Springer Handbook of Auditory Research Series Editors: Richard R. Fay and Arthur N. Popper http://avaxho.me/blogs/ChrisRedfield Springer Handbook of Auditory Research Volume1:TheMammalianAuditoryPathway:Neuroanatomy EditedbyDouglasB.Webster,ArthurN.Popper,andRichardR.Fay Volume2:TheMammalianAuditoryPathway:Neurophysiology EditedbyArthurN.PopperandRichardR.Fay Volume3:HumanPsychophysics EditedbyWilliamYost,ArthurN.Popper,andRichardR.Fay Volume4:ComparativeHearing:Mammals EditedbyRichardR.FayandArthurN.Popper Volume5:HearingbyBats EditedbyArthurN.PopperandRichardR.Fay Volume6:AuditoryComputation EditedbyHaroldL.Hawkins,TeresaA.McMullen,ArthurN.Popper,andRichardR.Fay Volume7:ClinicalAspectsofHearing EditedbyThomasR.VanDeWater,ArthurN.Popper,andRichardR.Fay Volume8:TheCochlea EditedbyPeterDallos,ArthurN.Popper,andRichardR.Fay Volume9:DevelopmentoftheAuditorySystem EditedbyEdwinWRubel,ArthurN.Popper,andRichardR.Fay Volume10:ComparativeHearing:Insects EditedbyRonaldHoy,ArthurN.Popper,andRichardR.Fay Volume11:ComparativeHearing:FishandAmphibians EditedbyRichardR.FayandArthurN.Popper Volume12:HearingbyWhalesandDolphins EditedbyWhitlowW.L.Au,ArthurN.Popper,andRichardR.Fay Volume13:ComparativeHearing:BirdsandReptiles EditedbyRobertDooling,ArthurN.Popper,andRichardR.Fay Volume14:GeneticsandAuditoryDisorders EditedbyBronyaJ.B.Keats,ArthurN.Popper,andRichardR.Fay Volume15:IntegrativeFunctionsintheMammalianAuditoryPathway EditedbyDonataOertel,RichardR.Fay,andArthurN.Popper Volume16:AcousticCommunication EditedbyAndreaSimmons,ArthurN.Popper,andRichardR.Fay Volume17:Compression:FromCochleatoCochlearImplants EditedbySidP.Bacon,RichardR.Fay,andArthurN.Popper Volume18:SpeechProcessingintheAuditorySystem EditedbyStevenGreenberg,WilliamAinsworth,ArthurN.Popper,andRichardR.Fay Volume19:TheVestibularSystem EditedbyStephenM.Highstein,RichardR.Fay,andArthurN.Popper Volume20:CochlearImplants:AuditoryProsthesesandElectricHearing EditedbyFan-GangZeng,ArthurN.Popper,andRichardR.Fay Volume21:Electroreception EditedbyTheodoreH.Bullock,CarlD.Hopkins,ArthurN.Popper,andRichardR.Fay Continuedafterindex Richard J. Salvi Arthur N. Popper Richard R. Fay Editors Hair Cell Regeneration, Repair, and Protection RichardJ.Salvi ArthurN.Popper CenterforHearingandDeafness DepartmentofBiology UniversityofBuffalo UniversityofMaryland Buffalo,NY14214 CollegePark,MD20742 USA USA [email protected] [email protected] RichardR.Fay ParmlyHearingInstitute 6525NorthSheridanRoad LoyolaUniversityChicago Chicago,IL60626 USA [email protected] SeriesEditors: RichardR.Fay ArthurN.Popper ParmlyHearingInstitute DepartmentofBiology 6525NorthSheridanRoad UniversityofMaryland LoyolaUniversityChicago CollegePark,MD20742 Chicago,IL60626 USA USA ISBN:978-0-387-73363-0 e-ISBN:979-0-387-3364-7 LibraryofCongressControlNumber:2007929278 ©2008SpringerScience+BusinessMedia,LLC Allrightsreserved.Thisworkmaynotbetranslatedorcopiedinwholeorinpartwithoutthewritten permissionofthepublisher(SpringerScience+BusinessMedia,LLC,233SpringStreet,NewYork, NY10013,USA),exceptforbriefexcerptsinconnectionwithreviewsorscholarlyanalysis.Use in connection with any form of information storage and retrieval, electronic adaptation, computer software,orbysimilarordissimilarmethodologynowknownorhereafterdevelopedisforbidden. The use in this publication of trade names, trademarks, service marks, and similar terms, even if theyarenotidentifiedassuch,isnottobetakenasanexpressionofopinionastowhetherornot theyaresubjecttoproprietaryrights. Coverillustration:TheimageincludespartsofFigures5.2and2.5appearinginthetext. Printedonacid-freepaper 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: [email