allin 3. D. Webster 20. A. Mason 37. A. Musicant 54. 1. Rosowski 4. R. Fay 2l. S. Yack 38. C. Gans 55. 1. Fullard 5. R. Northcutt 22. L. Gunn 39. T. Hetherington 56. P. Narins 6. C. Platt 23. Z. Wollberg 40. E. Lombard 57. A. Michelsen 7. R. Hoy 24.1. Clack 4l. H. Romer 58. B. Budelmann 8. N. Fuzessery 25. K. Mahadevan 42. B. Lewis 59. R. Williamson 9.1. Hall 26. W. Yost 43. R. Heffner 60. 1. Montgomery lO. R. Masterton 27. 1. Hopson 44. G. Meredith 6l. B. L. Roberts 11. M. Lenhardt 28. C. Schreiner 45. W. Plassmann 62. G. Patton 12. 1. Lu 29. H. Heffner 46. M.G. Sneary 63. D. Ketten 13. 1. Crawford 30. G. Pollak 47. M. Weiderhold 64. S. Frost 14. C. Koppl 3l. 1. Christensen-Dalsgaard 48. C. McCormick 65. 1. Jannsen 15. K. Keller 32.1. Bolt 49. R. Dooling 66. P. Edds 16. C. Carr 33. E. Lewis 50. S. Coombs 67. K. Cortopassi 17. T. Bullock 34. G. Manley 51. C. von Bartheld 68. B. Fritzsch Preface

To develop a science of hearing that is intellectu• The five-day conference was held at the Mote ally satisfying we must first integrate the diverse, Marine Laboratory in Sarasota, Florida, May 20- extensive body of comparative research into an 24, 1990. The invited participants came from the evolutionary context. The need for this integra• fields of comparative anatomy, physiology, biophys• tion, and a conceptual framework in which it could ics, animal behavior, psychophysics, evolutionary be structured, were demonstrated in landmark biology, ontogeny, and paleontology. Before the papers by van Bergeijk in 1967 and Wever in 1974. conference, preliminary manuscripts of the invited However, not since 1965, when the American papers were distributed to all participants. This Society of Zoologists sponsored an evolutionary facilitated - even encouraged - discussions through• conference entitled ''The Vertebrate Ear;' has there out the conference which could be called, among been a group effort to assemble and organize other things, "lively." The preview of papers, along our current knowledge on the evolutionary-as with the free exchange of information and opinion, opposed to comparative-biology of hearing. also helped improve the quality and consistency of In the quarter century since that conference the final manuscripts included in this volume. there have been major changes in evolutionary In addition to the invited papers, several studies concepts (e.g., punctuated equilibrium), in sys• were presented as posters during evening sessions. tematics (e.g., cladistics), and in our understand• The poster abstracts appear at the end of each ing of hearing (e. g., hair cell mechanisms). appropriate group of papers. Moreover, the study of hearing and the ear has The final half-day of the conference was devoted matured to the point where peripheral and central to discussion, in order to allow time for topics not investigations are recognized as of equal impor• previously heard, to attempt consensus on con• tance and are often coordinated. troversial topics, and to suggest some fruitful With these considerations in mind, we realized avenues of future research. This final session was that the time was ripe for an international confer• videotaped and a summary is presented in the final ence on the Evolutionary Biology of Hearing, chapter of this volume. which would have a threefold purpose: to focus on the evolutionary implications of comparative Douglas B. Webster studies; to integrate central and peripheral audi• Richard R. Fay tory studies; and to include both vertebrates and Arthur N. Popper invertebrates. January, 1991

ix Acknowledgments

We are grateful to the National Institute of Deaf• to help us with problems. Without him, and them, ness and Other Communicative Disorders (Grant the conference could not have been as successful. NS I-R13-DCOO667), the National Science Foun• While everyone at Mote has our thanks, a few dation (Grant BNS-8912389) and the Office of deserve special mention: Dr. Robert Heuter for Naval Research (Grant N00014-90-I1799) for pro• extraordinary help in many facets of the organiza• viding funds to support the conference that led to tion of the meeting; Mr. Daniel Bebak, Curator of this volume. the Mote Aquarium; lab photographer, Ms. Car• Without doubt the conference could not have men Harris; Ms. Linda Franklin and Ms. Pamela taken place without the guidance, creativity, James, Administrative Assistants; and Mr. Paul expertise, and support of Dr. William N. Tavolga, Shrader, Business Manager. We are most grateful Senior Scientist at Mote Marine Laboratory. Dr. to Ms. Sandy Hingtgen of the Holiday Inn/Lido Tavolga has become an expert on how to make con• Beach for doing everything possible to make our ferences work. He devoted enormous amounts of stay in Sarasota a pleasant one, and to the Sarasota time and effort to assure that every detail was taken Outboard Club for use of their facilities during part care of so that the conference attendees, including of the meeting. the editors, had no cares except scientific inter• Finally, all the participants thank Chef Alain actions. Mons of the French Affair Delicatessen in Sarasota We are also grateful to Dr. Selvakumaran for once again turning a meeting into a sensory Mahadevan, Director of the Mote Marine Labora• experience. By delighting our senses of taste and tory. He provided outstanding facilities and the smell at mealtimes, he made the long intervening cooperation of his staff, and was always available sessions devoted to hearing much easier.

xi Contents

Preface ...... , .. " ...... ix Acknowledgments ...... xi Contributors ...... xxxvii Ernest Glen Wever: Biography and Bibliography ...... xliii RICHARD R. FAY

SECTION I EVOLUTIONARY PERSPECTIVES Chapter I An Overview of the Evolutionary Biology of Hearing 3 CARL GANS

Chapter 2 Comparisons of Major and Minor Taxa Reveal Two Kinds of Differences: "Lateral" Adaptations and "Vertical" Changes in Grade ...... 15 THEODORE H. BULLOCK

Chapter 3 The Phylogeny of Octavolateralis Ontogenies: A Reaffirmation of Garstang's Phylogenetic Hypothesis 21 R. GLENN NORTHCUTT

Chapter 4 Evolution of the Vertebrate Inner Ear: An Overview of Ideas ...... 49 ARTHUR N. PoPPER, CHRISTOPHER PLATT, AND PEGGY L. EDDS

SECTION II INVERTEBRATES Chapter 5 Hearing and Sound Communication in Small Animals: Evolutionary Adaptations to the Laws of Physics...... 61 AXEL MICHELSEN

Chapter 6 Ecological Constraints for the Evolution of Hearing and Sound Communication in Insects ...... 79 HEINER ROMER

xiii xiv Contents

Chapter 7 The Processing of Auditory Signals in the CNS of Orthoptera ...... 95 BRIAN LEWIS

Chapter 8 The Evolution of Hearing in Insects as an Adaptation to Predation from Bats ...... 115 RONALD R. Hoy

Chapter 9 Hearing in Crustacea...... 131 BERND U. BUDELMANN

Chapter 10 Hearing of Nonarthropod Invertebrates...... 141 BERND U. BUDELMANN Contributed Abstracts A. The Mechanoreceptive Origin of Insect Tympanal Organs: A Comparative Study of Homologous Nerves in Tympanate and Atympanate Moths...... 156 JAYNE E. YACK AND JAMES H. fuLLARD B. Organization of the Auditory Pathway in Noctuoid Moths: Homologous Auditory Evolution in Insects...... 157 G.S. BOYAN, JAMES H. fuLLARD, AND IL.D. WILliAMS C. Hearing in the Primitive Ensiferan Cyphoderris monstrosa (Orthoperta: Haglidae) ...... 158 ANDREW C. MASON AND KLAUS SCHILDBERGER D. Hair Cell Sensitivity in Cephalopod Statocyst 159 RoDDY WILliAMSON

SECTION TIl ASPECTS OF HEARING AMONG VERTEBRATES Chapter 11 Convergence of Design in Vertebrate Acoustic Sensors 163 EDWIN R. LEWIS

Chapter 12 The Efferent Innervation of the Ear: Variations on an Enigma...... 185 BARRY L. ROBERTS AND GLORIA E. MEREDITH

Chapter 13 Evolution, Perception, and the Comparative Method...... 211 WILliAM C. STEBBINS AND MITCHELL S. SOMMERS

Chapter 14 Structure and Function in Sound Discrimination Among Vertebrates ...... 229 RICHARD R. FAY

Section IV Anamniotes Chapter 15 Functional and Evolutionary Implications of Peripheral Diversity in Lateral Line Systems ...... 267 SHERYL COOMBS, JOHN JANSSEN, AND JOHN MONTGOMERY Contents xv

Chapter 16 Functional Aspects of the Evolution of the Auditory System of Actinopterygian Fish ...... 295 NICO A.M. SCHELLART AND ARTHUR N. PoPPER

Chapter 17 Evolution of Central Auditory Pathways in Anamniotes ...... 323 CATHERINE A. MCCORMICK

Chapter 18 The Water-to-Land Transition: Evolution of the Tetrapod Basilar Papilla, Middle Ear, and Auditory Nuclei...... 351 BERND FRITZSCH

Chapter 19 Nature and Quality of the Fossil Evidence of Otic Evolution in Early Tetrapods ...... 377 JOHN R. BOLT AND ERIC R. LOMBARD

Chapter 20 The Stapes of Acanthostega gunnari and the Role of the Stapes in Early Tetrapods ...... 405 lA. CLACK

Chapter 21 The Effects of Body Size on the Evolution of the Amphibian Middle Ear...... 421 THOMAS E. HETHERINGTON

Chapter 22 Biological Constraints on Anuran Acoustic Communication: Auditory Capabilities of Naturally Behaving Animals ...... 439 PETER M. NARINS

Contributed Abstracts E. Some Unique Features of the Ear and the Lateral Line of a Catfish and their Potential Bearing for Sound Pressure Detection ...... 455 H. BLECKMAN, B. FRITZSCH, U. NIEMANN, AND H.M. MULLER F. Comparative Analysis of Electrosensory and Auditory Function in a Mormyrid Fish...... 457 JOHN D. CRAWFORD G. Biophysics of Underwater Hearing in the Clawed Frog, Xenopus laevis ...... 459 J CHRISTENSEN-DALSGAARD AND A. ELEPFANDT

SECTION V NONMAMMALIAN AMNIOTES Chapter 23 The Evolutionary Implications of the Structural Variations in the Auditory Papilla of Lizards...... 463 MALCOLM R. MILLER

Chapter 24 Functional Consequences of Morphological Trends in the Evolution of Lizard Hearing Organs ...... 489 CHRISTINE KOPPL AND GEOFFREY A. MANLEY xvi Contents

Chapter 25 Evolution of the Central Auditory System in Reptiles and Birds...... 511 CATHERINE E. CARR

Chapter 26 Hearing in Birds ...... 545 ROBERT 1. DOOLING

Chapter 27 Evolution and Specialization of Function in the Avian Auditory Periphery...... 561 GEOFFREY A. MANLEY AND OTTO GLEICH

Contributed Abstracts

H. Tuning in the Turtle: An Evolutionary Perspective ..... 581 MICHAEL G. SNEARY AND EDWIN R. LEWIS

I. Paratympanic and Spiracular Sense Organs: Phylogenetic Distribution and Theories of Function, Including Hearing ...... 582 CHRISTOPHER S. VON BARTHELD AND EDWIN W. RUBEL

SECIION VI MAMMALS Chapter 28 Evolution of the Auditory System in Synapsida ("Mammal-Like Reptiles" and Primitive Mammals) as Seen in the Fossil Record ...... 587 EDGAR F. ALLIN AND JAMES A. HOPSON

Chapter 29 Hearing in Transitional Mammals: Predictions from the Middle-Ear Anatomy and Hearing Capabilities of Extant Mammals...... 615 JOHN 1. ROSOWSKI

Chapter 30 Parallel Evolution of Low Frequency Sensitivity in Old World and New World Desert Rodents...... 633 DOUGLAS B. WEBSTER AND WOLFGANG PLASSMANN

Chapter 31 A Functional Model of the Peripheral Auditory System in Mammals and Its Evolutionary Implications...... 637 WOLFGANG PLASSMANN AND KURT BRANDLE

Chapter 32 Origin of Auditory Cortex...... 655 SHAWN B. FROST AND R. BRUCE MASTERTON

Chapter 33 Mammalian Auditory Cortex - Some Comparative Observations ...... 673 MICHAEL M. MERZENICH AND CHRISTOFF E. SCHREINER

Chapter 34 Evolution of Sound Localization in Mammals...... 691 RICKYE S. HEFFNER AND HENRY E. HEFFNER Contents xvii

Chapter 35 The Marine Mammal Ear: Specializations for Aquatic Audition and Echolocation...... 717 DARLENE R. KETTEN

