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The Auditory Cortex · Jeffery A. Winer Christoph E. Schreiner Editors The Auditory Cortex 123 Editors JefferyA.Winer ChristophE.Schreiner DepartmentofMolecular&CellBiology ColemanMemorialLaboratory UniversityofCalifornia DepartmentofOtolaryngology Berkeley,CA94720-3200,USA UniversityofCalifornia SanFrancisco,CA94143-0732,USA [email protected] ISBN978-1-4419-0073-9 e-ISBN978-1-4419-0074-6 DOI10.1007/978-1-4419-0074-6 SpringerNewYorkDordrechtHeidelbergLondon ©SpringerScience+BusinessMedia,LLC2011 Allrightsreserved.Thisworkmaynotbetranslatedorcopiedinwholeorinpartwithoutthewrittenpermission ofthepublisher(SpringerScience+BusinessMedia,LLC,233SpringStreet,NewYork,NY10013,USA),except forbriefexcerptsinconnectionwithreviewsorscholarlyanalysis.Useinconnectionwithanyformofinformation storageandretrieval,electronicadaptation,computersoftware,orbysimilarordissimilarmethodologynowknown orhereafterdevelopedisforbidden. Theuseinthispublicationoftradenames,trademarks,servicemarks,andsimilarterms,eveniftheyarenotidentified assuch,isnottobetakenasanexpressionofopinionastowhetherornottheyaresubjecttoproprietaryrights. Printedonacid-freepaper SpringerispartofSpringerScience+BusinessMedia(www.springer.com) r e n Wi A. e n a J f o y s e rt u o c h p a r g o ot h P JefferyA.Winer(1945–2008) Scholar,scientist,colleague,mentor,friend PhotographcourtesyofJaneA.Winer Preface Thisvolumeisasummaryandsynthesisofthecurrentstateofauditoryforebrainorganization. Wethinkitatimelycontributioninviewofthegrowinginterestinthisnetworkasthearbiter for hearing, as a key element in the larger communications network that spans and links the parietal, temporal, and frontal cortices, and as a candidate for clinical intervention, whether throughcochlearimplantsormoreexoticupstreamprosthesesthat,oneday,mayinvolvethe forebrainmoredirectly. The present account differs from the available efforts (Aitkin 1990; König et al. 2005) in twosignificantways.First,themedialgeniculatebodyisincludedasafullpartnersinceithas cooperative,reciprocal,androbustrelationswiththeauditorycortexthatsuggestapartnership in which the exclusion of either structure detracts from a functional portrait of their interac- tions. Second, our aim has been systematic and synoptic, including as it does a wide range ofspecies,methods,subsystems,physiologicalperspectives,andfunctionalarchitectures.We lookbackon100yearsofthedisciplineofauditoryforebrainstudieswithaviewtoframing a future agenda. As new methods emerge and as older approaches exhaust their potential, it seems appropriate to attempt a summing up and to forge a prospectus for future work. We cannotpresentafulltheoryofauditoryforebrainorganizationsincethefieldisstillsonewas a discipline; that task we must leave to a later, more mature volume that recognizes the dis- tributed nature of forebrain operations in a more refined way than is now possible. Our goal is to provide an experimental foundation and a conceptual framework for the auditory fore- brainusefultothedisciplineasawhole,andwhichonemightconsultasbothasummaryof workinprogressandaninvitationtoexplorefurther.Thisformidabletaskcouldnothavebeen accomplished without the contribution of an expert cohort of collaborators on whose efforts thisenterpriserests. Severalmethodologicalandconceptualinsightshaveconvergedtocreatethepresent,con- genial atmosphere for this effort. The emergence of new functional approaches such as the tissue slice and its varieties has enabled the exploration of new neurochemical and synaptic vistas (Metherate and Hsieh 2004) and allowed a more formal and anatomical–physiological characterizationofidentifiedneurons(Verbnyetal.2006).Relatedadvancesincludetheimpor- tantinsightsgleanedfromlargesiliconelectrodesthatspanthefullcorticaldepthandreveal critical facets of interneuronal and laminar organization invisible to a single extracellular pipet (Atencio and Schreiner 2008). Such local circuits in the medial geniculate body and auditory cortex are the functional building blocks upon which the large-scale