Changing Brains: Applying Brain Plasticity to Advance and Recover Human Ability PDF
Preview Changing Brains: Applying Brain Plasticity to Advance and Recover Human Ability
Advisory Editors Stephen G. Waxman BridgetMarieFlahertyProfessorofNeurology Neurobiology,andPharmacology; Director,CenterforNeuroscience& Regeneration/NeurorehabilitationResearch YaleUniversitySchoolofMedicine NewHaven,Connecticut USA Donald G. Stein AsaG.CandlerProfessor DepartmentofEmergencyMedicine EmoryUniversity Atlanta,Georgia USA Dick F. Swaab ProfessorofNeurobiology MedicalFaculty,UniversityofAmsterdam; LeaderResearchteamNeuropsychiatricDisorders NetherlandsInstituteforNeuroscience Amsterdam TheNetherlands Howard L. Fields ProfessorofNeurology EndowedChairinPharmacologyofAddiction Director,WheelerCenterfortheNeurobiologyofAddiction UniversityofCalifornia SanFrancisco,California USA Elsevier Radarweg29,POBox211,1000AEAmsterdam,TheNetherlands TheBoulevard,LangfordLane,Kidlington,Oxford,OX51GB,UK Firstedition2013 Copyright#2013ElsevierB.V.Allrightsreserved Nopartofthispublicationmaybereproduced,storedinaretrievalsystemortransmitted inanyformorbyanymeanselectronic,mechanical,photocopying,recordingor otherwisewithoutthepriorwrittenpermissionofthepublisher PermissionsmaybesoughtdirectlyfromElsevier’sScience&TechnologyRights DepartmentinOxford,UK:phone(þ44)(0)1865843830;fax(þ44)(0)1865853333; email:permissions@elsevier.com.Alternativelyyoucansubmityourrequestonlineby visitingtheElsevierwebsiteathttp://elsevier.com/locate/permissions,andselecting ObtainingpermissiontouseElseviermaterial Notice Noresponsibilityisassumedbythepublisherforanyinjuryand/ordamagetopersonsor propertyasamatterofproductsliability,negligenceorotherwise,orfromanyuseoroperation ofanymethods,products,instructionsorideascontainedinthematerialherein.Becauseof rapidadvancesinthemedicalsciences,inparticular,independentverificationofdiagnoses anddrugdosagesshouldbemade LibraryofCongressCataloging-in-PublicationData AcatalogrecordforthisbookisavailablefromtheLibraryofCongress BritishLibraryCataloguinginPublicationData AcataloguerecordforthisbookisavailablefromtheBritishLibrary ISBN:978-0-444-63327-9 ISSN:0079-6123 ForinformationonallElsevierpublications visitourwebsiteatstore.elsevier.com PrintedandboundinGreatBritain 13 14 15 16 11 10 9 8 7 6 5 4 3 2 1 Contributors Merav Ahissar ELSCCenterforBrainResearchandtheDepartmentofPsychology,TheHebrew University, Jerusalem, Israel Laura C.Anderson Yale Center for Translational DevelopmentalNeuroscience, YaleChild Study Center,New Haven, CT,USA Joaquin A. Anguera Departments ofNeurology, Physiologyand Psychiatry, University ofCalifornia, San Francisco, CA, USA Bruno Biagianti SanFranciscoDepartmentofVeteransAffairsMedicalCenter,andDepartmentof Psychiatry, University ofCalifornia,SanFrancisco, CA, USA Ioana Carcea Molecular Neurobiology Program, The Helen and Martin Kimmel Center for Biologyand Medicineat theSkirball Institute for Biomolecular Medicine, Department ofPhysiology andNeuroscience;Department ofOtolaryngology, New YorkUniversity School ofMedicine,and Center for Neural Science, New YorkUniversity, New York, NY, USA Naiyan Chen Picower Institutefor Learning and Memory,Department of Brain and Cognitive Sciences, Massachusetts Instituteof Technology, Cambridge, MA, USA Joseph M.DeGutis Department ofVeteran Affairs, and Department ofMedicine,Brigham and Women’s Hospital,Harvard MedicalSchool,Boston, MA, USA PatrickFissler Clinical&BiologicalPsychology, University ofUlm, Ulm, Germany Robert C. Froemke Molecular