Chapter 36 Adaptations of Basic Structures and Mechanisms in the Cochlea and Central Auditory Pathway of the Mustache Bat ...... 751 GEORGE D. PoLLAK Contributed Abstracts J. The Story of the Evolution of Hearing Identifying the Sources of Sound ...... 779 WILLIAM A. YOST K. Evolution of Ultrasonic and Supersonic Hearing in Man ...... 780 MARTIN L. LENHARDT AND ALEX M. CLARKE L. Broad Frequency Selectivity at High Sound Pressure Levels is Important for Speech Coding in the Cochlear Nucleus ...... 781 S. GREENBERG AND WILLIAM S. RHODE M. Direction-Dependent Acoustical Transformation in the External Ear of the Cat: Effects of Pinna Movement ...... 782 A.D. MUSICANT, lC.K. CHAN, AND lE. HIND N. Toward Understanding Mammalian Hearing Tractability: Preliminary Underwater Acoustical Perception Thresholds in the West Indian Manatee, Tricherchus manatus ...... 783 GEOFFREY W. PATTON AND EDMUND GERSTEIN o. The Acoustic Spatial Environment of the Mustache Bat Within the Context of Evolution ...... 784 Z.M. FUZESSERY

SECfION VII EPILOGUE Chapter 37 Epilogue to the Conference on the Evolutionary Biology of Hearing ...... 787 DOUGLAS B. WEBSTER

Author Index ...... 795 Animal Index ...... 819 Subject Index ...... 841 Detailed Chapter Contents

Preface ...... ix Acknowledgments ...... xi Contributors ...... XXXVll Ernest Glen Wever: Biography and Bibliography RICHARD R. FAY ...... xliii

SECTION I EVOLUTIONARY PERSPECTIVES Chapter I An Overview of the Evolutionary Biology of Hearing CARL GANS...... 3 I . Introduction...... 3 2. Evolutionary Patterns...... 3 2.1 Phenotype and Environment...... 3 2.2 Physiology, Behavior, and Environmental Demands. . . . . 4 2.3 Sequences and Experiments ...... 5 2.4 Uncertainty ...... 5 3. Hearing...... 6 3.1 Aspects...... 6 3.2 Cues and Discrimination...... 7 3.3 Liquids and Gases...... 7 3.4 Transition from Water to Land...... 8 3.5 The Uses of Sounds-Benefits and Costs...... 9 3.6 Social Vocalization in Frogs as an Example of Complexity 10 4. Overview: Trends and Questions ...... 11 5. Summary...... 12 Chapter 2 Comparisons of Major and Minor Taxa Reveal Two Kinds of Differences: "Lateral" Adaptations and "Vertical" Changes in Grade THEODORE H. BULLOCK ...... 15 I . Introduction...... 15 2. Evolution of Hearing ...... 15 3. Estimation of Complexity ...... 16 4. Admission of Vertical Grades...... 17 5. Agenda for Future Research...... 17 6. Summary...... 18

XIX xx Detailed Chapter Contents

Chapter 3 The Phylogeny of Octavolateralis Ontogenies: A Reaffirmation of Garstang's Phylogenetic Hypothesis R. GLENN NORTHCUTT...... 21 1. Introduction...... 21 2. A Cladistic Method for the Analysis of Ontogenies...... 22 2.1 Description and Recognition of Ontogenetic Stages .. . . . 22 2.2 Formulation of Hypotheses of Homologous Ontogenetic Stages ...... 22 2.3 The Polarity of Suspected Homologous Ontogenetic Stages ...... 23 2.4 Generation of Phylogenetic Scenarios...... 24 2.5 Testing Phylogenetic Scenarios ...... 25 2.6 Ontogenetic Changes...... 25 3. Developmental Stages of a Primitive Octavolateralis Placode . . 27 4. The Ancestral Number and Distribution of Octavolateralis Placodes ...... 29 5. The Phylogeny of Ontogenetic Changes in Lateral Line Placodes ...... 33 5.1 Changes in Ontogenetic Stages of Placodes ...... 35 5.2 Changes in Placodal Cell Lineages...... 37 5.3 Frequency of Different Types of Ontogenetic Change ... 40 5.4 Future Directions...... 41 6. Summary...... 42 Chapter 4 Evolution of the Vertebrate Inner Ear: An Overview of Ideas ARTHUR N. PoPPER, CHRISTOPHER PLATT, AND PEGGY L. EDDS ...... 49 1. Introduction...... 49 1.1 A Caution About Terminology ...... 49 2. Germinal Papers...... 50 2.1 Origin of the Vertebrate Inner Ear ...... 50 2.2 The Acousticolateralis Hypothesis...... 50 2.3 Van Bergeijk (1967): "Evolution of Vertebrate Hearing".. 51 2.4 Baird (1974): ''Anatomical Features of the Inner Ear in Submammalian Vertebrates" ...... 51 2.5 Wever (1974): ''The Evolution of Vertebrate Hearing" ...... 53 3. Issues from the Reviewed Papers ...... 54 3.1 Acousticolateralis Hypothesis...... 54 3.2 Auditory Organ Homologies...... 55 4. Summary...... 56

SECTION II INVERTEBRATES CHAPTER 5 Hearing and Sound Communication in Small Animals: Evolutionary Adaptations to the Laws of Physics AXEL MICHELSEN...... 61 1. Introduction...... 61 2. The Transmission Channel...... 61 3. Sound Emission ...... 63 3.1 Animal Monopoles and Dipoles ...... 64 3.2 Communicating Through a Solid Substrate...... 65 3.3 The Metabolic Costs of Signaling...... 65 Detailed Chapter Contents XXI

3.4 Long-Range Signaling: A Summary...... 66 3.5 Close-Range Signals ...... 66 3.6 Physical Restraints on Signal Coding...... 67 4. The Hearing Organs...... 68 4.1 Directional Hearing...... 69 4.2 Frequency Analysis...... 73 5. Summary and Conclusions...... 75 Chapter 6 Ecological Constraints for the Evolution of Hearing and Sound Communication in Insects HEINER ROMER ...... 79 I. Introduction...... 79 2. Range of Communication...... 79 2.1 Signal Attenuation...... 79 2.2 Frequency Filtering...... 81 2.3 Consequences for the Evolution of Signaling...... 82 3. Signal Degradation ...... 83 3.1 Degradation of Temporal Cues ...... 83 3.2 Degradation of Directional Cues ...... 86 4. Noise and Hearing in the Field...... 88 4.1 Interspecific Interference ...... 88 4.2 Intraspecific Interference ...... 89 5. Reliable and Nonreliable Acoustic Cues...... 90 6. Summary...... 90 Chapter 7 The Processing of Auditory Signals in the CNS of Orthoptera BRIAN LEWIS ...... 95 1. Introduction...... 95 1. I Signal Structure and Behavior ...... 95 1.2 The Input to the CNS ...... 96 2. The Central Auditory Pathway ...... 97 2.1 Primary Sensory Neuropil ...... 97 2.2 Local and Intersegmental Neurons...... 97 2.3 Brain Neurons ...... 98 2.4 Descending Brain Neurons ...... 99 3. Central Processing...... 100 3.1 Temporal Selectivity of Central Neurons...... 105 3.2 The Integration of Sound and Vibration...... 108 4. Conclusions ...... 110 Chapter 8 The Evolution of Hearing in Insects as an Adaptation to Predation from Bats RONALD R. Hoy ...... 115 1. Introduction ...... 115 2 Old Problems, Sound Answers ...... 115 2. I Sexual Signals and Ears ...... 115 2.2 Predator Detection and Ears...... 115 2.3 Which Came First: Bats or Ears'? ...... 116 3. Hearing Organs in Insects ...... 117 3.1 Cytological Aspects ...... 117 3.2 Development and Evolution ...... 118 4. Ultrasound Startle/Escape Reactions in Insects ...... 120 4.1 Hearing and Startle in Moths ...... 120 4.2 Hearing and Ultrasound Startle in Crickets ...... 121 xxii Detailed Chapter Contents

4.3 Hearing Organs ...... 121 4.4 Central Nervous Mechanism...... 121 4.5 Hearing and Startle in the Praying Mantis...... 123 4.6 The Mantis Hearing Organ...... 123 4.7 Central Auditory Pathways...... 124 5. Summary and Conclusions...... 125 Chapter 9 Hearing in Crustacea BERND U. BUDELMANN ...... 131 1. Introduction...... 131 2. Production of Sound...... 131 2.1 Production of Sound in Water...... 131 2.2 Production of Sound on Land...... 132 3. Reception of Sound...... 132 3.1 Reception of Sound in Water...... 133 3.2 Reception of Sound on Land...... 136 4. Concluding Remarks...... 136 5. Summary...... 136 Chapter 10 Hearing in Nonarthropod Invertebrates BERND U. BUDELMANN ...... 141 1. Introduction...... 141 2. Possible Receptor Systems for Hearing...... 142 2.1 Superficial Receptor Systems...... 142 2.2 Statocyst Receptor Systems...... 146 3. Evolutionary Aspects and Conclusions...... 151 4. Summary...... 152 Contributed Abstracts...... 156 A. The Mechanoreceptive Origin of Insect Tympanal Organs: A Comparative Study of Homologous Nerves in Tympanate and Atympanate Moths JAYNE E. YACK AND JAMES H. fuLLARD ...... 156 B. Organization of the Auditory Pathway in Noctuoid Moths: Homologous Auditory Evolution in Insects G.S. BOYAN, JAMES H. FULLARD, AND lL.D. WILUAMS ...... 157 C. Hearing in the Primitive Ensiferan Cyphoderris monstrosa (Orthoperta: Haglidae) ANDREW C. MASON AND KLAUS SCHILDBERGER...... 158 D. Hair Cell Sensitivity in the Cephalopod Statocyst RODDY WILUAMSON ...... • . • • . .. 159

Section III Aspects of Hearing Among Vertebrates Chapter 11 Convergence of Design in Vertebrate Acoustic Sensors EDWIN R. LEWIS...... 163 1. Introduction...... 163 2. Theoretical and Conjectural Preamble ...... 164 2.1 Some Technical Formalities...... 164 2.2 Speculations Concerning Selective Advantages...... 166 2.3 Appropriate Signal Processing Schemes ...... 167 3. High-Order Dynamics in Peripheral Acoustic Filters...... 169 3.1 SIISO Functions from Reverse Correlation ...... 169 3.2 How High-Order Dynamics Might Be Achieved...... 174 4. Summary and Conclusions...... 181 Detailed Chapter Contents xxiii

Chapter 12 The Efferent Innervation of the Ear: Variations on an Enigma BARRY L. ROBERTS AND GLORIA E. MEREDITH...... 185 1. Introduction...... 185 2. Targets for the Efferent Innvervation ...... 185 3. Patterns of Efferent Innervation of Auditory Endorgans ...... 187 4. Central Organization of the Auditory Efferent System ...... 189 4.1 Organization in Anamniotes ...... 191 4.2 Organization in Amniotes ...... 192 5. Putative Neurotransmitters of the Auditory Efferent System...... 193 5.1 Neurotransmitter Distribution in Animals Other Than Mammals ...... 193 5.2 Neurotransmitter Distribution in Mammals...... 196 6. Circuitry Underlying the Activation of the Auditory Efferent System ...... 196 6.1 Sensory Activation of Efferent Neurons...... 196 6.2 Central Activation of Efferent Neurons...... 198 7. Trends in the Evolution of OEN ...... 2oo 8. Other Hair Cell Systems with an Efferent Innervation ...... 202 9. The Origins of the OES ...... 202 10. Summary and Conclusions...... 203

Chapter 13 Evolution, Perception, and the Comparative Method WILLIAM C. STEBBINS AND MITCHELL S. SOMMERS...... 211 1. Introduction...... 211 2. Precursors...... 212 3. The Comparative Method ...... 214 4. The Research Program...... 216 5. Summary...... 224

Chapter 14 Structure and Function in Sound Discrimination Among Vertebrates RICHARD R. FAY ...... 229 1. Introduction...... 229 1.1 What Are the Functions of Hearing? ...... 229 2. Sound Discrimination...... 230 2. 1 How Is Sound Discrimination Measured? ...... 231 2.2 Operant Methods with Reward ...... , ...... 231 2.3 Avoidance Methods...... 232 2.4 Classical Conditioning...... 232 3. Hearing and Sound Discrimination in Vertebrates...... 232 3.1 Hearing Sensitivity and Bandwidth (Audiograms) ...... 234 3.2 Level Discrimination...... 235 3.3 Temporal Analysis in Hearing...... 236 4. Frequency Analysis ...... 243 4.1 Four Behavioral Measures of Frequency Resolution. . . .. 243 4.2 Structure and Function in Frequency Analysis ...... 245 4.3 Can Cochlear Maps Predict Behavioral Performance in Frequency Analysis? ...... 248 4.4 Psychophysical Tuning Curves...... 255 4.5 Fishes May Be Similar to Mammals and Birds in Patterns of Frequency Analysis...... 256 5. Summary and Conclusions...... 257 xXiv Detailed Chapter Contents

