Springer Handbook of Auditory Research

Series Editors: Richard R. Fay and Arthur N. Popper

Springer Handbook of Auditory Research

Volume 1: The Mammalian Auditory Pathway: NeuroanatomyEdited by Douglas B. Webster, Arthur N. Popper, and Richard R. Fay

Volume 2: The Mammalian Auditory Pathway: NeurophysiologyEdited by Arthur N. Popper and Richard R. Fay

Volume 3: Human PsychophysicsEdited by William Yost, Arthur N. Popper, and Richard R. Fay

Volume 4: Comparative Hearing: MammalsEdited by Richard R. Fay and Arthur N. Popper

Volume 5: Hearing by BatsEdited by Arthur N. Popper and Richard R. Fay

Volume 6: Auditory ComputationEdited by Harold L. Hawkins, Teresa A. McMullen, Arthur N. Popper, and Richard R. Fay

Volume 7: Clinical Aspects of HearingEdited by Thomas R. Van De Water, Arthur N. Popper, and Richard R. Fay

Volume 8: The CochleaEdited by Peter Dallos, Arthur N. Popper, and Richard R. Fay

Volume 9: Development of the Auditory SystemEdited by Edwin W Rubel, Arthur N. Popper, and Richard R. Fay

Volume 10: Comparative Hearing: InsectsEdited by Ronald Hoy, Arthur N. Popper, and Richard R. Fay

Volume 11: Comparative Hearing: Fish and AmphibiansEdited by Richard R. Fay and Arthur N. Popper

Volume 12: Hearing by Whales and DolphinsEdited by Whitlow W.L. Au, Arthur N. Popper, and Richard R. Fay

Volume 13: Comparative Hearing: Birds and ReptilesEdited by Robert Dooling, Arthur N. Popper, and Richard R. Fay

Volume 14: Genetics and Auditory DisordersEdited by Bronya J.B. Keats, Arthur N. Popper, and Richard R. Fay

Volume 15: Integrative Functions in the Mammalian Auditory PathwayEdited by Donata Oertel, Richard R. Fay, and Arthur N. Popper

Volume 16: Acoustic CommunicationEdited by Andrea Simmons, Arthur N. Popper, and Richard R. Fay

Volume 17: Compression: From Cochlea to Cochlear ImplantsEdited by Sid P. Bacon, Richard R. Fay, and Arthur N. Popper

Volume 18: Speech Processing in the Auditory SystemEdited by Steven Greenberg, William Ainsworth, Arthur N. Popper, and Richard R. Fay

Volume 19: The Vestibular SystemEdited by Stephen M. Highstein, Richard R. Fay, and Arthur N. Popper

Volume 20: Cochlear Implants: Auditory Prostheses and Electric HearingEdited by Fan-Gang Zeng, Arthur N. Popper, and Richard R. Fay

Volume 21: ElectroreceptionEdited by Theodore H. Bullock, Carl D. Hopkins, Arthur N. Popper, and Richard R. Fay

Continued after index

Jochen SchachtArthur N. PopperRichard R. FayEditors

Auditory Trauma, Protection,and Repair

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EditorsJochen Schacht Arthur N. PopperKresge Hearing Research Institute Department of BiologyUniversity of Michigan University of MarylandAnn Arbor, MI 48109 College Park, MD 20742USA USAschacht@umich.edu apopper@umd.edu

Richard R. FayParmly Hearing Institute6525 North Sheridan RoadLoyola University ChicagoChicago, IL 60626USArfay@luc.edu

Series EditorsRichard R. Fay Arthur N. PopperParmly Hearing Institute and Department of Biology

Department of Psychology University of MarylandLoyola University Chicago College Park, MD 20742Chicago, IL 60626 USAUSA

ISBN: 978-0-387-72560-4 e-ISBN: 978-0-387-72561-1

Library of Congress Control Number: 2007926238

© 2008 Springer Science+Business Media, LLCAll rights reserved. This work may not be translated or copied in whole or in part without the writtenpermission of the publisher (Springer Science+Business Media, LLC, 233 Spring Street, New York,NY 10013, USA), except for brief excerpts in connection with reviews or scholarly analysis. Usein connection with any form of information storage and retrieval, electronic adaptation, computersoftware, or by similar or dissimilar methodology now known or hereafter developed is forbidden.The use in this publication of trade names, trademarks, service marks and similar terms, even ifthey are not identified as such, is not to be taken as an expression of opinion as to whether or notthey are subject to proprietary rights.

