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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: Neuroanatomy

Edited by Douglas B. Webster, Arthur N. Popper, and Richard R. Fay

Volume 2: The Mammalian Auditory Pathway: Neurophysiology

Edited by Arthur N. Popper and Richard R. Fay

Volume 3: Human Psychophysics

Edited by William Yost, Arthur N. Popper, and Richard R. Fay

Volume 4: Comparative Hearing: Mammals

Edited by Richard R. Fay and Arthur N. Popper

Volume 5: Hearing by Bats

Edited by Arthur N. Popper and Richard R. Fay

Volume 6: Auditory Computation

Edited by Harold L. Hawkins, Teresa A. McMullen, Arthur N. Popper, and Richard R. Fay

Volume 7: Clinical Aspects of Hearing

Edited by Thomas R. Van De Water, Arthur N. Popper, and Richard R. Fay

Volume 8: The Cochlea

Edited by Peter Dallos, Arthur N. Popper, and Richard R. Fay

Volume 9: Development of the Auditory System

Edited by Edwin W Rubel, Arthur N. Popper, and Richard R. Fay

Volume 10: Comparative Hearing: Insects

Edited by Ronald Hoy, Arthur N. Popper, and Richard R. Fay

Volume 11: Comparative Hearing: Fish and Amphibians

Edited by Richard R. Fay and Arthur N. Popper

Volume 12: Hearing by Whales and Dolphins

Edited by Whitlow W.L. Au, Arthur N. Popper, and Richard R. Fay

Volume 13: Comparative Hearing: Birds and Reptiles

Edited by Robert Dooling, Arthur N. Popper, and Richard R. Fay

Volume 14: Genetics and Auditory Disorders

Edited by Bronya J.B. Keats, Arthur N. Popper, and Richard R. Fay

Volume 15: Integrative Functions in the Mammalian Auditory Pathway

Edited by Donata Oertel, Richard R. Fay, and Arthur N. Popper

Volume 16: Acoustic Communication

Edited by Andrea Simmons, Arthur N. Popper, and Richard R. Fay

Volume 17: Compression: From Cochlea to Cochlear Implants

Edited by Sid P. Bacon, Richard R. Fay, and Arthur N. Popper

Volume 18: Speech Processing in the Auditory System

Edited by Steven Greenberg, William Ainsworth, Arthur N. Popper, and Richard R. Fay

Volume 19: The Vestibular System

Edited by Stephen M. Highstein, Richard R. Fay, and Arthur N. Popper

Volume 20: Cochlear Implants: Auditory Prostheses and Electric Hearing

Edited by Fan-Gang Zeng, Arthur N. Popper, and Richard R. Fay

Volume 21: Electroreception

Edited by Theodore H. Bullock, Carl D. Hopkins, Arthur N. Popper, and Richard R. Fay

Continued after index

Richard J. Salvi

Arthur N. Popper

Richard R. Fay

Editors

Hair Cell Regeneration,

Repair, and Protection

Richard J. Salvi

Arthur N. Popper

Center for Hearing and Deafness

Department of Biology

University of Buffalo

University of Maryland

Buffalo, NY 14214

College Park, MD 20742

USA

USA

salvi@buffalo.edu

apopper@umd.edu

Richard R. Fay

 

Parmly Hearing Institute

 

6525 North Sheridan Road

 

Loyola University Chicago

 

Chicago, IL 60626

 

USA

 

rfay@luc.edu

 

Series Editors:

 

Richard R. Fay

Arthur N. Popper

Parmly Hearing Institute

Department of Biology

6525 North Sheridan Road

University of Maryland

Loyola University Chicago

College Park, MD 20742

Chicago, IL 60626

USA

USA

 

ISBN: 978-0-387-73363-0

e-ISBN: 979-0-387-3364-7

Library of Congress Control Number: 2007929278

© 2008 Springer Science+Business Media, LLC

All rights reserved. This work may not be translated or copied in whole or in part without the written permission 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. Use in connection with any form of information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter developed is forbidden. The use in this publication of trade names, trademarks, service marks, and similar terms, even if they are not identified as such, is not to be taken as an expression of opinion as to whether or not they are subject to proprietary rights.

Cover illustration: The image includes parts of Figures 5.2 and 2.5 appearing in the text.

Printed on acid-free paper

9 8 7 6 5 4 3 2 1

springer.com

Contents

Contributors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . vii

Series Preface. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ix

Volume Preface . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . xi

1.

Overview: Regeneration and Repair . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

1

 

Richard J. Salvi

 

2.

Morphological Correlates of Regeneration and Repair

 

 

in the Inner Ear . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

39

 

Jason R. Meyers and Jeffrey T. Corwin

 

3.

Recovery of Function in the Avian Auditory System

 

 

After Ototrauma . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

77

 

James C. Saunders and Richard J. Salvi

 

4.

Functional Recovery After Hair Cell Regeneration in Birds . . . . . . . . . .

117

 

Robert J. Dooling, Micheal L. Dent, Amanda M. Lauer,

 

 

and Brenda M. Ryals

 

5.

Hair Cell Regeneration: Mechanisms Guiding Cellular Proliferation

 

 

and Differentiation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

141

 

Elizabeth C. Oesterle and Jennifer S. Stone

 

6.

Protection and Repair of Inner Ear Sensory Cells . . . . . . . . . . . . . . . . . . .