SECTION IV ANAMNIOTES

Chapter 15 Functional and Evolutionary Implications of Peripheral Diversity in Lateral Line Systems SHERYL COOMBS, JOHN JANSSEN, AND JOHN MONTGOMERY ...... 267 1. Introduction...... 267 2. Peripheral Anatomy and Innervation of the Lateral Line System ...... 268 3. Phyletic Distribution and Origin of the Lateral Line System ...... 269 4. Anatomical Dimensions of Variability and Functional Consequences ...... 270 4.1 Superficial Neuromasts vs Canal Neuromasts ...... 271 4.2 Canal Width...... 272 5. Developmental Mechanisms in the Evolution of the Lateral Line System ...... 275 6. Selective Pressures in the Evolution of Lateral Line Systems .. 276 6.1 The Evolution of Widened Head Canals in Percid Fishes. 277 6.2 The Evolution of Supernumerary Free Neuromasts in Amb1yopsid Blind Cavefish...... 278 7. Lateral Line and Inner Ear Stimuli - From Incompressible Water Flow to Propagated Pressure Waves ...... 279 8. Operational and Functional Trends in the Evolution of the Lateral Line and Inner Ear ...... 283 9. Functional Overlap Between the Lateral Line and Auditory System...... 287 10. Summary and Conclusions...... 288

Chapter 16 Functional Aspects of the Evolution of the Auditory System of Actinopterygian Fish NICO A.M. SCHELLART AND ARTHUR N. PoPPER ...... 295 1. Introduction...... 295 2. The Diversity of Underwater Acoustic Environments...... 295 2.1 Underwater Acoustics ...... 296 2.2 Constraints of Underwater Sound Characteristics on the Evolution of Fish Hearing ...... 296 2.3 Background Noise...... 297 2.4 Conclusions...... 299 3. Use of Sounds by Fishes ...... 302 4. Structure and Function of Teleost Ears...... 303 4.1 Ear Structure ...... 303 4.2 Ear Stimulation...... 305 5. Hearing Abilities, Specializations, and Habitat...... 306 6. The Swimbladder ...... 310 6.1 Swimbladder Mechanics ...... 310 6.2 The Swimbladder and Hearing...... 311 6.3 Swimbladder Shape and Hearing...... 311 6.4 Conclusions...... 313 7. Functional Morphology of the Inner Ear ...... 313 7.1 Hair Cell Orientation Patterns ...... 313 7.2 Otolith Structure and Relationship to the Epithelium. . .. 315 7.3 Functional Specialization of Otolith Systems: Multifunctionality and Directional Hearing...... 315 Detailed Chapter Contents xxv

8. Evolution of the Ear in Agnathans and Elasmobranchs ...... 317 8.1 Agnathans...... 317 8.2 Elasmobranches...... 317 9. Summary ...... 318 Chapter 17 Evolution of Central Auditory Pathways in Anamniotes CATHERINE A. MCCORMICK...... 323 1. Introduction...... 323 2. Class Agnatha...... 323 2.1 Inner Ear Structure and Function...... 323 2.2 Central Representation of the Agnathan Inner Ear...... 325 3. Class Chondrichthyes...... 325 3.1 Inner Ear Structure and Function...... 325 3.2 Central Representation ofInner Ear Endorgans ...... 327 3.3 Higher-Order Acoustic Areas...... 328 4. Class Osteichthyes ...... 329 4.1 Inner Ear Structure and Function...... 329 4.2 Inner Ear Projections in Osteichthyans: Primitive Pattern ...... 330 4.3 Inner Ear Projections in Teleosts: Minor Variations on the Primitive Pattern ...... 330 4.4 More Elaborate Variations on the Primitive Pattern in Teleosts ...... 331 4.5 Higher Order Acoustic Projections...... 334 5. Class Amphibia...... 337 5.1 Structure and Function of the Inner Ear ...... 337 5.2 Inner Ear Projections to the Medulla...... 338 5.3 Higher Order Auditory Connections ...... 341 6. Discussion .... . 342 7. Summary ...... 345 Chapter 18 The Water-to-Land Transition: Evolution of the Tetrapod Basilar Papilla, Middle Ear, and Auditory Nuclei BERND FRITZSCH ...... 351 I . Introduction...... 351 2. Presumed Adaptations of the Ear of Sarcopterygian Fish to Detect the Pressure Component of Aquatic Sound ...... 352 2.1 Perilymphatic, Pressure-Detection Endorgans in Vertebrates...... 354 2.2 Definition and Distribution of a Basilar Papilla...... 355 2.3 Relationship of the Basilar Papilla to the Lagenar Macula and Recess...... 357 2.4 Ontogenetic Events Related to the Phylogenetic Diversity of the Lagena and Basilar Papilla...... 357 2.5 The Evolution of the Perilymphatic Labyrinth ...... 359 2.6 The Evolution of the Perilymphatic Foramen to the Cranial Cavity ...... 361 2.7 The Spiracular Pouch and the Possible Evolution of a Tympanic Ear in Water...... 361 2.8 The Canalis Communicans...... 362 2.9 What Could Cause Differences in Pressure on Either Side of the Basilar Papilla? ...... 362 2.10 Physical Constraints of Underwater Hearing...... 364 2.11 The Ear and the Systematic Position of Latimeria ...... 364 xxvi Detailed Chapter Contents

3. The Water-to-Land Transition: De Novo Development of a Tympanic Ear or Transformation of an Aquatic Tympanic Ear? ...... 365 3.1 Changed Physical Conditions Necessitate the Transformation of an Aquatic Tympanic Ear ...... 366 3.2 Insertion of the Hyomandibular Bone and Development ofthe Perilymphatic Labyrinth...... 367 3.3 The Evolution of the Amphibian Papilla...... 368 3.4 Biological Context of Hearing of Ancestral Tetrapods ... 369 4. Reorganizations in the Central Nervous System During the Water-to-Land Transition...... 369 4.1 Metamorphic Loss ofthe Lateral Line System Does Not Correlate with the Development of Auditory Nuclei in Frogs ...... 369 4.2 Loss of Electroreception Shows Phylogenetic Coincidence with the Appearance of Primary Auditory Nuclei...... 370 4.3 What Causes the Formation of Separate Projections of "Perilymphatic Endorgans" in Vertebrates? ...... 370 5. Summary...... 372

Chapter 19 Nature and Quality of the Fossil Evidence for Otic Evolution in Early Tetrapods JOHN R. BOLT AND R. ERIC LOMBARD ...... 377 1. Introduction...... 377 2. Paleozoic Tetrapods ...... 377 2.1 Time and Space...... 377 2.2 The Nature of the Fossils ...... 380 2.3 The Major Taxa...... 384 3. Evolutionary Relationships ...... 385 4. Overview of Otic Structure...... 387 4.1 The Scope of the Data...... 387 4.2 Otic Structure ...... 389 5. Evolution of the Ear ...... 392 6. Summary and Conclusions...... 399 Appendix...... 402

Chapter 20 The Stapes of Acanthostega gunnari and the Role of the Stapes in Early Tetrapods lA. CLACK...... 405 1. Introduction...... 405 2. The Stapes and Otic Region of Acanthostega gunnari ...... 405 2.1 Description and Comparative Morphology ...... 406 2.2 The Temporal Notch of Acanthostega ...... 409 2.3 The Otic Capsule of Acanthostega ...... 409 2.4 Phylogenetic Considerations...... 410 3. The Function of the Stapes and Otic Region in Early Tetrapods ...... 411 3.1 Recent Hypotheses...... 411 3.2 Relationships of the Stapes, Palate, Braincase, and Skull Roof in Early Tetrapods-The Fallacy of Autostyly in the Earliest Tetrapods...... 412 3.3 Functional Considerations...... 415 4. Summary...... 418 Detailed Chapter Contents XXVII

Chapter 21 The Effects of Body Size on the Evolution of the Amphibian Middle Ear THOMAS E. HETHERINGTON...... 421 1. Introduction...... 421 2. Design and Function of Acoustic Receptive Systems in Amphibians...... 421 2.1 The Tympanic Middle Ear...... 421 2.2 The Opercularis System ...... 422 2.3 Other Nontympanic Pathways of Sound Reception...... 424 2.4 An Integrated View of Acoustic Reception in Amphibians ...... 425 3. Effects of Body Size on Mechanisms of Acoustic Reception . .. 426 3.1 Scaling of Middle Ear Morphology ...... 426 3.2 Scaling of the Frequency Response of the Tympanic Middle Ear...... 427 3.3 Scaling of Nontympanic Sound Reception...... 428 3.4 An Overview of the Effects of Body Size on Acoustic Reception...... 429 4. Loss of the Tympanic Middle Ear-A Major Evolutionary Trend...... 430 4.1 Morphological Patterns of Tympanic Middle Ear Reduction ...... 430 4.2 Factors Correlated with Reduction and Loss of the Tympanic Ear ...... 431 4.3 The Relationship Between Body Size and Loss of the Tympanic Ear ...... 433 5. Discussion and Summary...... 434

Chapter 22 Biological Constraints on Anuran Acoustic Communication: Auditory Capabilities of Naturally Behaving Animals PETER M. NARINS...... 439 1. Introduction...... 439 1.1 A "Representative" Neotropical Chorusing Anuran...... 440 2. Field Psychoacoustics...... 440 2.1 Behavioral Response Functions...... 440 2.2 Isointensity Response ...... 441 2.3 Timing Shifts as a Measure of Threshold...... 441 2.4 Call Duration Sensitivity...... 443 2.5 Effective Critical Ratio and Effective Critical Band. . . .. 443 2.6 Intensity Discrimination...... 444 3. Interindividual Time Constants...... 447 3.1 Behavioral Refractory Period (BRP)...... 447 3.2 Call Synchronization Rate (CSR) ...... 447 3.3 Relationship Between BRP and CSR ...... 449 4. Collective Acoustic Behavior of Anuran Amphibians ...... 449 4.1 Dynamic Chorus Structure (DCS) ...... 450 5. Summary and Conclusions...... 451 Contributed Abstracts E. Some Unique Features of the Ear and the Lateral Line of a Catfish and Their Potential Bearing for Sound Pressure Detection H. BLECKMAN, B. FRITZSCH, U. NIEMANN, AND H.M. MULI.ER ...... 455 xxviii Detailed Chapter Contents

F. Comparative Analysis of Electrosensory and Auditory Function in a Mormyrid Fish JOHN D. CRAWFORD ...... 457 G. Biophysics of Underwater Hearing in the Clawed Frog, Xenopus laevis J CHRISTENSEN-DALSGAARD AND A. ELEPFANDT ...... 459

SECfION V NONMAMMALIAN AMNIOTES

Chapter 23 The Evolutionary Implications of the Structural Variations in the Auditory Papilla of Lizards MALCOLM R. MILLER ...... 463 1. Introduction...... 463 2. Basic Anatomy of the Lizard Cochlear Duct and Basilar Papilla ...... 463 3. Comparative Anatomy of the Cochlear Duct and Basilar Papilla of Lizard Families...... 466 3.1 Relationship of Lizard Cochlear Duct and Basilar Papilla Anatomy to that of Other Reptiles ...... 466 3.2 The Development of Bidirectionally Oriented Hair Cells in Lizards ...... 468 3.3 Gross Anatomical Features of the Cochlear Duct of Species of Different Lizard Families ...... 470 3.4 Groups of Ear-Related Lizard Families Based on Gross and Fine Structural Anatomy...... 471 4. Phylogeny of Lizard Families Based on Cochlear Duct and Basilar Papilla Structure ...... 480 4.1 Ancestral Type Auditory Papilla and Its Relationship to the Papillae of the Teiidae and Varanidae ...... 480 4.2 Possible Lines of Descent ...... 480 5. Possible Taxonomic and Phylogenetic Relationships of Lizard Families Based on Wever's (1978) Reptilian Ear Studies and on that of Other Anatomical Characters ...... 483 5. I Wever's Taxonomic Grouping of Lizard Families ...... 483 5.2 Taxonomic Relationships Based on Brain Anatomy. . . .. 484 5.3 Taxonomic Relationships Based on Other Anatomical Characters ...... 484 5.4 Camp's (1923) Classic Proposal of Lizard Family Phylogeny...... 484 6. Possible Significance of Cochlear Duct and Basilar Papilla Structural Variations...... 485 7. Summary and Conclusions...... 485

Chapter 24 Functional Consequences of Morphological Trends in the Evolution of Lizard Hearing Organs CHRISTINE KOPPL AND GEOFFREY A. MANLEY...... 489 1. Introduction...... 489 2. The Hearing of the Red-Eared Turtle (Pseudemys scripta) as an Example of the Presumed Ancestral Condition...... 489 2.1 Hearing Range...... 489 2.2 Tonotopic Organization of the Turtle's Basilar Papilla. . .. 489 2.3 Frequency Selectivity ...... 490 2.4 An Active Force-Generating Mechanism in Hair Cells. .. 492 Detailed Chapter Contents xxix