Neurobiology Program, The Helen and Martin Kimmel Center for Biologyand Medicineat theSkirball Institute for Biomolecular Medicine, DepartmentofPhysiologyandNeuroscience;DepartmentofOtolaryngology,New York University SchoolofMedicine, and Center for NeuralScience,New York University, New York, NY, USA Adam Gazzaley Departments ofNeurology, Physiologyand Psychiatry, University ofCalifornia, San Francisco, CA, USA Robbin Gibb CanadianCentre for Behavioural Neuroscience, University ofLethbridge, Lethbridge, AB, Canada v vi Contributors SethA.Hays The University ofTexas atDallas, School ofBehavioral Brain Sciences, and TheUniversityofTexasatDallas,TexasBiomedicalDeviceCenter,Richardson, TX, USA TakaoK. Hensch FM Kirby Neurobiology Center, Boston Children’s Hospital, Harvard Medical School,Boston,andCenterforBrainScience,DepartmentofMolecular&Cellular Biology, Harvard University, Cambridge, MA, USA Nori Jacoby Interdisciplinary Center for Neural Computation,The HebrewUniversity, Jerusalem, and Music Department, Bar Ilan University, Ramat Gan,Israel Michael P.Kilgard The University ofTexas atDallas, School ofBehavioral Brain Sciences, and TheUniversityofTexasatDallas,TexasBiomedicalDeviceCenter,Richardson, TX, USA Robert T.Knight DepartmentofNeurologicalSurgery,UniversityofCalifornia—SanFrancisco,San Francisco; Helen WillsNeuroscience Institute,andDepartment ofPsychology, University ofCaliforniaBerkeley, Berkeley, CA,USA Iris-Tatjana Kolassa Clinical &BiologicalPsychology, University of Ulm, Ulm, Germany Bryan Kolb Canadian Centre for Behavioural Neuroscience, University ofLethbridge, Lethbridge, AB, Canada Nina Kraus AuditoryNeuroscienceLaboratory, Northwestern University; Communication Sciences; Institute for Neuroscience; Neurobiology and Physiology, and Otolaryngology, Evanston, IL,USA Olivia Ku¨ster Clinical &BiologicalPsychology, University of Ulm, Ulm, Germany HyunkyuLee BrainPlasticityInstituteatPosit Science Corporation, San Francisco, CA, USA Michael M. Merzenich BrainPlasticityInstituteatPosit Science Corporation, San Francisco, CA, USA JyotiMishra Departmentsof Neurology, Physiology and Psychiatry, University of California, San Francisco, CA, USA Arif Muhammad Canadian Centre for Behavioural Neuroscience, University ofLethbridge, Lethbridge, AB, Canada Contributors vii Richelle Mychasiuk CanadianCentre for Behavioural Neuroscience, University ofLethbridge, Lethbridge, AB, Canada Ikue Nagakura Picower Institutefor Learning and Memory,Department of Brain and Cognitive Sciences, Massachusetts Instituteof Technology, Cambridge, MA, USA Mor Nahum Brain Plasticity Institute atPosit Science Corporation,San Francisco, and Department ofOptometry, University ofCalifornia, Berkeley, CA,USA Lindsay Oberman Berenson-AllenCenterforNoninvasiveBrainStimulation,BethIsraelDeaconess MedicalCenter,Harvard Medical School, Boston, MA, USA Devon Oosting Yale Center for Translational DevelopmentalNeuroscience, YaleChild Study Center,New Haven, CT,USA Alvaro Pascual-Leone Berenson-AllenCenterforNoninvasiveBrainStimulation,BethIsraelDeaconess MedicalCenter,Harvard Medical School, Boston, MA, USA BrianN. Pasley Helen Wills Neuroscience Institute,University ofCalifornia Berkeley, Berkeley, CA, USA Kevin A.Pelphrey Yale Center for Translational DevelopmentalNeuroscience, YaleChild Study Center,New Haven, CT,USA Robert L. Rennaker The University ofTexas atDallas, SchoolofBehavioral Brain Sciences; The University ofTexas atDallas, Texas Biomedical Device Center,and The UniversityofTexasatDallas,ErikJonssonSchoolofEngineeringandComputer