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NEUROCIRCUITRY OF ADDICTION This page intentionally left blank NEUROCIRCUITRY OF ADDICTION Edited by N W. G ICHOLAS ILPIN LSUHealthSciencesCenter, USA AcademicPress isanimprintofElsevier 125London Wall,London EC2Y5AS,UnitedKingdom 525BStreet,Suite1650,SanDiego,CA92101,UnitedStates 50HampshireStreet,5thFloor, Cambridge,MA02139,UnitedStates TheBoulevard,Langford Lane,Kidlington,OxfordOX5 1GB,UnitedKingdom Copyright©2023ElsevierInc.Allrightsreserved. Nopart ofthispublicationmay bereproduced ortransmittedinanyformor byanymeans, electronicor mechanical, includingphotocopying, recording,oranyinformation storageandretrieval system,without permissioninwritingfrom thepublisher.Details onhowtoseekpermission, further informationaboutthe Publisher’spermissions policies andourarrangements withorganizations suchastheCopyrightClearance CenterandtheCopyrightLicensingAgency,canbefoundatourwebsite:www.elsevier.com/permissions. Thisbookandtheindividualcontributionscontained initareprotected undercopyrightbythePublisher (otherthanasmaybenotedherein). Notices Knowledgeandbestpracticeinthisfieldareconstantlychanging. Asnewresearch andexperiencebroaden ourunderstanding, changesinresearchmethods,professional practices,ormedicaltreatment maybecome necessary. Practitionersandresearchers mustalwaysrelyontheir ownexperienceandknowledgeinevaluating andus- ingany information,methods,compounds,orexperiments describedherein.In usingsuchinformation or methodstheyshouldbemindfuloftheirown safetyandthesafetyofothers,includingpartiesforwhom theyhave aprofessionalresponsibility. Tothefullestextentofthelaw,neitherthePublishernortheauthors,contributors, oreditors,assume any li- abilityforanyinjury and/ordamagetopersonsorproperty asamatterofproductsliability, negligenceor otherwise,orfrom anyuseoroperation ofany methods,products,instructions, orideascontainedinthe materialherein. ISBN:978-0-12-823453-2 Forinformation onallAcademic Presspublications visitourwebsite at https://www.elsevier.com/books-and-journals Publisher:NikkiP.Levy Acquisitions Editor: JoslynT.Chaiprasert-Paguio EditorialProjectManager:SaraPianavilla ProductionProjectManager:Fahmida Sultana CoverDesigner: Christian J.Bilbow TypesetbyTNQTechnologies Contents Contributors ix Drugaddictionandlong-term memory 58 Preface xi VTAdopamineneuronsandrelapseto seekingdrugs ofabuse 59 VTADAneuronsandtheiroutputsinreinstatement 1. Leveraging circuits to todrugseeking 59 understand addiction InputstoVTADAneuronsandreinstatementto MichaelC.Salling drugseeking 60 Acknowledgments 62 Introduction 1 References 62 Identificationofneuralcircuits implicatedin addiction:whereto start? 3 3. Striatal circuits Humanhistopathological techniques 3 Applicationofmolecular biologytechniques to MichaelS.PattonandBrianN.Mathur humansamples 5 Introduction 73 Neuroimaging techniquesinclinical studies 7 Anatomyofthestriatum 74 Preclinical researchmethodstoidentify circuits Thestriatum: cellsandcircuits 76 andtheiradaptationsto addictivedrugs 10 Thestriatumin actionselection 80 Neuraltracingtechniques 11 Thenucleusaccumbens:motivatedbehaviorand Conventionaltracers 12 addiction 81 Characterization ofcircuits throughcelltype Thedorsalstriatum: motivated behaviorand identification 13 addiction 84 Genetic approachesto