3. The Hearing of Modern Lizards ...... 492 3.1 The Alligator Lizard Gerrhonotus multicarinatus (Anguidae) and the Granite Spiny Lizard Sceloporus orcutti (Iguanidae) ...... 492 3.2 The Bobtail Lizard TIliqua rugosa (Scincidae) ...... 496 3.3 The Lacertid Lizards Podarcis muralis and P. sicula (Lacertidae) ...... 499 3.4 The Tokay Gecko Gekko gecko (Gekkonidae) ...... 499 4. How Is the Diverse Anatomy of the Lizard Ear Reflected in its Function? ...... 500 4.1 The Hearing Range and Papillar Size Do Not Correlate.. 500 4.2 There Is a Fundamental Segregation of Low-Frequency and High-Frequency Processing...... 501 5. Implications for the Evolution of Lizard Hearing...... 504 5. I Differences Between the Hearing of the Turtle and of Lizards ...... 504 5.2 Anatomical Characteristics and the Origin of the High- Frequency Papillar Segment in Lizards ...... 505 5.3 Possible Causes of the Structural Variation in Lizards '" 506 6. Summary...... 507 Chapter 25 Evolution of the Central Auditory System in Reptiles and Birds CATHERINE E. CARR...... 511 1. Introduction...... 511 2. Phylogenetic Considerations ...... 511 2.1 Reptiles...... 512 2.2 Birds...... 512 3. Hearing Range ...... 513 3. 1 Auditory Sensitivity ...... 513 3.2 Sound Localization...... 513 3.3 Song and Vocalization...... 514 4. The Central Auditory System: Basic Reptilian Plan...... 514 4.1 Chelonia (Turtles and Tortoises)...... 514 4.2 Lepidosauria (Lizards and Snakes) ...... 515 4.3 Crocodilia (Caiman) ...... 519 5. The Central Auditory Pathways: Basic Avian Plan ...... 521 5.1 Basal Landbirds - Pigeon, Chicken, Guinea Fowl, and Budgerigar...... 521 5.2 Higher Landbirds...... 525 5.3 Waterbirds (Duck, Seagull) ...... 530 6. Evolution of Central Auditory Pathways in Birds and Reptiles. 530 6.1 Morphotype...... 530 6.2 Specializations in Reptiles...... 531 6.3 Specializations in Birds...... 532 6.4 Comparisons with the Mammalian Central Auditory System...... 535 7. Summary...... 537 Chapter 26 Hearing in Birds ROBERT J. DOOLING ...... 545 1. Introduction...... 545 2. Sensitivity to Changes in an Acoustic Signal...... 545 3. Absolute Threshold Sensitivity...... 546 3.1 Comparison Among the Orders of Birds ...... 547 xxx Detailed Chapter Contents

3.2 Comparison of Passerines/Nonpasserines/Owls ...... 547 3.3 Comparison Among the Families of Passerines ...... 548 3.4 Absolute Sensitivity and the Characteristics of Vocal Signals ...... 549 4. Vocal Learning and the Perception of Complex Sounds...... 551 4.1 Perceptual Categories for Vocal Signals: Species Differences ...... 552 4.2 Perceptual Categories for Vocal Signals: Effects of Experience and Sex ...... 554 5. Summary and Conclusions...... 557

Chapter 27 Evolution and Specialization of Function in the Avian Auditory Periphery GEOFFREY A. MANLEY AND OTTO GLEICH ...... 561 1. Introduction...... 561 2. The Middle Ear and the Hearing Range...... 561 3. Phylogenetic Considerations...... 562 3.1 The Phylogenetic Relationships of Extant Reptiles, Birds, and Mammals ...... 562 3.2 Relationships Between Extant Families of Birds ...... 563 4. The Starling as a Model of Bird Hearing ...... 563 4.1 The Avian Cochlear Duct ...... 564 4.2 Structure of the Starling's Hearing Organ...... 565 4.3 Physiology of the Auditory Papilla of the Starling...... 565 5. A Comparison of Structural and Functional Data from Other Avian Species ...... 571 6. The Evolution of the Avian Hearing Organ...... 573 6.1 General Trends in the Early Evolution of the Avian Papilla ...... 573 6.2 Functional Implications of Variations in Avian Papillar Anatomy...... 574 6.3 Mechanisms of Frequency Selectivity in the Avian Basilar Papilla ...... 575 6.4 Is the Avian Basilar Papilla a Multifunctional Sense Organ? ...... 577 7. Summary...... 578 Contributed Abstracts H. Tuning in the Turtle: An Evolutionary Perspective MICHAEL G. SNEARY AND EDWIN R. LEWIS...... 581 I. Paratympanic and Spiracular Sense Organs: Phylogenetic Distribution and Theories of Function, Including Hearing CHRISTOPHER S. VON BARTHELD AND EDWIN W. RUBEL ...... 582

SECTION VI MAMMALS

Chapter 28 Evolution of the Auditory System in Synapsida ("Mammal-Like Reptiles" and Primitive Mammals) as Seen in the Fossil Record EDGAR F. ALUN AND JAMES A. HOPSON ...... 587 1. Introduction...... 587 2. Homologies...... 590 Detailed Chapter Contents xxxi

3. Osteologic Features of Fossil Synapsid Groups ...... 592 3.1 Nontherapsid Synapsids ("Pelycosaurs") ...... 592 3.2 Biarmosuchia (Basal Therapsids) ...... 597 3.3 Advanced Nontheriodont Therapsids ...... 597 3.4 Noncynodont Theriodonts (Gorgonopsians and Therocephalians) ...... 598 3.5 Nonmammalian Cynodonts...... 599 3.6 Primitive Mammals...... 604 3.7 Advanced Mammals...... 606 4. Inner Ear ...... 606 5. Parallel Originations of the Definitive Mammalian Middle Ear (DMME) ...... 608 6. Mode of Transference of Postdentary Elements to the Cranium...... 608 7. Theories of Auditory Evolution: Comparison of Paradigms ... 609 8. Summary...... 611

Chapter 29 Hearing in Transitional Mammals: Predictions from the Middle-Ear Anatomy and Hearing Capabilities of Extant Mammals JOHN J. ROSOWSKI...... 615 1. Introduction...... 615 2. Review of the Structure of the Middle Ear of a Transitional Mammal, Morganucodon ...... 616 3. Comparisons of the Middle Ear of Morganucodon with those of Extant Mammals ...... 617 3.1 Comparisons of Middle-Ear Type...... 617 3.2 Comparisons of Middle-Ear Size ...... 619 4. Dependence of Auditory Function on Middle-Ear Structure. .. 619 4.1 Definition of Limits of Hearing ...... 620 4.2 Relationships Between Middle-Ear Type and Hearing Limits ...... 620 4.3 Relationships Between Middle-Ear Areas and Hearing Limits...... 621 5. Predicting Hearing Limits from Middle-Ear Dimensions. . . .. 623 5.1 Predictions of the Hearing Limits for Morganucodon . . .. 623 5.2 Tests ofthe Prediction Procedure...... 624 5.3 Hearing in Morganucodon...... 625 6. Discussion...... 626 6.1 The Influence of the Inner Ear...... 626 6.2 Absolute Hearing Sensitivity ...... 626 6.3 Mechanisms for the Observed Relationships Between Middle-Ear Structure and Hearing Function ...... 626 6.4 Effect of Head Size ...... 628 6.5 Speculations About the Niche Filled by Morganucodon and Other Early Mammals ...... 628 7. Summary and Conclusions...... 628

Chapter 30 Parallel Evolution of Low-Frequency Sensitivity in Old World and New World Desert Rodents DOUGLAS B. WEBSTER AND WOLFGANG PLASSMANN ...... 633 1. Introduction...... 633 2. Middle Ear Differences Between Heteromyids and Gerbils ... 633 xxxii Detailed Chapter Contents

3. Inner Ear Differences Between Heteromyid and Gerbilline Rodents ...... 634 4. Low-Frequency Hearing and Its Adaptive Value in Heteromyids and Gerbillines ...... 635 5. Summary...... 635 Chapter 31 A Functional Model of the Peripheral Auditory System in Mammals and Its Evolutionary Implications WOLFGANG PLASSMANN AND KURT BRANDLE ...... 637 1. Introductory Deliberations...... 637 1.1 Frequency Range and Adaptation...... 637 1.2 Adaptation versus Constraints...... 638 1.3 Methodological Deliberations...... 638 1.4 Basic Facts on the Peripheral Auditory System ...... 640 1. 5 Structural Model of the Peripheral Auditory System. . . .. 641 1.6 Fundamental Assumptions for the Model ...... 641 2. Functional Model of Mammalian Outer and Middle Ear...... 642 2.1 Assumptions and Acoustic Equations...... 642 2.2 Empirical Basis for Verification of the Functional Model. 642 2.3 Mathematical Deliberation...... 643 3. Basic Functional Model and Essential Deviations...... 643 3.1 Establishment of a Plausible Model Variant...... 643 3.2 Basic Functional Model and Approximation Procedure.. 644 3.3 Deviation from the Basic Model in Gerbilline Rodents .. 646 4. Basic Functional Model and Implications...... 648 4.1 Physical Functioning ofthe Model...... 648 4.2 Frequency Range of Best Sensitivity ...... 648 4.3 Interdependence of Structures and Resonance Frequencies ...... 648 4.4 Morphological Constraints for Frequency Shifts...... 649 4.5 Evolutionary Aspects...... 649 5. Summary...... 651 Appendix: Mathematical Solution...... 651 Chapter 32 Origin of Auditory Cortex SHAWN B. FROST AND R. BRUCE MASTERTON ...... 655 1. Introduction...... 655 1.1 Homology and Homoplasy Among Vertebrate Forebrains...... 655 1.2 Contribution of Mferent Projections to the Study of Forebrain Homologies...... 655 1.3 Relative Locations of Sensory Targets in the Forebrain .. 656 1.4 Phyletic Evidence of Nuclear Migration ...... 659 2. Telencephalic Projections of Medial Geniculate in Marsupials. 659 2.1 Subcortical Projections in Didelphis virginiana ...... 659 2.2 Subcortical Projections in Monodelphis domestica ...... 661 3. Telencephalic Projections of Medial Geniculate in Placentals .. 663 3.1 Subcortical Projections in Placentals ...... 664 3.2 Phyletic Reduction of Subcortical Projections...... 665 4. Discussion...... 665 4.1 Translocation of Auditory Telencephalon...... 665 4.2 Expansion of Preexisting Neocortex...... 669 4.3 Differentiation of Preexisting Neocortex...... 669 4.4 Importation of Non-Neocortex into Neocortex ...... 670 5. Summary...... 670 Detailed Chapter Contents xxxiii

Chapter 33 Mammalian Auditory Cortex - Some Comparative Observations MICHAEL M. MERZENICH AND CHRISTOFF E. SCHREINER 673 1. Introduction .... """.""""""", .... ",., .. "", 673 2. Some Comparative Observations on the Organization of Auditory Cortical Fields """""""",.""""", 673 2,1 Cytoarchitectonic and Myeloarchitectonic Studies of Auditory Cortical Fields, . , , , , , , , .. , . , , , , , . , , , , " 673 2,2 Physiological Identification of the Primary Auditory Cortex, , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , " 674 2.3 Identification of Other Auditory Cortical Fields, , , , , , " 678 2.4 Internal Organization of Auditory Cortical Fields; Topographic Organization Beyond Tonotopicity , .. , , , " 681 3. Studies of Phylogenetic Development of Cortical Representations in Other Sensory Systems; Some Relevant Findings and Conclusions """."."""""""""" 683 4. Ontogenetic Formation of Cortical "Maps"; Implications for Comparative Studies, , , , , . , .. , , , , , , , . , , , , , , , , , . , , , ,. 684 5. Summary; Some General Conclusions " , , .. , , , , , , , , . , , , " 685

Chapter 34 Evolution of Sound Localization in Mammals RICKYE S. HEFFNER AND HENRY E. HEFFNER, , , , , . , , , , , .. ,. 691 1. Introduction .. ,."",."""""""""""""""" 691 2, The Cues for Sound Localization """""""""""" 691 2.1 Binaural Locus Cues, , , , , .. , . , , . , , , . , . , , , , , . , , , , " 692 2.2 Monaural Spectral Cues, . , , , , , , , , , , , , , , . , , , , , , , , , " 694 3, Variation in the Use of Binaural Locus Cues Among Mammals , . , , , , , , , , . , , , , , , , , , , , , , , , , , , , , , , , , " 695 3.1 Determining the Use of Binaural Locus Cues ,.,.,.,.,. 695 3.2 Species Using Binaural Phase and Intensity Difference Cues, , , , , , , . , , , , , . , , , , , , , . , , , , , .. , , , " 695 3.3 Species with Limited or Absent Ability to Use Binaural Phase Differences .. , , , .... , .... , .. ' ..... ,. 697 3.4 Species with Reduced or Absent Ability to Use Binaural Intensity Differences .. ,." .. , ...... ,... 698 3.5 Species Using Neither Binaural Time Nor Intensity .. , .. 699 4. Use of Monaural Spectral Cues ... , ...... , .... , . .. 700 4.1 Sound Localization in the Horizontal Plane. , .... , .... , 700 4.2 Sound Localization in the Vertical Plane. , . , .. , . , .. , ., 701 4.3 Mobile Pinnae, , .. , . , , . , .. , .. , .. , .... , .. , .... , . .. 702 5. Variation in the Superior Olivary Complex ,., .. , .... ,..... 702 6. Evolution of High-Frequency Hearing ...... , .. , .. , ...... 703 6.1 High-Frequency Hearing and Sound Localization ... , . .. 703 6.2 Alternative Explanations of High-Frequency Hearing ... , 706 7. Evolution of Horizontal Sound-Localization Acuity, .. , .... ,. 707 7. I Availability of Binaural Cues ...... , .. ' . , .. , . .. 708 7.2 The Relation to Vision, .. , .. , .... , , .. , .... , .. , , . , ,. 708 8. Summary: Evolution of Mammalian Sound Localization .. , .. , 711