Science,Richardson, TX,USA WinfriedSchlee Clinical&BiologicalPsychology, University ofUlm, Ulm, Germany HirokiSugihara Picower Institutefor Learning and Memory,Department of Brain and Cognitive Sciences, Massachusetts Instituteof Technology, Cambridge, MA, USA Mriganka Sur Picower Institutefor Learning and Memory,Department of Brain and Cognitive Sciences, Massachusetts Instituteof Technology, Cambridge, MA, USA Anne E.Takesian FM Kirby Neurobiology Center,BostonChildren’s Hospital, Harvard Medical School,Boston, MA, USA viii Contributors PaulaTallal Rutgers,TheStateUniversityofNewJersey,CenterforMolecularandBehavioral Neuroscience,Newark,NJ, USA EdwardTaub DepartmentofPsychology,UniversityofAlabamaatBirmingham,Birmingham, AL,USA AdamTierney AuditoryNeuroscienceLaboratory,NorthwesternUniversity,andCommunication Sciences, Evanston,IL, USA Gitendra Uswatte Department ofPsychology, and Department ofPhysicalTherapy, University of Alabama atBirmingham, Birmingham, AL,USA Thomas M.VanVleet BrainPlasticityInstituteatPosit Science Corporation, San Francisco, and Department ofVeteran Affairs, Martinez, CA,USA Pamela E.Ventola YaleCenter for Translational DevelopmentalNeuroscience, YaleChild Study Center,New Haven,CT, USA Sophia Vinogradov SanFranciscoDepartmentofVeteransAffairsMedicalCenter,andDepartmentof Psychiatry, University ofCalifornia, San Francisco, CA,USA David A.Ziegler Departmentsof Neurology, Physiology and Psychiatry, University of California, San Francisco, CA, USA Introduction The science of neuroplasticity has resulted in a new level of understanding of the neurological origins of human ability (Merzenich, 2013). From this science, the “rules”governinglearningandbehavioralcontrolhavebeenfurtherdefined,inin- creasinglycompleteandelaboratedetail,intermsoftheneurologicalprocessesthat underliethem.Thatscientificelucidationhasledtothedevelopmentofanewclass oftherapeutictoolsthatexploitneuroplasticitytoachievestrengtheningorcorrective neurologicalchangesinthebrainsofmanyclassesofneurologicallyimpairedindi- viduals.Adescriptionofthisscience,thetherapeuticstrategiesthatstemfromit,and theinitialapplicationofthissciencetotreatpsychiatricandneurologicalclinicalin- dicationsisthe subject ofthis volume. Itshouldbenotedthatthedevelopmentandmedicalapplicationofneuroplasticity- based therapeutics is a result of a sea change in how we view development of the physical brain and the personal evolution of our operational abilities across our life spans.Inthelatenineteenthandearlytwentiethcenturies,mostneurologicallyfocused scientistsviewedthebrainas“plastic,”thatis,physicallymodifiedbyourexperiences in ways that accounted for the acquisition and improvement of skills and abilities underlyingourremarkablebehavioralevolutionacrossourpassagethroughlife(see Boring, 1929; Hebb,1949; James, 1890; Merzenich, 2013). Primarilyin the middle decadesofthelastcentury,a“locationist”perspectiveemerged,thenpredominated. By that view, remodeling of brain connections was limited to an early “sensitive” or “critical period”; by the end of that developmental epoch in childhood, neuronal connections werebelievedtobe“hardwired,”with allbrain neuronsand supporting elementsachievingtheirmaturestatus.Postnatalchangesinthephysicalbrainwere commonly viewed as a continuation of embryological maturation (e.g., see Hubel andWiesel,2005;Hensch,Chapter1).Insum,mostneuroscientistsinthiserabelieved