Cover illustration: This image is Figure 8.2 from the text.

Printed on acid-free paper

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Dedication

This volume is dedicated to Professor Joseph Elmer Hawkins, Jr., scholar,educator, and oto-historian, in recognition of his lifelong contributions to theanatomy and pathology of the auditory system. Every chapter of this book reflectshis influence as a scientist and mentor.

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Contents

Contributors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ix

Series Preface . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . xiii

Volume Preface . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . xv

1. Auditory Pathology: When Hearing Is Out of Balance . . . . . . . . . . . . . . . 1Jochen Schacht

2. Genetics of Hearing Loss . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9Ella Shalit and Karen B. Avraham

3. Cochlear Homeostasis and Homeostatic Disorders . . . . . . . . . . . . . . . . . . . 49Philine Wangemann

4. Tinnitus: Theories, Mechanisms, and Treatments . . . . . . . . . . . . . . . . . . . . 101Carol A. Bauer and Thomas J. Brozoski

5. Autoimmune Inner Ear Disease . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 131Quinton Gopen and Jeffrey P. Harris

6. Age-Related Hearing Loss and Its Cellular and Molecular Bases . . . . . .145Kevin K. Ohlemiller and Robert D. Frisina

7. Patterns and Mechanisms of Noise-Induced Cochlear Pathology . . . . . . 195Donald Henderson, Bohua Hu, and Eric Bielefeld

8. Drug-Induced Hearing Loss . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 219Leonard P. Rybak, Andra E. Talaska, and Jochen Schacht

9. Central Consequences of Cochlear Trauma . . . . . . . . . . . . . . . . . . . . . . . . . 257D. Kent Morest and Steven J. Potashner

10. Cell Death and Cochlear Protection . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 275Steven H. Green, Richard A. Altschuler, and Josef M. Miller

11. Emerging Strategies for Restoring the Cochlea . . . . . . . . . . . . . . . . . . . . . . 321Stefan Heller and Yehoash Raphael

Index. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .339

vii

Contributors

richard a. altschuler

Kresge Hearing Research Institute, Department of Otolaryngology, Universityof Michigan, Ann Arbor, MI 48109-0506, USA, Email: shuler@umich.edu

karen b. avraham

Department of Human Molecular Genetics and Biochemistry, Sackler Schoolof Medicine, Tel Aviv University, Tel Aviv 69978 Israel, Email: karena@post.tau.ac.il

carol a. bauer

Southern Illinois University School of Medicine, Department of Surgery,Springfield, IL 62794-9662, USA, Email: cbauer@siumed.edu

eric bielefeld

Center for Hearing & Deafness, SUNY at Buffalo, Buffalo, NY 14214, USA,Email: ecb2@buffalo.edu

thomas j. brozoski

Southern Illinois University School of Medicine, Department of Surgery,Springfield, IL 62794-9629, USA, Email: tbrozoski@siumed.edu

robert d. frisina

Otolaryngology Department, University Rochester School of Medicineand Dentistry, Rochester NY, 14642-8629, USA, Email: Robert_Frisina@urmc.rochester.edu

quinton gopen

Division of Otology and Laryngology, Harvard Medical School, Children’sHospital Boston, Brigham and Women’s Hospital, Boston, MA 02115, USA,Email: quinton.gopen@childrens.harvard.edu

steven green

Department of Biological Sciences, University of Iowa, Iowa City, IA 52242-1324, USA, Email: steven-green@uiowa.edu