operations of spectral analysis, aurality, and frequency modulation are arrayed. How these several subsys- temsinteractcooperativelyasanetworkisamongthemostchallengingquestionsforthefuture. Other powerful insights flowed from the ability to record from synaptically joined pairs of cells(Milleretal.2001)contributingtoanewperspectiveonthethalamocorticaltransforma- tion(Wineretal.2005).Understandingsuchtransformations—tectothalamic,thalamocortical, corticocortical,andcorticofugal—remainsanenterpriseforthefuture. vii viii Preface A second wave of insight arose from the neuroimaging domain, where positron emission tomography,functionalmagneticresonanceimaging,andmagnetoencephalographyeachpro- vided powerful documentation of the locus and density of activity in the living brain during specifictasksorafterparticularpathologies.Thisworknotonlydefinedthesiteofactivation, butrelatedmeasuressuchas2-deoxygluoseprovidedthefirstfullperspectiveonthelimitsof auditory-responsivecortex(Porembaetal.2003). Neuroanatomical and immunocytochemical approaches have provided credible maps of connectivity in the thalamocortical and corticocortical systems (Huang and Winer 2000; de La Mothe et al. 2006), documenting a vast web of forebrain long- and short-range circuits. Theimplementationofstudiesoflamina-specificinterneuronalpropertieshasprovidedvalu- ableinsightsintothesedynamicsystems(Atencioetal.2009).Thecorticothalamicandother corticofugalsystemslikewisearenowconstruedasprospectivedynamicplayersinregulating auditorycorticalexcitabilityratherthanasfeedbackpathways(Wineretal.2001).Combined physiological-connectional studies established the existence of specific pathways for sound localizationandobjectidentification(RauscheckerandTian2000). Thedramaticdemonstrationandensuingexplorationofwidespreadauditoryforebrainplas- ticity(KilgardandMerzenich1998;Weinberger1998)wasawatershedanditsimplementation inthedescendingsystems(Zhangetal.2005)suggestedaroleforthecorticofugalsystemsvery differentfromearlieraccountsthatemphasizedfeedback.Theauditorycortexnowappearsto beasconcernedwiththecontrolofinferiorcolliculusexcitabilityandplasticityandinforma- tionprocessingasitisintheanalysisofsoundparametersandcategoricalperceptualanalyses. Suchfindingswerealinchpininlargereffortstocharacterizethedistributedauditorycortexas anentitythatrepresentshearinginitslargestandmostinclusivesense(WinerandLee2007). The present volume can be construed as a multidisciplinary effort to further implement and instantiatethatperspective. Berkeley,CA JefferyA.Winer SanFrancisco,CA ChristophE.Schreiner References Aitkin L (1990) The Auditory Cortex: Structural and Functional Bases of Auditory Perception.ChapmanandHall,London. Atencio CA and Schreiner CE (2008) Spectrotemporal processing differences between auditory cortical fast-spiking and regular-spiking neurons. Journal of Neuroscience 28: 3897–3910. AtencioCA,SharpeeTO,andSchreinerCE(2009)Hierarchicalcomputationinthecanonical auditory cortical circuit. Proceedings of the National Academy of Sciences of the United StatesofAmerica106:21894–21899. de La Mothe L, Blumell S, Kajikawa Y, and Hackett TA (2006) Thalamic connections of the auditory cortex in marmoset monkeys: core and medial belt regions. Journal of ComparativeNeurology496:72–96. HuangCLandWinerJA(2000)Auditorythalamocorticalprojectionsinthecat:laminarand arealpatternsofinput.JournalofComparativeNeurology427:302–331. Kilgard MP and Merzenich MM (1998) Cortical map reorganization enabled by nucleus basalisactivity.Science279:1714–1718. KönigR,HeilP,BudingerE,andScheichH(eds.)