Chapter 35 The Marine Mammal Ear: Specialization for Aquatic Audition and Echolocation DARLENE R. KETTEN , ..... , .. ,. , ... , .. , .. , .... , .. , ...... 717 1. Introduction ... ,., .. , ...... ,." ... , ...... ,.... 717 1.1 Adaptive Radiation of Cetacea . , . , , ... , .... , ...... , 717 xxxiv Detailed Chapter Contents

2. Sound Production Characteristics and Audition...... 719 2.1 Audiometric Data ...... 719 2.2 Cetacean Vocalizations ...... 720 3. Cetacean Cranial Morphology...... 720 3.1 Telescoping...... 722 3.2 Cranial Paths for Emitted Sounds...... 722 3.3 Cranial Structures for Sound Reception...... 724 4. The Extant Cetacean Ear ...... , 725 4.1 The Tympano-Periotic Complex...... 725 4.2 The Middle Ear ...... 727 4.3 The Inner Ear ...... , 729 5. The Extinct Cetacean Ear ...... 738 6. Cetacean Auditory Adaptations...... 741 6.1 Comparative Speculations...... 741 6.2 Future Directions and Open Questions ...... , 742 7. Summary...... 743 Appendix I-Marine Mammal Divisions...... 749 Chapter 36 Adaptations of Basic Structures and Mechanisms in the Cochlea and Central Auditory Pathway of the Mustache Bat GEORGE D. PoLLAK ...... 751 1. Introduction ...... 751 2. The Doppler Based Biosonar System of the Mustache Bat .... 752 3. Adaptation of the Peripheral Auditory System for Processing 60 kHz ...... 754 3.1 Anatomical Features of the Basal Region of the Mustache Bat's Cochlea ...... 755 3.2 Two Regions of the Basal Cochlea Are Densely Innervated ...... 756 3.3 The Frequency-Place Map of the Mustache Bat's Cochlea ...... 758 3.4 Speculations on the Functional Consequences of the Anatomical Specializations ...... 758 4. Response Properties of Auditory Nerve Fibers Reflect Cochlear Features ...... 760 4.1 Sharply Tuned Filter Units Are Sensitive to Amplitude and Frequency Modulations ...... 761 5. Peripheral Adaptations Are Conserved in the Central Auditory Pathway ...... 762 6. Collieular Features Derived from Processing in the Central Auditory Pathway: Monaural and Binaural Representation .... 764 7. The Source of Ascending Projections to Each of the Aural Regions of the Dorsoposterior Division of the Mustache Bat's Inferior Colliculus ...... 766 8. The Population of E-I Neurons Have Different Sensitivities for Interaural Intensity Disparities ...... 767 8.1 Ultrasonic Frequencies Generate Large Interaural Intensity Disparities ...... 768 8.2 The Spatial Selectivities of 60 kHz E-I Neurons Are Determined by the Disparities Generated by the Ears and the Neuron's Inhibitory Threshold ...... 769 8.3 Inhibitory Thresholds of 60 kHz E-I Neurons Are Topographically Organized Within the Dorsoposterior Division and Create a Representation of Acoustic Space .. 770 Detailed Chapter Contents xxxv

9. One Group of E-E Neurons Code for Elevation Along the Midline...... 771 10. Spatial Properties of Neurons Tuned to Other Frequencies. . .. 772 10.1 The Representation of Auditory Space in the Mustache Bat's Inferior Colliculus...... 773 11. Conclusions...... 774 Contributed Abstracts J. The Story of the Evolution of Hearing Identifying the Sources of Sound WILLIAM A. YOST ...... 779 K. Evolution of Ultrasonic and Supersonic Hearing in Man MARTIN L. LENHARDT AND ALEX M. CLARKE...... 780 L. Broad Frequency Selectivity at High Sound Pressure Levels Is Important for Speech Coding in the Cochlear Nucleus S. GREENBERG AND WILLIAM S. RHODE ...... 781 M. Direction-Dependent Acoustical Transformation in the External Ear of the Cat: Effects of Pinna Movement A.D. MUSICANT, lC.K. CHAN AND lE. HIND...... 782 N. Toward Understanding Mammalian Hearing Tractability: Preliminary Underwater Acoustical Perception Thresholds in the West Indian Manatee, Trichechus manatus GEOFFREY W. PATTON AND EDMUND GERSTEIN...... 783 O. The Acoustic Spatial Environment of the Mustache Bat Within the Context of Evolution Z.M. FUZESSERY ...... 784

SECTION VII. EPILOGUE Chapter 37 Epilogue to the Conference on the Evolutionary Biology of Hearing DOUGLAS B. WEBSTER ...... 787 1. Definition of Hearing ...... 787 2. How Often and Where Has Hearing Evolved? ...... 788 2.1 Invertebrates...... 788 2.2 Fishes...... 788 2.3 Transition from Water to Land...... 788 3. Is the Evolution of Hearing More Complex Than the Evolution of Other Sensory Systems? ...... 789 4. Central Auditory System of Vertebrates ...... 790 5. Hair Cells ...... 790 6. Cochlear Emissions ...... 790 7. Selective Pressure for Hearing...... 790 8. Topics Not Adequately Covered in the Conference...... 792 8.1 Hearing Ability and Mechanisms in Nonteleost Fishes. .. 792 8.2 Evolutionary Biology of Middle Ear in Extant Mammals. 792 8.3 Evolutionary Biology of Cochlea in Extant Mammals ... 792 8.4 Evolutionary Biology of Auditory Brainstem in Extant Mammals ...... 792 9. Summary...... 792

Author Index ...... 795 Animal Index ...... 819 Subject Index ...... 841 Contributors

Edgar F. Allin Department of Anatomy, Chicago College of Osteopathic Medicine, Chicago, IL 60615, USA

H. Bleckman Universitat Bielefeld, Fakultat fUr Biologie, Lehrstuhl fUr Neurophysiologie, 4800 Bielefeld, FRG

John Bolt Department of Geology, Field Museum of Natural History, Chicago, IL 60605, USA

G.S. Boylan Molecular Neurobiology Group, Research School of Biological Sciences, Australian National University, Canberra City, ACT 2601, Australia

Kurt Brandle Zoologisches Institiit, J.w. Goethe Universitat. D-6000 Frankfurt/Main, FRG

Bernd U. Budelmann The Marine Biomedical Institute. The University of Texas Medical Branch at Galveston, Galveston, TX 77550-2772, USA

Theodore H. Bullock Department of Neurosciences A-OOl, University of California at San Diego, La Jolla, CA 92093-0201, USA

Catherine E. Carr Department of Zoology, University of Maryland, College Park, MD 20742, USA

IC.K. Chan Department of Neurophysiology. University of Wisconsin Medical School, Madison. WI 53706. USA

Jacob Christensen-Dalsgaard Institute of Biology, University of Odense, DK-5230 Odense M, Denmark

Jennifer A. Clack University of Cambridge, Museum of Zoology. Cambridge, CB2 3EJ, England, UK

xxxvii xxxviii Contributors

Alex M. Clark Department of Otolaryngology and Division of Biomedical Engineering, Medical College of Virginia, Virginia Commonwealth University, Richmond, VA 23298, USA

Sheryl Coombs Parmly Hearing Institute, Loyola University of Chicago, Chicago, IL 60626, USA

John D. Crawford Parmly Hearing Institute, Chicago, IL 60626, USA

Robert J. Dooling Department of Psychology, University of Maryland, College Park, MD 20742, USA

Peggy L. Edds Department of Zoology, University of Maryland, College Park, MD 20742, USA

Andreas Elapfandt Fakultiit fiir Biologie, Universitiit Konstan D-7750 Konstanz, FRG

Richard R. Fay Parmly Hearing Institute and Loyola University of Chicago, Chicago, IL 60626, USA

Bernd Fritzsch Creighton University, Department of Biomedical Sciences, Division of Anatomy, Omaha, NE 68178, USA

Shawn B. Frost Department of Psychology, Florida State University, Tallahassee, FL 32306, USA

James H. Fullard Department of Zoology, Erindale College, University of Toronto, Mississauga, Ontario, Canada

Z.M. Fuzessery Department of Zoology, University of Wyoming, Laramie, WY 82071, USA

Carl Gans Department of Biology, The University of Michigan, Ann Arbor, MI 48109, USA

Edmund Gerstein Mote Marine Laboratory, Sarasota, FL 33577, USA

Otto Gleich Institiit fiir Zoologie, Technische Universitiit Munchen, 8046 Garching, FRG

Steven Greenberg Department of Neurophysiology, University of Wisconsin, Wisconsin Medical School, Madi• son, WI 53706, USA

Henry E. Heffner Department of Psychology, University of Toledo, Toledo, OH 43606, USA Contributors xxxix

Rickye S. Heffner Department of Psychology, University of Toledo, Toledo, OR 43606, USA

Thomas E. Hetherington Department of Zoology, Ohio State University, Columbus, OR 43210-1293, USA

D.E. Hind Department of Neurophysiology, University of Wisconsin Medical School, Madison, WI 53706, USA

James A. Hopson Department of Anatomy, University of Chicago, Chicago, IL 60637, USA

Ronald R. Hoy Section of Neurobiology and Behavior, Cornell University, Ithaca, NY 14853, USA

John Janssen Department of Biology, Loyola University, Chicago, IL 60626, USA

Darlene R. Ketten Department of Otology and Laryngology, Harvard Medical School, Massachusetts Eye and Ear Infirmary, Boston, MA 02114, USA

Christine Koppl Institiit fiir Zoologie, Technische Universitiit Munchen, 8046 Garching, FRG

Martin L. Lenhardt Medical College of Virginia, Richmond, VA 23298-0168, USA

Edwin R. Lewis Department of Electrical Engineering and Computer Science, University of California, Ber• keley, CA 94720, USA

Brian Lewis Faculty of Life and Environmental Sciences, City of London Polytechnic, London EI 7NT, England, UK

Eric Lombard Department of Anatomy, University of Chicago, Chicago, IL 60637, USA

Selvakumaran Mahadaven Mote Marine Laboratory, Sarasota, FL 33577, USA

Geoffrey A. Manley Institut fiir Zoologie, Technische Universitiit Munchen, 8046 Garching, FRG

Andrew C. Mason Department of Biology, Erindale College, University of Toronto, Mississauga, Ontario, Canada, L5L 1C6

R. Bruce Masterton Department of Psychology, Florida State University, Tallahassee, FL 32306, USA xl Contributors

Catherine A. McCormick Department of Biology, Oberlin College, Oberlin, OR 44074, USA

Gloria E. Meredith Vrije Universiteit, Faculteit Der Geneeskunde, Laboratorium Voor Anatomie en Embryologie, 1007 MC Amsterdam, The Netherlands

Michael M. Merzenich Coleman Memorial Laboratory, University of California, San Francisco, CA 94143, USA

Axel Michelsen Institute of Biology, Odense University, DK 5230 Odense M, Denmark

Malcolm R. Miller Department of Anatomy, University of California, San Francisco, CA 94143, USA

John Montgomery Zoology Department, University of Auckland, Auckland, New Zealand

H.M. Muller Universitiit Bielefeld, Fakultiit fur Biologie, Lehrstuhl fur Neurophysiologie, 4800 Bielefeld, FRG

Alan D. Musicant Department of Neurophysiology, University of Wisconsin Medical School, Madison, WI 53706, USA

Peter M. Narins Department of Biology, University of California, Los Angeles, CA 90024, USA

U. Niemann Universitiit Bielefeld, Fakultiit fur Biologie, Lehrstuhl fur Neurophysiologie, 4800 Bielefeld, FRG

R. Glenn Northcutt Department of Neurosciences, A-OOl, University of California, San Diego, La Jolla, CA 92093, USA

Geoffrey W. Patton Mote Marine Laboratory, Sarasota, FL 33577, USA

Wolfgang Plassmann Fachbereich Biologie, IW. Goethe - Universitat Zoologie, 6000 Frankfurt am Main, FRG

Christopher Platt Program Director of Sensory Systems, National Science Foundation, Washington, D.C. 20550, USA

George D. Pollak Department of Zoology, University of Texas at Austin, Austin, TX 78712, USA Contributors xli

Arthur N. Popper Department of Zoology, University of Maryland, College Park, MD 20742, USA

William S. Rhode Department of Neurophysiology, University of Wisconsin, Madison, WI 53706, USA

Barry L. Roberts Department of Experimental Zoology, University of Amsterdam, 1098 SM Amsterdam, The Netherlands