protected] micheal l. dent Department of Psychology, University at Buffalo–SUNY, Buffalo, NY 14260, USA, Email: [email protected] robert j. dooling Department of Psychology and Center for the Comparative Evolutionary Biology of Hearing, University of Maryland, College Park, MD 20742, USA, Email: [email protected] andrew forge Centre for Auditory Research, UCL Ear Institute, University College London, London WC1X 8EE, UK, Email: [email protected] matthew c. holley Department of Biomedical Science, University of Sheffield, Sheffield, S10 2TN, UK, Email: [email protected] amanda m. lauer Department of Psychology and Center for the Comparative Evolutionary Biology of Hearing, University of Maryland, College Park, MD 20742, USA, Email: [email protected] jason r. meyers Department of Molecular, Cellular and Developmental Biology, University of Michigan, Ann Arbor MI 48109, USA, Email: [email protected] elizabeth c. oesterle Virginia Merrill Bloedel Hearing Research Center, Department of Otolaryn- gology, University of Washington, Seattle, WA 98195-7923, USA, Email: [email protected] vii viii Contributors marcelo n. rivolta CentreforStemCellBiology,UniversityofSheffield,Sheffield,S102TN,UK, Email: [email protected] brenda m. ryals Department of Communication Sciences and Disorders, James Madison University, Harrisonburg, VA 22807, USA, Email: [email protected] richard j. salvi University of Buffalo, Center for Hearing and Deafness, Buffalo, NY 14214, USA, Email: [email protected] james c. saunders University of Pennsylvania, Philadelphia, PA 19104, USA, Email: [email protected] jennifer s. stone Virginia Merrill Bloedel Hearing Research Center, Department of Otolaryn- gology, Seattle, WA 98195 7923, USA, Email: [email protected] thomas r. van de water DepartmentofOtolaryngology,CochlearImplantResearchProgram,University ofMiamiEarInstitute,UniversityofMiami,MillerSchoolofMedicine,Miami, FL 33136-1015, USA, Email: [email protected] Series Preface TheSpringerHandbookofAuditoryResearchpresentsaseriesofcomprehensive andsyntheticreviewsofthefundamentaltopicsinmodernauditoryresearch.The volumesareaimedatallindividualswithinterestsinhearingresearch,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. Eachvolumeintheseriesconsistsofafewsubstantialchaptersonaparticular 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 topicsthathavebeguntomaturemorerecently,suchasdevelopment,plasticity, andcomputationalmodelsofneuralprocessing.Inmanycases,theserieseditors 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 ofneuralactivitythatcanbeinterpretedbysophisticatedneuralnetworkslocated atmultiplelevelsofthecentralnervoussystem.Ithaslongbeenknownthathair celllossinmammalsduetoaging,ototoxicdrugs,acoustictrauma,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 engineeringsolutions.Whilemuchefforthasbeenmadetouseelectronicmeans toimprovehearing,thenextgiantsteptowardrestoringhearingtotheprofoundly 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 biologicallybasedmedicalinnovationsthatweresetintomotionduringthepast 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 regeneratedhairsarisefromrepairofdamagedcells,conversionofsupportcells tohaircells,orproliferationofsupportcellsthatdifferentiatetoeitherhaircells or replacement support cells. One of the most important areas that stimulated studies of damage, regen- eration, and repair has been in the avian auditory system. In Chapter 3, Salvi andSaundersdescribetheremarkablerecoveryoffunctionoftheavianauditory systemfollowingacoustictraumaandototoxicinsult.Physiologicalstudiesshow significant recovery, with only minor deficits except for cases in which the xi