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x Contributors

jeffrey p. harris

Division of Otolaryngology-Head and Neck Surgery,University of CaliforniaSan Diego Medical Center, La Jolla, CA 92037, USA, Email: jpharris@ucsd.edu

stefan heller

Departments of Otolaryngology/HNS and Molecular & Cellular Physiology,Stanford University School of Medicine, Stanford, CA 94305, USA, Email:Hellers@stanford.edu

donald henderson

Center for Hearing & Deafness, SUNY at Buffalo, Buffalo, NY 14214, USA,Email:donaldhe@acsu.buffalo.edu

bohua hu

Center for Hearing & Deafness, SUNY at Buffalo, Buffalo, NY 14214, USA,Email: bhu@buffalo.edu

josef m. miller

Kresge Hearing Research Institute, Department of Otolaryngology, Universityof Michigan, Ann Arbor, MI 48109-0506, USA, Email: josef@umich.edu

d. kent morest

University of Connecticut Medical Center, Department of Neuroscience,Farmington, CT 06030-3401, USA, Email: kentmorest@neuron.uchc.edu

kevin k. ohlemiller

Department of Otolaryngology, Central Institute for the Deaf at WashingtonUniversity Medical School, St. Louis, MO 63110-1010, USA, Email:kohlemiller@wustl.edu

steven j. potashner

University of Connecticut Medical Center, Department of Neuroscience,Farmington, CT 06030-3401, USA, Email: SJP9713@neuron.uchc.edu

yehoash raphael

Kresge Hearing Research Institute, University of Michigan, Ann Arbor, MI48109-0506, USA, Email: yoash@umich.edu

leonard p. rybak

Southern Illinois University School of Medicine, Department of Surgery/Otolaryngology, Springfield, IL 62794-9653, USA, Email: lrybak@siumed.edu

Contributors xi

jochen schacht

Kresge Hearing Research Institute, University of Michigan, Ann Arbor, MI48109-0506, USA, Email: schacht@umich.edu

ella shalit

Department of Human Molecular Genetics and Biochemistry, SacklerSchool of Medicine, Tel Aviv University, Tel Aviv 69978, Israel, Email:shalitel@post.tau.ac.il

andra e. talaska

Kresge Hearing Research Institute, University of Michigan, Ann Arbor, MI48109-0506, USA, Email: atalaska@umich.edu

philine wangemann

Department of Anatomy & Physiology, Kansas State University, Manhattan,KS 66506, USA, Email: wange@vet.ksu.edu

Series Preface

The Springer Handbook of Auditory Research presents a series of comprehensiveand synthetic reviews of the fundamental topics in modern auditory research. Thevolumes are aimed at all individuals with interests in hearing research includingadvanced graduate students, postdoctoral researchers, and clinical investigators.The volumes are intended to introduce new investigators to important aspectsof hearing science and to help established investigators to better understand thefundamental theories and data in fields of hearing that they may not normallyfollow closely.

Each volume presents a particular topic comprehensively, and each serves asa synthetic overview and guide to the literature. As such, the chapters presentneither exhaustive data reviews nor original research that has not yet appearedin peer-reviewed journals. The volumes focus on topics that have developed asolid data and conceptual foundation rather than on those for which a literatureis only beginning to develop. New research areas will be covered on a timelybasis in the series as they begin to mature.

Each volume in the series consists of a few substantial chapters on a particulartopic. In some cases, the topics will be ones of traditional interest for whichthere is a substantial body of data and theory, such as auditory neuroanatomy(Vol. 1) and neurophysiology (Vol. 2). Other volumes in the series deal withtopics that have begun to mature more recently, such as development, plasticity,and computational models of neural processing. In many cases, the series editorsare joined by a co-editor having special expertise in the topic of the volume.

Richard R. Fay, Chicago, ILArthur N. Popper, College Park, MD

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Volume Preface

The past decade has brought great advances in our understanding of the mecha-nisms underlying auditory pathologies. Molecular biology and genetics primarilyhave contributed to this enhanced understanding, which in turn has driven thedesign of novel rational therapeutic interventions. This volume presents recentdevelopments in auditory research and their potential translation to the clinicalsetting. In particular, the authors address the major entities of peripheral auditorytrauma; discuss the underlying mechanisms, the central nervous system conse-quences, and protective interventions; and finally explore the possibilities torestore cochlear morphology and function.