thatthebrainrapidlycompleteditsdevelopmentpostnatallyandfromthatpointfor- wardwasahardwired,aplasticmachine. Thisperspectivearoseinpartbecausestudiesofbrainconnectivityemployedrel- ativelycrudestrategiesfortrackingdestination-to-destinationconnectivity.Thema- jor trunk lines connecting different brain areas were shown to be modifiable in a limitedperinatalepoch,butatolderagesthereroutingofmajorconnectionalpath- wayswasnolongerachievable.Althoughwenowknowthatlarge-scale,station-to- station connectional strengthening and local network changes are occurring on a large scale, throughout life, they could not have been recorded using the crude methodsused.Studiesconductedinthemostheavilystudiedmodelsofdevelopmen- talplasticity,theemergent“ocular-dominancecolumns”and“orientationcolumns” of the primaryvisual cortex (V1; Brodmannarea 17),and the “barrel field” repre- sentingthefacialvibrissaeintheprimarysomatosensorycortex(S1)ofrodents,also contributed greatly to the locationist model. In normal animals, competitive pro- cessesinanearlypostnataldevelopmentalperiodthathadadefinedbeginningand endinginearly prenatallife resulted inabalanced,bandeddivisionoftheprimary xxi xxii Introduction visual cortex’s layer-4 zones separately dominated by the two eyes (and, in later studies,segregatingandtopographicallyorderingneuronspreferringdifferentvisual stimulusorientations)(seeHubelandWiesel,1977,2005)andintheelegantvibrissa- by-vibrissa representation of sensory facial whiskers in S1 (Woolsey and Wann, 1976).Asaresultofclosingoneeyeorremovingvibrissaethroughthisnarrowwidow oftimeinearlydevelopment,theopeneyeorremainingvibrissaecompetitively(plas- tically)capturedanexpandedcorticalterritory.Thisterritorialcompetitionbetween activeversusnonactiveanatomicalinputsforthedominationofneuronsinlayer4in V1orS1wasshowntobestrictlylimitedtoaseveral-day-toseveral-week-long“crit- ical” or “sensitive” period. While some simple manipulations could shorten or lengthenthisepochofdramaticphysicalandfunctionalremodeling,itwasarguedthat nosignificantchangesonthatscalecouldberecordedinanimalsofanolderage.How- ever,laterstudieshaveshownthatthe“anatomicalmaturation”ofocular-dominance andorientationcolumnsinV1andof“barrels”inS1isspecialtothesecorticalzones- andthatevenwiththeirhardening,large-scalelocalconnectionalremodelingcanand doesoccurasaresultofneurobehavioralengagementonalargescale,eveninthese least-plasticcorticalareas,throughoutadultlife.Themarkedplasticityofthecritical period,andthetransitionto“adult”plasticity,isstillaveryimportantaspectofany deepunderstandingofbrainplasticity.Here,thatimportantaspectofthedevelopment ofourneurobehavioralabilitiesisreviewedbytwomajor,currentcontributorstoit, Drs.HenschandKolb(Chapters1and2,respectively). Collectively,these(andmanyother)studiesledtothepredominantconclusion,in the neuroscience mainstream and in neurological and pediatric medicine, that the brainwasaplasticfromearlychildhoodonward.Brainconnectivityandlocalbrain circuitsandtheconstituentneuronswithinthem“matured”inearlylifetoachievean “adult”statusthatwasinalterable,totheendoflife.Bythisview,once“maturation” was fullyrealized,the onlyaspectofchangeinplaywasage-related deterioration. NEUROPLASTICITY Inparallelwithstudiesthatsostronglyentrenchedadoctrineofstrict“locationism,” otherexperimentsconductedprincipallybyphysiologicalpsychologistsacrossthis sameerasupportedtheviewthatthebrainwascontinuouslyplastic.Theseparallel investigationsrecordedphysical(primarilyneuroanatomical)andneuronalresponse changesinadultanimals resulting fromexposureofanimalsto“enrichedenviron- ments,” or from training them using Pavlovian (classical) conditioning (Pavlov, 1927). In the former case, studies beginning with seminal experiments conducted in the University of California laboratory of Mark Rosenzweig repeatedly showed that the cortical mantle thickened as a result of environmental enrichment (Diamond et al., 1964; Rosenzweig et al., 1962). Those thickness and volume changes, recorded in both subcortical and cortical areas, were primarilyaccounted for by dendritic, axonal arbor, and synapse elaboration that manifested large-scale connectional remodelingof local networks. Introduction xxiii In other studies conducted by physiological psychologists in the same era, re- sponsesinthebrainsofadultmammalswereshowntobealteredbyaversivePavlovian conditioningpairedwithelectricalornaturalacousticstimuli,withchangesspecificto- andappropriatelyneurologicallylocatedtoareasrelatedto-representationsofcondi- tionedandunconditionedstimuliandresponses(forreviews,seeGlucketal.,2008; Thompson,1976,2005;Weinberger,1993;WeinbergerandDiamond,1987).Impor- tantly,changesinneuronalresponsesselectivelyexaggeratedtherepresentationsofa reward-paired stimulus or a conditioned response, via both positive facilitatory and negative inhibitory remodeling. Those changes, enduring as long as conditioning wassustained,werereversedbybehavioral“extinction.” Retrospectively, it is now difficult to understand why these studies, so directly challengingastrictlocationistview,didnotsupersedetheaplasticadult-brainper- spective held by the majority of neuroscientists and medical practitioners across the decades of the 1960s through the 1990s. Fortunately, seven other classes of studies helped to demonstrate to the wider neuroscience community that the brain wascontinuously plastic, onalarge scale. We detailthese seven classes ofstudies below. First,studiesdocumentedthephenomenaoflong-termpotentiationanddepres- sion, ultimately explaining, in the terms of specific synaptic receptors and related cellular,synaptic,andmolecularprocesses,thefundamentalmechanismsthatunder- lie plasticity at all brain ages. Our current advanced understanding of the mecha- nisms underlying cortical plasticity, here summarized in Chapters 3 (by Carcea and Froemke) and 6 (Nahum et al.), is a key point of reference for all later neuroscience-guided studies that have deployed it in an attempt to control brain changesfor therapeutic purposes. Second,scientistsbegantodocumentlarge-scalecompetitiveplasticchangesfol- lowing peripheral or central injury (or stimulation) in adults, showing that those changes appeared to be accounted for by Hebb-like (coincident input-dependent) plasticity.Thatbrainremodelingfollowinginjurycanbemassive.AsDrs.Uswatte andTaub(Chapter15)describeintheirsummaryofstudiesofstrokerecoverycon- ductedin movement-impaired patients with wounded brains, large-scaleneurolog- ical remodeling provides the primary path to recovery. Drs. Pasley and Knight (Chapter17)provideuswithanotherexampleofplasticity-mediatedrecoveryinpa- tientswho have degradedlanguage abilities arisingfrom brain injury or stroke. Third,changesexplainingprogressiveperformanceimprovementsachievedvia operantconditioningprovidedamoredirectandmorecompleteaccountingforthe evolutionofhumanperformance abilities, showingthatthe acquisition orprogres- siveimprovement ofaskillorabilityatanyage oflifewas directlyattributableto connectional(andotherphysical)remodeling(seeMerzenich,2013).Thesestudies alsofarmorecompletelyexplainedchangephenomenaintermsoflocalcorticalnet- worksandtheirbehaviorallydrivenremodeling.Ourownstudiesdirectlystemfrom