Heiner Romer Ruhr-Universitat Bochum, Fakultat fur Biologie, Allg. Zoologie und Neurobiologie, D-4630 Bochum 1, FRG

John 1. Rosowski Eaton-Peabody Laboratory, Massachusetts Eye and Ear Infirmary, Boston, MA 02114, USA

Edwin W. Rubel Hearing Development Laboratories, University of Washington RL-30, Seattle, WA 98195, USA

Nico Schellart A.M., Laboratory of Medical Physics, University of Amsterdam, 1105 AZ Amsterdam, The Netherlands

Klaus Schildberger Department of Biology, Erindale College, University of Toronto, Mississauga, Ontario, Canada L5L 1C6

Christoff E. Schreiner Coleman Memorial Laboratory, University of California, San Francisco, CA 94143, USA

Michael G. Sneary Department of Electrical Engineering and Computer Science, University of California, Berkeley, CA 94720, USA

Mitchell S. Sommers Department of Psychology and Kresge Hearing Research Institute, University of Michigan, Ann Arbor, MI 48109-0506, USA

William C. Stebbins Department of Psychology and Kresge Hearing Research Institute, University of Michigan, Ann Arbor, MI 48109-0506, USA

William N. Tavolga Mote Marine Laboratory, Sarasota, FL 33577, USA

Christopher von Bartheld Hearing Development Laboratories, Department of Otolaryngology, RL-30, University of Washington, Seattle, WA 98195, USA xlii Contributors

Douglas B. Webster School of Medicine in New Orleans, Louisiana State University Medical Center, New Orleans, LA 70112-2234, USA

Molly Webster School of Medicine in New Orleans, Louisiana State University Medical Center, New Orleans, LA 70112-2234, USA

T.L.D. Williams Max-Planck Institiit fur Verhalttenphysiologie, D-8130 Seewiesen, FRG

Roddy Williamson The Marine Laboratory, Citadel Hill, Plymouth PLl 2PB, England, UK

Jayne E. Yack Department of Zoology, Erindale College, University of Toronto, Mississauga, Ontario, Canada L5L 1C6

William A. Yost Parmly Hearing Institute, Loyola University of Chicago, Chicago, IL 60626, USA Ernest Glen Wever: A Brief Biography and Bibliography

Richard R. Fay

1. Introduction degrees from Harvard University in 1924 and 1926. In 1928 he was married to Suzanne Rinehart. Wever taught Science at Roanoke, IL High The international symposium "Evolutionary Biol• School (1922-1923), and at Gunnery Preparatory ogy of Hearing" (May 20-24, 1990, Sarasota, FL), School in Washington, CT (1924-1925). After one and this volume are dedicated to Ernest Glen year as an instructor in Psychology at U.e. Ber• Wever. This brief biographical sketch and bibliog• keley (1926-1927), Wever was hired as an instruc• raphy were compiled for the participants of the tor of Psychology at Princeton University in 1927. meeting to introduce Glen Wever to younger scien• He was promoted to Assistant Professor in 1929, tists, and to document his contributions to the field and to Associate Professor in 1931. During 1936 to of the evolutionary biology of hearing. Scholars 1937, Wever worked on a fellowship at the Otolog• wishing to delve deeper into the history of Wever's ical Research Laboratory at Johns Hopkins Univer• scientific contributions should contact The Direc• sity with Stacy Guild and S.l Crowe. In 1941, he tor, Archives of the History of American Psychol• was promoted to Professor, and named the Dor• ogy, University of Akron, Ohio, where many of man T. Warren Professor (1946-1950), and the Wever's notes, books, and papers are collected. Eugene Higgins Professor (1950-1971). Wever Scholars wishing to study Wever's vast and well• was a consultant to the National Defense Research organized histological slide collection, primarily Committee on anti-submarine warfare during on the heads and ear regions of reptiles and World War II. He was a Research Associate at the amphibians, should contact the Division of Rep• Lempert Institute of Otology in New York (1947- tiles and Amphibians, U.S. National Museum of 1957) and served as Psychology Department Chair Natural History, the Smithsonian Institution, from 1955 to 1958. Washington, DC. Some carcasses are also con• Wever was elected to the National Academy of served for species identification. Additional tissue Sciences and the National Academy of Arts and from Wever's research collection can be found at Sciences, and was a fellow of the Acoustical Soci• the Carnegie Museum, Division of Amphibians ety of America and the Society of Experimental and Reptiles. Psychologists. He was a member of the American Psychological Association, the Association for Research in Otolaryngology, and the American 2. Biographical Sketch Otological Society. Wever had received the following honors: Ernest Glen Wever was born October 16, 1902 in Howard Crosby Warren Medal from the Society of Benton, IL, the son of Ernest Sylvester and Mary Experimental Psychologists (1931), the George Schurtz Wever. He received an A.B. degree from Shambaugh Prize in Otology (1957), The Gold Illinois College in 1922, and the MA and PhD Medal and Certificate of Merit from the American

xliii xliv Ernest Glen Wever: A Brief Biography and Bibliography

Otological Society (1959), Honors of the Associa• spatial code for frequency.) Wever and von Bekesy tion from the American Speech and Hearing Asso• became good friends during the '50s following a ciation (1967), The Beltone Institute for Hearing .period during which Wever was rather critical of Research Award (1969), and was the Guest of von Bekesy's work. Von Bekesy cherished the new Honor at the 104th meeting of the American Oto• friendship but regretted losing his most valuable logical Society (1971). In 1981 Wever received the critic when relations turned personally warm. Silver Medal in Psychological and Physiological Wever translated from the German and edited all Acoustics from the Acoustical Society of America, von Bekesy's papers published up to 1948 to pro• and in 1983 received the Award of Merit from the duce the book, Experiments in Hearing. This Association for Research in Otolaryngology. scholarship on Wever's part probably played a role Wever's first experiments were in vision where in von Bekesy's winning the 1961 Nobel Prize in the figure and ground distinctions (and other Physiology and Medicine. Wever also edited von Gestalt concepts) in perception were influential at Bekesy's last book, Sensory Inhibition. the time. This led to an interest in auditory mask• Wever had three or more careers in hearing ing, and to a valuable relationship with Wegel and research: 1) With Charles Bray and Merle Law• others at Bell Labs. rence, Wever discovered and further investigated During the late 1920s, Charles W. Bray returned of the cochlear potential, and used it as a tool to Princeton after a summer spent learning neu• for investigating the biomechanical function of rophysiology with Forbes at Harvard Medical the outer, middle, and inner ears. This work cul• School. Both Wever and Bray were interested in minated in Physiological Acoustics (E.G. Wever the problem of pitch perception and frequency rep• and Merle Lawrence, Princeton University Press, resentation in the nervous system, and their 1954). This book was a "bible" in its time, and experiments resulted in the discovery of the coch• nothing of its scope has been attempted since. 2) lear potential. With an electrode placed near the Wever reviewed, evaluated, and developed con• auditory nerve of the anesthetized cat and the temporary theories of hearing, including his well• potentials monitored using an audio system, Bray known "volley principle" which he combined with heard Wever's voice transduced by the hair cells of a place principle to account for frequency analysis the cat's ear. This resulted in the paper ''Auditory by the auditory system. This scholarly and theoret• nerve impulses" (Science, 1930, 71, p. 215, 191 ical work was published in his Theory ofHearing in words long), and the "Wever-Bray Effect:' This 1949. This book remains today the most ambi• was the beginning of cochlear electrophysiology. tious, complete, and well-written book on hearing. The general scientific response was strongly criti• 3) Wever founded, defined, and for several decades cal, and Wever and Bray spent the next few years maintained the modern field that is represented in eliminating possible artifacts. Wever had com• this volume, the evolutionary biology of hearing. It mented that Adrian visited the lab during this is clear from his bibliography that he was period and ': .. approved of everything he saw ... :' interested in evolutionary issues from the start I recall Wever telling me that the result he got (early '30s), and began studies on both vertebrates (faithful temporal encoding of the sound wave• and invertebrates. These interests in comparative form) was unexpected - his initial motivation for and evolutionary issues in hearing brought forth the experiment was to demonstrate that the evi• The Reptile Ear in 1978 and The Amphibian Ear in dence would not support the improbable "tele• 1985, both from Princeton University Press. These phone theory" of Rutherford. He expected to rule books are unparalleled treatises on the comparative out a temporal code for frequency. (I have always study of the ear. Wever's comparative work on found it interesting that von Bekesy related to me a hearing is responsible, directly or indirectly, for similar story about his experiments leading to the the careers of many of the contributors to this description of the traveling wave. He also got unex• volume, and probably for the fact that the National pected results - his initial motivation for the Institutes of Health, the National Science Founda• experiments was to demonstrate that a place• tion, and the Office of Naval Research (ONR) principal based on resonance could not operate in funds this sort of research. Wever had one of the the ear. He expected to rule out a Helmholtz-type first ONR grants. Ernest Glen Wever: A Brief Biography and Bibliography xlv

During the 1960s, Wever's comparative interests potentials of the cat's ear as an input to the tape came to dominate his work and thinking, and it is recorder, and various drills and chisels were used during this period many new investigators entered to illustrate the possibly damaging effects of the the field of hearing research and applied new noises they produced. This recording was kindly approaches and techniques. Wever didn't rush to the made available to me by Dr. William F. Strother, most modern of techniques (e.g. single fiber record• and has been transferred to cassette at Loyola ing, electron microscopy), and remained truly inter• University. Copies may be obtained from me. ested in evolutionary questions when many others During the 1970s, Wever delivered a series of studying diverse species were simply developing Langfeld Lectures at Princeton on the reptile ear "animal models" to study particular processes or which were video-recorded by Joseph Pylka of the structures. During this time, Wever seemed, to Department of Psychology. some, to be out of the "main stream" of auditory research which he dominated during the previous decades. With his help, the contributors to this vol• 3. Bibliography ume, and many others, are carrying on a vigorous new stream of comparative and evolutionary studies This bibliography is not a piece of historical on hearing. Glen Wever clearly takes his place as scholarship, and may contain errors of omission. In founder of the modern study of the evolutionary many cases, I included items from Wever's curricu• biology of hearing, and as an inspiration for all of us. lum vitae such as book reviews and notices of Some additional personal and professional infor• presentations that were apparently later published. mation about E.G. Wever, including photographs, I included these because Wever himself considered can be found in Hearing and Other Senses: Presen• them important, possibly for establishing a tations in Honor of E.G. ~aver, R. Fay and G. detailed chronology of ideas. Gourevitch (eds.), Amphora Press, Groton, CT, particularly in chapters by Frank Geldard, Lawry 1927 Wever EG: Figure and ground and the visual Gulick, Jim McCormick, Merle Lawrence, Jack perception of form. Am J Psychol 38:194- Vernon, and Bob Ruben. This volume presents 226. papers given at a conference in honor of Glen 1928 Wever EG: Attention and clearness in the Wever that George Courevitch and I organized in perception of figure and ground. Am J Phys• 1982 (May 16-18). The contributors were many of choI40:51-74. Wever's students and closest scientific friends. For 1928 Wever EG: The effect of a secondary tone that occasion, a video tape was made of Frank Gel• upon hearing. Science 67:612-613. dard interviewing Glen about his earliest years in 1928 Wever EG, Truman SR: The course of the research. This tape was shown at the meeting from auditory threshold in the presence of a tonal which this volume arose. background. J Exp Psychol 11: 98-112. In the 1950s, Wever delivered a brief lecture on 1928 Truman SR, Wever EG: The judgement of the stimulation of the ear caused by various surgical pitch as a function of the series. Univ Calif procedures used at that time that was tape-recorded. Publ Psychol 3:215-223. The first few sentences of this lecture follow: 1928 Wever EG, Zener C: The method of absolute judgement in psychophysics. Psychol Rev ''The following recording was made in the Auditory 35:466-493. Research Laboratories of Princeton University. Par• 1929 Wever EG: Beats and related phenomena ticipating in the work were Dr. L.E. Wolfson of Boston resulting from the simultaneous sounding of Massachusetts, Dr. George von Bekesy of Harvard two tones. Psychol Rev 36:402-418. University, and Drs. E.G. Wever, w.F. Strother, and 1929 Wever EG: High-speed lamps for tachisto• W.E. Rahm of Princeton University. The sounds that you will hear from now on were recorded through the ear of scopic work. J Gen PsychoI2:553-556. an anesthetized cat:' 1929 Zener KE, Wever EG: A multiple-choice apparatus. Am J PsychoI51:647-648. The lecture was delivered by Wever in one of the 1930 Wever EG: The upper limit of hearing in the surgical rooms at his laboratory, using the cochlear cat. J Comp PsychollO:221-233. xlvi Ernest Glen Wever: A Brief Biography and Bibliography