Two themes pervade the chapters in this book: cellular homeostasis and celldeath. In the broadest sense, all auditory pathologies are disorders of cellularhomeostasis. The book appropriately starts with a consideration of genetic factorsthat determine the function and the dysfunction of the auditory organ andpredispose an individual to acquired hearing loss. Shalit and Avraham (Chapter2) review the revolution in genetics that has given us profound insight into thegenes that are involved in inner ear disorders. Extending the chapter on geneticsfrom a physiological perspective, Wangemann in Chapter 3 treats disorders ofthe cochlea with the background of our understanding of cellular metabolism andmetabolic regulation. Following a comprehensive assessment of the principlesof homeostasis, the author discusses the most prominent or well understoodhomeostatic disorders.

Tinnitus, a major enigma among hearing disorders, is the topic of Chapter 4 byBauer and Brozoski. The authors review current theories, potential mechanisms,and promising treatments. Autoimmune inner ear disease is now recognizedas a genuine inner ear disorder. In Chapter 5, Gopen and Harris discuss thebasic immunology of the inner ear, the pathophysiology of the disease includingthat studied in animal models, as well as clinical diagnosis and treatment ofautoimmune hearing loss. The changes in hearing associated with age-relatedhearing loss reflect alterations in both the cochlea and the central auditorypathways. In Chapter 6, Ohlemiller and Frisina discuss our current understandingof the various forms of presbycusis derived from clinical observations and animalmodels. Auditory pathologies resulting from noise or drugs have long beenestablished. Noise-induced hearing loss is discussed in Chapter 7 by Henderson,Hu, and Bielefeld, while in Chapter 8, Rybak, Talaska, and Schacht summarizethe latest on drug-induced hearing loss.

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xvi Volume Preface

While the preceding chapters primarily deal with the peripheral auditorysystem as the site of the initial lesion of auditory trauma, Morest and Potashnerdetail the pathophysiology of central auditory pathways and its molecular basisin Chapter 9.

The complexity of the cellular regulation of cell death pathways, as well asendogenous protective mechanisms, are considered in Chapter 10 by Green,Altschuler, and Miller. In addition to a detailed consideration of cell deathpathways, the authors outline the state-of-the-art attempts to protect the cochleaagainst environmental insults, with special attention to the spiral ganglionneurons.

Finally, Heller and Raphael introduce the most recent revolutionary develop-ments in hair cell regeneration and stem cell therapy in Chapter 11. They giveus a vision of a future when hearing loss and loss of hair cells may be reversedby genetic or pharmacological manipulation.

As often is the case, earlier volumes of the Springer Handbook of AuditoryResearch Series also provide background or additional information about materialcovered in this volume. Related topics in Vol. 7 of the series (Clinical Aspectsof Hearing, edited by Van de Water, Popper, and Fay) include chapters onmolecular genetics (Steel and Kimberling), ototoxicity (Garetz and Schacht),and the psychophysical study of tinnitus (Penner and Jastreboff). An additionaldiscussion of homeostasis is found in a chapter by Wangemann and Schacht inVol. 8 (The Cochlea, edited by Dallos, Popper, and Fay). Supplementing thesummary of genetics in this volume are the chapters of Vol. 14 (Genetics andAuditory Disorders, edited by Keats, Popper, and Fay) that discuss genes andmutations in hearing impairment (Avraham and Hasson), genetic epidemiologyof deafness (Nance and Pandya), and genetic counseling (Arnos and Oelrich).Finally, Vol. 26 (Development of the Inner Ear, edited by Kelley, Wu, Popper,and Fay) includes several relevant chapters on the molecular biology of eardevelopment, including a chapter by Herzano and Avraham on developmentalgenes associated with hearing loss in humans. The current volume thus buildson and expands the information presented in earlier volumes of the Handbookof Auditory Research.

Jochen Schacht, Ann Arbor, MIArthur N. Popper, College Park, MD

Richard R. Fay, Chicago, IL