199

 

Andrew Forge and Thomas R. Van De Water

 

7.

Gene Arrays, Cell Lines, Stem Cells, and Sensory Regeneration

 

 

in Mammalian Ears . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

257

 

Marcelo N. Rivolta and Matthew C. Holley

 

Index . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

309

v

Contributors

jeffrey t. corwin

Department of Neuroscience, University of Virginia School of Medicine, Charlottesville, VA 22908, USA, Email: jcorwin@virginia.edu

micheal l. dent

Department of Psychology, University at Buffalo–SUNY, Buffalo, NY 14260, USA, Email: mdent@buffalo.edu

robert j. dooling

Department of Psychology and Center for the Comparative Evolutionary Biology of Hearing, University of Maryland, College Park, MD 20742, USA, Email: dooling@psyc.umd.edu

andrew forge

Centre for Auditory Research, UCL Ear Institute, University College London, London WC1X 8EE, UK, Email: a.forge@ucl.ac.uk

matthew c. holley

Department of Biomedical Science, University of Sheffield, Sheffield, S10 2TN, UK, Email: m.c.holley@sheffield.ac.uk

amanda m. lauer

Department of Psychology and Center for the Comparative Evolutionary Biology of Hearing, University of Maryland, College Park, MD 20742, USA, Email: alauer1@umd.edu

jason r. meyers

Department of Molecular, Cellular and Developmental Biology, University of Michigan, Ann Arbor MI 48109, USA, Email: jrmeyers@umich.edu

elizabeth c. oesterle

Virginia Merrill Bloedel Hearing Research Center, Department of Otolaryngology, University of Washington, Seattle, WA 98195-7923, USA, Email: oesterle@u.washington.edu

vii

viii Contributors

marcelo n. rivolta

Centre for Stem Cell Biology, University of Sheffield, Sheffield, S10 2TN, UK, Email: m.n.rivolta@sheffield.ac.uk

brenda m. ryals

Department of Communication Sciences and Disorders, James Madison University, Harrisonburg, VA 22807, USA, Email: ryalsbm@cisat.jmu.edu

richard j. salvi

University of Buffalo, Center for Hearing and Deafness, Buffalo, NY 14214, USA, Email: salvi@buffalo.edu

james c. saunders

University of Pennsylvania, Philadelphia, PA 19104, USA, Email: saunderj@mail.med.upenn.edu

jennifer s. stone

Virginia Merrill Bloedel Hearing Research Center, Department of Otolaryngology, Seattle, WA 98195 7923, USA, Email: stoner@u.washington.edu

thomas r. van de water

Department of Otolaryngology, Cochlear Implant Research Program, University of Miami Ear Institute, University of Miami, Miller School of Medicine, Miami, FL 33136-1015, USA, Email: tvandewater@med.miami.edu

Series Preface

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

Each volume presents a particular topic comprehensively, and each serves as a synthetic overview and guide to the literature. As such, the chapters present neither exhaustive data reviews nor original research that has not yet appeared in peer-reviewed journals. The volumes focus on topics that have developed a solid data and conceptual foundation rather than on those for which a literature is only beginning to develop. New research areas will be covered on a timely basis in the series as they begin to mature.

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

Richard R. Fay, Chicago, IL

Arthur N. Popper, College Park, MD

ix

Volume Preface

The human brain’s ability to sense and interpret acoustic events taking place in remote or nearby locations in the external environment is mediated by highly specialized and extremely sensitive sensory hair cells located in the inner ear. These cells transduce acoustic information from the environment into a pattern of neural activity that can be interpreted by sophisticated neural networks located at multiple levels of the central nervous system. It has long been known that hair cell loss in mammals due to aging, ototoxic drugs, acoustic trauma, infection, or genetic factors results in permanent hearing loss or balance problems. Over the past 50 years, efforts to find a cure for deafness have focused on hardware and engineering solutions. While much effort has been made to use electronic means to improve hearing, the next giant step toward restoring hearing to the profoundly deaf will involve regenerating the damaged biological structures in the inner ear, in particular the hair cells and spiral ganglion neurons. The major clinical advances in hearing and balance that will occur in the 21st century will involve biologically based medical innovations that were set into motion during the past few decades by the discovery of hair cell regeneration and by the recognition that stem cells exist in many regions of the nervous system, including the inner ear.

These discoveries, and the potential for helping people with hearing loss, are the focus of this volume. In Chapter 1, Salvi reviews the history of studies on hair cell regeneration and provides an overview of current knowledge as well as new technologies to promote regeneration and repair. The recognition that hair cell regeneration can occur in nonmammals gave way to ground breaking studies using gene therapy to simulate hair cell regeneration in mammals. The history of the field, as well as what is known about the morphology associated with regeneration and repair of sensory hair cells, are the focus of Chapter 2 by Meyers and Corwin. One of the fundamental issues examined is whether regenerated hairs arise from repair of damaged cells, conversion of support cells to hair cells, or proliferation of support cells that differentiate to either hair cells or replacement support cells.

One of the most important areas that stimulated studies of damage, regeneration, and repair has been in the avian auditory system. In Chapter 3, Salvi and Saunders describe the remarkable recovery of function of the avian auditory system following acoustic trauma and ototoxic insult. Physiological studies show significant recovery, with only minor deficits except for cases in which the

xi