1930 Wever EG, Bray CW: Auditory nerve 1933 Wever EG, Bray CW: A new method for the impulses. Science 71:215. study of hearing in insects. J Cell Comp 1930 Wever EG, Bray CW: Action currents in the PhysioI4:79-93. auditory nerve in response to acoustical stim• 1934 Wever EG, Bray CW, Horton GP: The ulation. Proc Natl Acad Sci USA 16: problem of stimulation deafness as studied 344-350. by auditory nerve techniques. Science 80: 1930 Wever EG, Bray CW: The nature of acoustic 18-19. response: The relation between sound fre• 1935 Wever EG: A study of hearing in the sulphur• quency and frequency of impulses in the winged grasshopper (Arphia sulphurea). J auditory nerve. J Exp Psychol13:373-387. Comp Psychol20: 17-20. 1930 Wever EG, Bray CW: Present possibilities 1935 Wever EG: Book review: Freeman GL for auditory theory. Psychol Rev 37:365- Introduction to Physiological Psychology. 380. Psychol Bull 32:310-313. 1930 Wever EG, Bray CW: Action currents in the 1935 Wever EG: Book review: Stewart GW auditory nerve in response to acoustical Introductory Acoustics. Psychol Bull 32: stimulation; experiments demonstrating the 102-104. correspondence between sound and nerve 1935 Wever EG: Audition. In EG Boring, HS impulse. Paper read before the National Langfeld and HP Weld Psychology, A Factual Academy of Sciences, April 28, 1930. Textbook. Wiley, New York, pp 102-139 Abstracted in Science, 193071:515- 516. (Chapter 5). 1930 Robinson EW, Wever EG: Visual distance 1935 Wever EG, Bray CW, Horton GP: Tone perception in the rat. Univ CalifPubl Psychol localization in the cochlea. Ann Otol Rhinol 4:233-239. LaryngoI44:772-776. 1931 Wever EG: Impulses from the acoustic nerve 1936 Wever EG, Bray CW: The nature of acoustic of the guinea pig rabbit and rat. Am J Psychol response: the relation between sound inten• 43:457-462. sity and the magnitude of responses in the 1931 Wever EG: Auditory nerve experiments in cochlea. J Exp PsychoI19:129-143. animals and their relation to hearing. Laryn• 1936 Wever EG, Bray CW: Hearing in the pigeon goscope 41:387-391. as studied by the electrical responses of the 1931 Wever EG, Bray CW: Auditory nerve inner ear. J Comp PsychoI22:353-363. responses in the reptile. Acta Otolaryngol 1936 Wever EG, Bray CW: The nature of bone 16:154-159. conduction as shown in the electrical 1932 Wever EG: Water temperature as an incen• response of the cochlea. Ann Otol Rhinol tive to swimming activity in the rat. J Comp LaryngoI45:822-530. Psychol 14:219-224. 1937 Wever EG, Bray CW, Willey CF: The 1932 Wever EG, Bray CW: Kreezer and Darge on response of the cochlea to tones of low fre• auditory action currents. Science 75:267. quency. J Exp PsychoI20:336-349. 1932 Wever EG, Bray CW: A note on ''A neglected 1937 Wever EG, Bray CW: The tensor tympani possibility in frequency theories of hearing." muscle and its relation to sound conduction. Am J PsychoI44:192-193. Ann Otol Rhinol Laryngol 46:947-961. 1932 Wever EG, Bray CW: Auditory nerve 1937 Wever EG, Bray CW: A comparative study of responses and auditory theory. Paper read at the electrical response of the ear. Proc Am meeting of the Acoust Soc Am, May 3, 1932. Phil Soc 78:407-410. J Acoust Soc Amer 4: 10. 1937 Wever EG, Bray CW: The perception of low 1933 Wever EG, Bray CW: Auditory sensitivity of tones and the resonance-volley theory. J Psy• katydids and crickets. Paper read at NY choI3:101-114. Branch APA, Yale University, April 1 , 1933. 1937 Wever EG, Bray CW: A discussion of Ruck• Abstracted in Psychol Bull 30:548. mick's critical review of audition. Psychol 1933 Wever EG: The physiology of hearing: The Bull 34:39-43. nature of response in the cochlea. Physiol 1937 Wever EG, Bray CW: The effects of chemical Rev 13:400-425. substances upon the electrical response Ernest Glen Wever: A Brief Biography and Bibliography xlvii

of the cochlea I The application of sodium 1942 Wever EG, Bray CW: The stapedius muscle chloride to the round window membrane. in relation to sound conduction. J Exp Psy• Ann Otol Rhinol LaryngoI46:291-302. choI31:35-43. 1937 McCrady E Jr, Wever EG, Bray CW: The 1944 Wever EG, Smith KR: The problem of stimu• development of hearing in the opossum. J lation deafness; I cochlear impairments as a Exp Zool 75:503-517. function of tonal frequency. J Exp Psychol 1938 Wever EG: The width of the basilar mem• 34:239-245. brane in man. Ann Otol Rhinol Laryngol 1946 Wever EG: Audition: In JM Luck and VE 47:37-47. Hall (eds) Annual Review of Physiology 1938 Wever EG, Bray CW: Distortion in the ear as 8:447-450. shown by the electrical responses of the 1946 Wever EG: The acoustic characteristics of cochlea. J Acoust Soc Am 9:227-233. the ear In Harriman L et al Twentieth Century 1938 Wever EG, Bray CW: The nature of acoustic Psychology: Recent Developments in Psychol• response: the relation between stimulus ogy New York Philosophical Library Inc pp intensity and the magnitude of cochlear 371-386. responses in the cat. J Exp Psychol 22: 1-16. 1947 Wever EG, NeffWD: A further study of the 1939 Wever EG: The electrical responses of the effects of partial section of the auditory ear. Psychol Bull 36: 143-187. nerve. J Comp Physiol PsychoI40:217-226. 1940 Wever EG, Bray CW, Lawrence M: A quan• 1947 Lempert J, Wever EG, Lawrence M: The titative study of combination tones. J Exp cochleogram and its clinical applications; a PsychoI27:469-496. preliminary report. Arch Otolaryngol 45: 1940 Wever EG, Bray CW, Lawrence M: The ori• 61-67. gin of combination tones. J Exp Psychol 1948 Wever EG, Lawrence M, Smith KR: The 27:217-226. effects of negative air pressure in the middle 1940 Wever EG, Bray CW, Lawrence M: The ear. Ann Otol Rhinol Laryngol 57:418-528. locus of distortion in the ear. J Acoust Soc 1948 Wever EG, Lawrence M: The functions of Am 11:427-433. the round window. Ann Otol Rhinol Laryn• 1940 Wever EG, Bray CW, Lawrence M: The goI57:579-589. interference of tones in the cochlea. J Acoust 1948 Wever EG, Lawrence M, Smith KR: The Soc Am 12:268-280. middle ear in sound conduction. Arch 1940 McCrady E, Wever EG, Bray CW: A further Otolaryngol48: 19-35. investigation of the development of hearing 1949 Wever EG: Theory of Hearing. New York: in the opossum. J Comp Psychol 30:17-21. Wiley. 1941 Wever EG: The designation of combination 1949 Wever EG, Lawrence M: The patterns of tones Psychol Rev 48:93-104. response in the cochlea. J Acoust Soc Am 1941 Wever EG, Bray CW, Lawrence M: The 21:127-134. effect of middle ear pressure upon distortion. 1949 Wever EG, Lawrence M, Hemphill RW, J Acoust Soc Am 13: 1892-187. Straut CB: Effects of oxygen deprivation 1941 Wever EG, Bray CW, Lawrence M: The upon the cochlear potentials. Am J Physiol nature of cochlear activity after death. Ann 159: 199-208. Otol Rhinol LaryngoI50:317-329. 1949 Lempert J, Wever EG, Lawrence M, Meltzer 1941 Wever EG, Lawrence M: Tonal interference PE: Perilymph: Its relation to the improve• in relation to cochlear injury. J Exp Psychol ment of hearing which follows fenestration of 29:283-295. the vestibular labyrinth in clinical otosclero• 1941 Wever EG, Wedell CH: Pitch discrimination sis. Arch OtolaryngoI50:377-387. at high frequencies. Psychol Bull 38:727. 1949 Smith KR, Wever EG: The problems of 1942 Wever EG: The problem of the tonal dip. stimulation deafness III. The functional and Laryngoscope 52: 169-187. histological effects of a high-frequency 1942 Wever EG, Bray CW, Lawrence M: The stimulus. J Exp Psychol 39:238-241. effects of pressure in the middle ear. J Exp 1950 Wever EG: Recent investigations of sound Psychol 30:40-52. conduction II. The ear with conductive xlviii Ernest Glen Wever: A Brief Biography and Bibliography

impairment. Paper presented to meeting of ogy of Me~re's disease. Ann Otol Rhinol Amer Otol Soc May 21, 1950. Ann Otol Otolaryngol 61 :717-737. Rhinol and Otolaryngol 59: 1037-1061. 1953 Wever EG, Lawrence M: Auditory theory: 1950 Wever EG: [A review of progress during the An experimental study of the place principle. period June 1949-June 1950] In CP Stone Bull NY Acad Med 29:159-163. and DW Taylor (eds) Annual Review of Psy• 1954 Wever EG, Lawrence M, Rahm WE Jr: The chology 2:65-75. phase characteristics of the ear. Proc Nat! 1950 Wever EO: Review: Meyer MF How M Acad Sci USA 40:209-218. Hear; How Tones Make Music. Amer J Psy• 1954 Wever EG, Lawrence M: Physiological chol 64:625-626. Acoustics. Princeton, New Jersey: Princeton 1950 Wever EG, Lawrence M: The acoustic path• University Press. ways to the cochlea. J Acoust Soc Am 22: 1954 Wever EG, Lawrence M, von Bekesy G: A 460-467. note on recent developments in auditory the• 1950 Wever EG, Lawrence M: The transmission ory. Proc Nat! Acad Sci USA 40:508-512. properties of the middle ear. Ann Otol Rhinol 1954 Lempert J, Wever EG, Lawrence M: Are the LaryngoI59:5-18. membranous walls of the endolymphatic 1950 Wever EG, Lawrence M: The transmission labyrinth permeable? Trans Am Acad Opthal properties of the stapes. Ann Otol Rhinol Otolaryngol 58:460-465 (Also in Acta LaryngoI59:322-330. Otolaryngol Suppl 116: 182-188). 1950 Lawrence M, Wever EG: Recent investiga• 1955 Wever EG: Sound conduction in the ear. tions of sound conduction Part I: The normal Paper presented at ONR Symposium Pensa• ear; Part 2: The ear with conductive impair• cola, FL March 10-11, 1955, Published in ment. Ann Otol Rhinol Laryngol 59: 1020- proceedings: Symposium on Physiological 1062. Psychology ONR Symposium Report ACR- 1950 Lempert J, Meltzer PE, Wever EG, Law• 1:202-214. rence M: The cochleogram and its clinical 1955 Wever EG: Book review: Helmholtz H On applications; concluding observations. Arch the Sensations of Tone. New York: Dover Otolaryngol 51: 307 - 311. (1954 reprinting). Scientific Monthly 81: 1951 Wever EG: Some remarks on the modem sta• 256. tus of auditory theory. J Acoust Soc Am 1955 Wever EG: Book review: SS Stevens, JGC 23:287-289. Loring and D Cohen (eds) Bibliography on 1952 Wever EG: Chapters 25, 26, 27, 28 in Hearing Cambridge: Harvard University Stevens SS Handbook of Experimental Psy• Press. Science 122:380. chology.Am J PsychoI65:130-132. 1955 Wever EG: Book Review: On the Sensations 1952 Wever EG, Lawrence M: The place principle of Tone as a Physiological Basis for the The• in auditory theory. Proc Natl Acad Sci USA ory of Music. The Scientific Monthly 81. 38: 133-138. 1955 Wever EG, Lawrence M: Patterns of injury 1952 Wever EG, Lawrence M: Sound conduction produced by overstimulation of the ear. J in the cochlea. Ann Otol Rhinol Laryngol Acoust Soc Am 27:853-858. 61:824. 1955 Wever EG, Vernon JA: The effects of the 1952 Lawrence M, Wever EG: Effects of oxygen tympanic muscle reflexes upon sound trans• depriVation upon the structure of the organ of mission. Acta OtolaryngoI45:433-439. corti. Arch OtolaryngoI55:31-37. 1955 Wever EG, Vernon JA, Lawrence M: The 1952 Lempert J, Meltzer PE, Wever EG, Law• maximum strength of the tympanic muscles. rence M, Rambo JHT: Structure and func• Ann Otol Rhinol Otolaryngol 64:383-391. tion of the cochlear aqueduct. Arch Oto• 1955 Wever EG, Vernon JA: The threshold sensi- laryngoI55:134-145. tivity of the tympanic muscle reflexes. Arch 1952 Lempert J, Wolff D, Rambo J, Wever EG, OtolaryngoI62:204-213. Lawrence M: New theory for the correlation 1956 Wever EG, Lempert J, Meltzer PE, Rambo of the pathology and the symptomatol- JHT: The effectS of injury to the lateral semi- Ernest Glen Wever: A Brief Biography and Bibliography il