(2005)TheAuditoryCortex.ASynthesis ofHumanandAnimalResearch,LawrenceErlbaumAssociates,Mahwah. Metherate R and Hsieh CY (2004) Synaptic mechanisms and cholinergic regulation in auditorycortex.ProgressinBrainResearch145:143–156. Preface ix Miller LM, Escabí MA, and Schreiner CE (2001) Feature selectivity and interneuronal cooperationinthethalamocorticalsystem.JournalofNeuroscience21:8136–8144. PorembaA,SaundersRC,CraneAM,CookM,SokoloffL,andMishkinM(2003)Functional mappingoftheprimateauditorysystem.Science299:568–572. Rauschecker JP and Tian B (2000) Mechanisms and streams for processing of “what” and “where”inauditorycortex.ProceedingsoftheNationalAcademyofSciencesoftheUnited StatesofAmerica97:11800–11806. Verbny YL, Erdélyi F, Szabó G, and Banks MI (2006) Properties of a population of GABAergic cells in murine auditory cortex weakly excited by thalamic stimulation. JournalofNeurophysiology96:3194–3208. WeinbergerNM(1998)Tuningthebrainbylearningandbystimulationofthenucleusbasalis. TrendsinCognitiveSciences2:271–273. Winer JA, Diehl JJ, and Larue DT (2001) Projections of auditory cortex to the medial geniculatebodyofthecat.JournalofComparativeNeurology430:27–55. WinerJAandLeeCC(2007)Thedistributedauditorycortex.HearingResearch229:3–13. WinerJA,MillerLM,LeeCC,andSchreiner CE(2005)Auditorythalamocortical transfor- mation:structureandfunction.TrendsinNeurosciences28:255–263. ZhangY,HakesJJ,BonfieldSP,andYanJ(2005)Corticofugalfeedbackforauditorymidbrain plasticityelicitedbytonesandelectricalstimulationofbasalforebraininmice.European JournalofNeuroscience22:871–879. Acknowledgments Our colleagues, collaborators, and students were instrumental in expressing the need for and inspiring the preparation of this book. In lieu of a list that might inadvertently omit some worthy of mention, we simply thank the many whose encouragement and labors made this volumepossible.Interactionswiththemwereadelightandtheiringenuityandcreativitywas asourceofmuchpleasure.Wethankthechapterauthorsforstrivingtocapturetheessenceof adynamicfieldwithinthespaceconstraints. Onamoreindividualbasisweareespeciallygratefultooureditor,AnnAvourisofSpringer New York for her unfailing efforts to help us realize our vision. She was the ideal editor, providingtimelyandbalancedcounselandremindinguswithcourtesyoftheshortestpathto ourgoal.DavidT.Larueusedhisgraphicsexpertisetoorganizeandperfectthemanyfigures thatareattheheartofthisvolume. Eachofuswerebeneficiariesoftheaidandencouragementofourfamilies,JaneM.Winer, CarolR.Galbraith,andEileenG.WinerforJeff,andMarciaRaggioandChristinaSchreiner forChristoph.Wearemostthankfulfortheirunfailingandlovingsupport. Berkeley,CA JefferyA.Winer SanFrancisco,CA ChristophE.Schreiner xi Contents 1 TheHistoricalDevelopmentofIdeasAbouttheAuditoryCortex . . . . . . . 1 EdwardG.Jones 2 AProfileofAuditoryForebrainConnectionsandCircuits . . . . . . . . . . 41 JefferyA.Winer 3 ThalamocorticalRelations . . . . . . . . . . . . . . . . . . . . . . . . . . . . 75 MatthewI.BanksandPhilipH.Smith 4 AuditoryCorticalOrganization:EvidenceforFunctionalStreams . . . . . . 99 JosefP.RauscheckerandLizabethM.Romanski 5 TheCommissuralAuditorySystem . . . . . . . . . . . . . . . . . . . . . . . 117 TroyA.HackettandDennisP.Phillips 6 IntrinsicConnectionsoftheAuditoryCortex . . . . . . . . . . . . . . . . . . 133 MarkN.WallaceandJufangHe 7 ASynthesisofAuditoryCorticalConnections:Thalamocortical, CommissuralandCorticocorticalSystems . . . . . . . . . . . . . . . . . . . 147 CharlesC.LeeandJefferyA.Winer 8 AuditoryCorticalProjectionstotheMedialGeniculateBody . . . . . . . . . 171 HisayukiOjimaandEricM.Rouiller 9 Descending Connections of Auditory Cortex to the Midbrain andBrainStem . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 189 ManuelS.MalmiercaandDavidK.Ryugo 10 Neurochemical Organization of the Medial Geniculate Body andAuditoryCortex . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 209 JefferyA.Winer 11 SynapticIntegrationinAuditoryCortex . . . . . . . . . . . . . . . . . . . . 235 MichaelWehrandRajuMetherate 12 PhysiologicalPropertiesofNeuronsintheMedialGeniculateBody . . . . . 251 Jean-MarcEdeline 13 SpectralProcessinginAuditoryCortex . . . . . . . . . . . . . . . . . . . . . 275 ChristophE.Schreiner,RobertC.Froemke,andCraigA.Atencio 14 TemporalCodinginAuditoryCortex . . . . . . . . . . . . . . . . . . . . . . 309 JosJ.EggermontandXiaoqinWang 15 CorticalRepresentationofAuditorySpace . . . . . . . . . . . . . . . . . . . 329 AndrewJ.KingandJohnC.Middlebrooks xiii
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