thisclassofexperiments(seeNahumetal.,Chapter6;Tallal,Chapter7).Mostofthe computer-deliveredtherapeuticstrategiesdescribedlaterinthisvolumeapplythese neuroplasticity-informed operant-conditioning procedures. xxiv Introduction Fourth,scientistsbegantodocumenttheneurologicalbasesofthemodulationof plasticityasafunctionofbehavioralcontext,instudiesrichlyinformedbynearlya centuryofempiricalexperience-andlearning-relatedresearchcontributedbyexper- imental and physiological psychology (see Buonomano and Merzenich, 1998). Thesestudiesareespeciallyimportantforourconsiderationhere,becausetheyfur- ther delineate the necessary and optimum conditions for driving positive plastic changesinthebrain,andexplainhowinappropriatelydesignedtherapeuticregimes canbeineffective,orcanhaveevennegativeconsequences.Childandadultstudies haverichlydrawnfromthisexperimentalpsychologyandneuroscienceliterature,to evolvethedesignsofremedialtrainingprogramsthatarecontrollingandrewarding inwaysthatassuretherapeuticsuccess. Theelegantscienceelucidatingthe neuro- modulatory control of plasticity led Kilgard (see Hays et al., Chapter 11) and Van VleetandDeGutis(Chapter13)tothedevelopmentoftrainingstrategiesspecifically also targeting the plasticity ofthe modulatory controlmachinery itself, illustrating that even the machinery that controlsplasticity isplastic. Fifth, many studies have now shown that plasticity is achieved via reversible physicochemicalchangeprocesses.Wehaveknownformanyyearsthat,atthecore, plasticity follows a Hebbian rule. That led to our understanding of how we could refine or degrade the brain’s representation of the details of what we hear or see orfeel;inthiscase merelychanging the timestructuresanddistributionsofinputs deliveredcompetitivelyintobrainnetworksundertherightplasticity-enablingcon- ditions(MerzenichanddeCharms,1996;Merzenich,2000).Morerecently,wehave shownthatthemachineryofthebrain“deteriorates” invirtuallyallfunctionaland physicalaspectswithaging,oracrossthecourseofchronicneurologicalillness(see deVillers-Sidanietal.,2010,2011).Animportantconclusionofthesestudiesisthat thechangesinthebrainnormallyassociatedwithagingorwiththeprogressivede- teriorationinfunctionmarkingmostneurologicalandpsychiatricillnessesareactu- allytheresultofprogressive,“negative,”plasticity-drivenchanges.Moreover,and importantly for the subject at hand, all of these physical and functional changes markingthedeteriorationordegradationofbrainanatomyandfunctionarerevers- ible,viaappropriateformsoftraining.Wedescribefurtherkeyaspectsofthisscience in ourown contribution tothis volume (Nahum et al., Chapter 6). Sixth,especiallyoverthepastdecade, cognitive neuroscienceapplyingmodern toolsofbehavior andbrainrecordingandimagingsciencehave shownus,now by manyexamples,thathumanconnectivityandmanyaspectsofthebrain’sphysicality, chemistry,andfunctionalityarealteredinparallelwiththeacquisitionorlossofskill orabilityinwaysthatappeartoaccountforthosegainsorlosses.Here,Obermanand Pascual-Leone(Chapter4)andJacobyandAhissar(Chapter5)leadusintoimportant introductions of this powerfully contributing and rapidly evolving contributor to brainplasticity-guidedneurorehabilitation. Finally, we have now applied this science directly, to drive positive changes affirmedbycontrolledtrials,inthebehaviorandintheneurologyofarichvariety ofhumanpatients(seeMerzenich,2013).Thesepracticalstudiesrichlydemonstrate the power and potential of neuroplasticity-based therapeutics. In this volume,
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