circular canal. Trans Amer Acad Ophthalmol mechanisms of the bat's ear. Ann Otol Rhinol Otolaryngol Sept-Oct 718. LaryngoI70:5-18. 1956 Wever EG, Vernon JA: The Sensitivity of 1961 Wever EG, Vernon JA: Hearing in the bat the turtle's ear as shown by its electrical Myotis lucifugus as shown by the cochlear potentials. Proc Natl Acad Sci USA 42:213- potentials. J Aud Res 2:158-175. 220. 1961 Wever EG, Vernon JA: Cochlear potentials in 1956 Wever EG, Vernon JA: Sound transmission in the marmoset. Proc Natl Acad Sci USA the turtle's ear. Proc Natl Acad Sci USA 47:739-741. 42:292-299. 1961 B6k6sy G von, Wever EG, Rahm WE Jr, 1956 Wever EG, Vernon JA: The control of sound Rambo JHT: A new method of perfusion for transmission by the middle ear muscles. Ann the fixation of tissues. Laryngoscope 71: Otol Rhinol Laryngol 65:5. 1534-1547. 1956 Wever EG, Vernon JA: Auditory responses in 1962 Wever EG: The transmission of sound in the the common box turtle. Proc Natl Acad Sci ear. Henry Ford Hospital International Sym• USA 42:962-965. posium: Otosclerosis. Boston: Little Brown 1957 Wever EG, Vernon JA: Auditory responses in and Company, pp 139-152. the spectacled caiman. J Cell Comp Physiol 1962 Wever EG: Development of traveling-wave 50:333-339. theories. J Acoust Soc Am 34:1319-1324. 1957 Wever EG, Vernon JA: The auditory sensitiv• 1962 Wever EG: Hearing. In: Farnsworth PR (ed) ity of the atlantic grasshopper. Proc Nat! Annu Rev Psychol13:225-150. Acad Sci USA 43:346-348. 1963 Wever EG, Crowley DE, Peterson EA: Audi• 1958 Wever EG, Vernon JA: Auditory responses in tory sensitivity in four species of lizards. J reptiles. Symposium Proceedings, Office of Aud Res 3:151-157. Naval Research Pensacola, Florida, March 1963 Wever EG, Peterson EA: Auditory sensitiv• 191-196. ity in three iguanid lizards. J Aud Res 3: 1958 Wever EG, Vernon JA, Lawrence M: The 205-212. nature of the cochlear potentials in the mon• 1963 Wever EG, Vernon JA, Peterson EA: The key. Acta otolaryngol 49:38-49. high-frequency sensitivity of the guinea pig 1958 Wever EG, Vernon JA, Rahm WE, Strother ear. Proc Nat! Acad Sci USA 49:319-322. WF: Cochlear potentials in the cat in 1963 Wever EG, Vernon JA, Peterson EA, Crow• response to high-frequency sounds. Proc ley DE: Auditory responses in the tokay Natl Acad Sci USA 44:1087-1090. gecko. Proc Nat! Acad Sci USA 50: 806-811. 1959 Wever EG: The cochlear potentials and their 1964 Wever EG: The physiology of the peripheral relation to hearing. Ann Otol Rhinol Laryn• hearing mechanism. In: Fields WS and Alford goI68:975-989. BR (eds) Neurological Aspects ofAuditory and 1959 Wever EG, Rahm WE Jr, Strother WF: The Vestibular Disorders Springfield, IL: Charles lower range of the cochlear potential. Proc C. Thomas. Chapter 2, pp 24-50. Natl Acad Sci USA 45:1447-1449. 1964 Wever EG, Peterson EA, Crowley DE, Ver• 1959 Wever EG, Vernon JA: The auditory sensitiv• non JA: Further studies of hearing in the gek• ity of orthoptera. Proc Nat! Acad Sci USA konid lizards. Proc Nat! Acad Sci USA 45:413-419. 51:561-567. 1960 Wever EG: Translator and editor, Bekesy G 1965 Wever EG: The degenerative processes in the von Experiments in Hearing New York: ear of the shaker mouse. Ann Otol Rhinol McGraw-Hill. LaryngoI74:5-2l. 1960 Wever EG, Vernon JA: The problem of hear• 1965 Wever EG: Structure and function ofthe liz• ing in snakes. J Aud Res 1:77-83. ard ear. J Aud Res 5:331-37l. 1961 Wever EG: The physiological basis of musi• 1965 Wever EG, Vernon JA, Crowley DE, Peter• cal hearing. International Musical Society son EA: The electrical output of the lizard Report I 133-138. ear. Relation to hair-cell population. Science 1961 Wever EG, Vernon JA: The protective 150:1172-1174. Ernest Glen Wever: A Brief Biography and Bibliography

1966 Wever EG: Electrical potentials of the coch• sea turtle Chelonia mydas. Proc Nat! Acad lea. Physiological Rev 46: 102-127. Sci USA 64:884-890. 1966 Wever EG, Hepp-Reymond MC, Vernon JA: 1970 Wever EG: The Lizard Ear: Cordylus platy• Vocalization and hearing in the leopard liz• saurus and gerrhosaurus. J Morph 130: ard. Proc Natl Acad Sci USA 55:98-106. 37-56. 1966 Vernon JA, Dalland 11, Wever EG: Further 1970 Wever EG: The lizard ear: Scincidae. J studies of hearing in the bat Myotis lucifugus Morph 132:277-292. by means of cochlear potentials. J Aud Res 1970 Wever EG, Werner YL: The function of the 6:153-163. middle ear in lizards: Crotaphytus col/aris 1967 Wever EG: The tectorial membrane of (Iguanidae). J Exp ZooI175:327-342. the lizard ear: Types of structure. J Morphol 1970 McCormick JG, Wever EG, Palin J, Ridgway 122:307-320. SH: Sound conduction in the dolphin ear. J 1967 Wever EG: The tectorial membrane of Acoust Soc Am 48:1418-1428. the lizard ear: species variations. J Morphol 1971 Wever EG: Hearing in the crocodilia. Proc 123:355-372. Nat Acad Sci 68: 1498-1500. 1967 Wever EG: Tonal differentiation in the lizard 1971 Wever EG: The lizard ear: Anguidae. J Aud ear. Laryngoscope 77: 1962-1973. Res 11:160-172. 1967 Wever EG: Editor: Bekesy G von Sensory 1971 Wever EG: The ear of Basiliscus (Sauria: Inhibition. Princeton, NJ: Princeton Univ Iguanidae); Its structure and function. Press. Copeia 1:139-144. 1967 Wever EG, Hepp-Reymond MC: Auditory 1971 Wever EG: The mechanics of hair-cell stim• sensitivity in the fan-toed gecko Ptyodactylus ulation. Ann Otol Rhinol Laryngol 80:786- hasselquistii puiseuxi Boutan. Proc Natl 804. Acad Sci USA 57:681-687. 1971 Wever EG: Modes of stimulation of hair 1968 Wever EG: Phonoreception. In: Encyclope• cells. In: Sachs MB (ed) Physiology of the dia of Science 3rd ed. New York: McGraw• Auditory System. Baltimore: National Edu• Hill, pp. 141-145. cational Consultants, pp 55-56. 1968 Wever EG: The lacertid ear: Eremias argus. 1971 Wever EG, McCormick JG, Palin J, Ridgway Proc Natl Acad Sci USA 61:1292-1299. SH: The cochlea of the dolphin Tursiops trun• 1968 Wever EG: The ear of the chameleon: catus: General morphology. Proc Natl Acad Chamaeleo senegalensis and Chamaeleo Sci USA 68:2381-2385. quilensis. J Exp Zool 168:423-436. 1971 Wever EG, McCormick JG, Palin J, Ridgway 1968 Wever EG, Herman PH: Stridulation and SH: Cochlea of the dolphin Tursiops trunca• hearing in the tenrec Hemicentetes semi• tus: The basilar membrane. Proc Nat! Acad spinosus. J Aud Res 8:39-42. Sci USA 68:2708-2711. 1969 Wever EG: The ear of the chameleon: The 1971 Wever EG, McCormick JG, Palin J, Ridgway round window problem. J Exp Zool 171: 1-6. SH: The cochlea of the dolphin Tursiops trun• 1969 The ear of the chameleon: Chamaeleo hoh• catus: Hair cells and ganglion cells. Proc nelii and Chamaeleo jacksoni. J Exp Zool Nat! Acad Sci USA 68:2908-2912. 171 :305-312. 1971 Simmons JA, Wever EG, Pylka JM: Periodi• 1969 Wever EG: Cochlear stimulation and lem• cal cicada: sound production and hearing. pert's mobilization theory. Arch Otolaryngol Science 171:212-213. 90:68-73. 1971 Pylka JM, Simmons JA, Wever EG: Sound 1969 Wever EG, Herman PN, Simmons JA, Hert• production and hearing in the rattlesnake. zler DR: Hearing in the blackfooted penguin Paper presented at meeting of AAAS Phila• Spheniscus demersus as represented by the delphia, PA Dec 26-31, 1971. Abstracted in cochlear potentials. Proc Nat! Acad Sci USA Herpetol Rev 1972 3: 107. 63:676-680. 1972 Wever EG, Gans C: The ear and hearing 1969 Ridgway SH, Wever EG, McCormick JG, in Bipes biporus (Amphisbaenia: Reptilia). Palin J, Anderson JH: Hearing in the giant Proc Nat! Acad Sci USA 69:2714-2716. Ernest Glen Wever: A Brief Biography and Bibliography Ii

1972 Wever EG, McCormick JG, Palin J, Ridgway 1974 Wever EG: Sound reception. In Encyclopedia SH: Cochlear structure in the dolphin Lage• Britannica, 15th edition 39-51. norhynchus obliquidens. Proc Nat! Sci Acad 1974 Gans C, Wever EG: Temperature effects on USA 69:657-661. hearing in two species of Amphisbaenia 1972 Gans C, Wever EG: The ear and hearing in (Squamata Reptilia). Nature 250:79-80. amphisbaenia (Reptilia). J Exp Zool 179: 1974 Ridgway SH, McCormick JG, Wever EG: 17-34. Surgical approach to the dolphin's ear. J Exp 1972 Werner YL, Wever EG: The function of the Zool 188:265-276. middle ear in lizards: Gekko gecko and Euble• 1975 Wever EG: The caecilian ear. J Exp Zool pharis macularius (Gekkonoidea). J Exp 191:63-72. ZooI179:1-16. 1975 Gans C, Wever EG: The amphisbaenian ear: 1973 Wever EG: The labyrinthine sense organs of Blanus cinerus and Diplometopon zarudnyi. the frog. Proc Natl Acad Sci USA 70: Proc Nat! Acad Sci USA 72:1487-1490. 498-502. 1976 Wever EG: Origin and evolution of the ear of 1973 Wever EG: Closure muscles of the external vertebrates. In: Masterson RB, Bitterman auditory meatus in gekkonidae. J Herpetol ME, Campbell CBG and Hotton N (eds) Evo• 7:323-329. lution of Brain and Behavior in Vertebrates 1973 Wever EG: The function of the middle ear in Hillsdale, NJ: Lawrence Erlbaum Assoc. lizards: Eumeces and Mabuya (Scincidae). J 1976 Wever EG, Gans C: The caecilian ear. Fur• Exp ZooI183:225-240. ther observations. Proc Nat! Acad Sci USA 1973 Wever EG: The function ofthe middle ear in 73:3744-3746. lizards: Divergent types. J Exp Zool 1976 Gans C, Wever EG: Ear and hearing in 184:97-126. Sphenodon punctatus. Proc Nat! Acad Sci 1973 Wever EG: Tectorial reticulum of the USA 73:4244-4246. labyrinthine endings of vertebrates. Ann Otol 1978 Wever EG: Sound transmission in the Rhinol Laryngol 82:277-289. salamander ear. Proc Nat! Acad Sci USA 1973 Wever EG, Gans C: The ear in amphisbaenia 75:529-530. (Reptilia); further anatomical observations. J 1978 Wever EG: The Reptile Ear. Princeton, NJ: Zool 171: 189-206. Princeton University Press. 1973 Wever EG: The ear and hearing in the frog 1979 Wever EG: Middle ear muscles of the frog. Ranapipiens. J Morph 141:461-478. Proc Nat! Acad Sci USA 76:3031-3033. 1974 Wever EG: The Ear of Lialis burtonis 1980 McCormick JG, Wever EG, Ridgeway SH, (Sauria: Pygopodidae), its structure and Palin J: Sound reception in the porpoise as it function. Copeia 2:297-305. relates to echolocation. In: Busnel RG (ed) 1974 Wever EG: The lizards ear: Gekkonidae. J Animal Sonar Systems Symposium New York: Morph 143:121-166. Plenum Press, pp 449-467. 1974 Wever EG: The evolution of vertebrate hear• 1981 Wever EG: The role of the amphibians in the ing. In: Keidel WD and NeffWD (eds) Hand• evolution of the vertebrate ear. Am J book of Sensory Physiology Vol V-J Auditory Otolaryngol 2: 145-152. System New York: Springer-Verlag, pp 1985 Wever EG: The Amphibian Ear Princeton, 423-454. NJ: Princeton University Press.