identifyingcircuits 15 Stress,habits,andaddiction 87 Genetic targetingapproaches 16 Striatal circuitsinmotivated behaviorand Viral vectorapproaches todissecting neural addiction 88 circuits 20 Inhibitory striatalcircuits inmotivated behaviorand Identifying neuroadaptations inneuralcircuits 22 addiction 102 Conclusions 38 Sexdifferencesin substanceusedisorder 104 References 39 Conclusions 106 Bibliography 106 2. Midbrain (VTA) circuits MariselaMoralesandM.FlaviaBarbano 4. Prefrontal Cortical (PFC) circuits VTAheterogenousneuronalcomposition 47 MatthewC.HearingandJohnR.Mantsch VTAneuronalactivity isregulatedbyconverging Introduction 125 inputsfrommultiplebrainareas 50 Functionalneuroanatomy ofthePFC 126 Plastic changesassociatedwithdrugintakein PFCdysfunctionandaddiction 129 midbraindopaminecircuits 51 StructureandphysiologyofthePFC 135 VTADAneuronsandpathwaysinvolvedinthe Drug-inducedadaptations 137 reinforcing effectsofdrugsofabuse 52 Impactof biologicalsex,stress,andpreexisting VTADAneuronsandwithdrawal 55 differences onaddictionandPFCfunction 145 Transitionto compulsioninaddiction 58 v vi CONTENTS Conclusions 149 9. Bed Nucleus of Stria Terminalis References 150 (BNST) circuits 5. Insular Cortical circuits SamuelW.Centanni,JordanA.Brown,KellieM.Williford, ElizabethA.Flook,JosephR.Luchsingerand ChristineIbrahimandBernardLeFoll DannyG.Winder Insula neuroanatomyandstructure 171 Introduction 321 Functionsoftheinsula 174 BNSTsubregionsandcelltypes 322 Evidenceimplicatingtheinsula inaddiction 177 BNSTafferents andefferents 328 Conclusions 195 Effectsofacuteandchronicdrugexposureonthe References 197 BNST 338 Longtermeffects ofdrugsofabuseonthe 6. Thalamic circuits BNST 344 AlessandraMatzeu,FranciscoJ.Flores-Ramirez Chemogeneticandoptogeneticcircuitmanipulation andRémiMartin-Fardon intheBNST 350 TranslationalworkinthehumanBNST 352 Overviewofthethalamus 209 Futureof BNSTcircuitryandaddiction 354 Thethalamus andsubstance usedisorder: References 355 overview 211 Thethalamus:humanstudies 212 10. Noradrenergic circuits Thethalamus:preclinical studies 217 Theparaventricularnucleusofthethalamus: ZoéA.McElligott,MadiganL.Bedard,SaraY.Conley, preclinicalstudies 218 IsabelM.Bravo,ElizabethS.Cogan andAnthonyM.Downs Other thalamicnuclei 225 Conclusions 231 Norepinephrinesynthesis, storage,receptors, Acknowledgments 231 transporters, andmetabolism 375 References 231 Anatomy/developmentofnorepinephrine circuits 377 7. Hippocampal circuits Norepinephrineinvolvementinstress, arousal,and locomotion 381 ChitraD.Mandyam Neurochemical techniquesusedformeasuring brain Introduction 247 NEcellandcircuitactivity 382 Hippocampalformation 248 Manipulating/probingNE circuits 383 Synapticplasticity inthehippocampus 248 Norepinephrineandopioids 386 Regulationofplasticity inthehippocampusby Norepinephrineandalcohol 390 addictivedrugs 258 Norepinephrineandpsychostimulants 392 Cocaine 260 Norepinephrineandothersubstancesofabuse 394 Alcohol 264 Norepinephrine,naturalrewards/psychosocial Conclusions 269 reward 396 Acknowledgments 270 Conclusions 398 References 270 References 398 8. Amygdala circuits 11. Cholinergic modulation of circuits LieselotL.G.Carrette,ElizabethA.SneddonandOlivierGeorge NiiA.Addy,ChristieD.FowlerandRobertJ.Wickham Introduction 289 Thediscoveryofacetylcholine 410 Conclusions 309 Fromnodestocircuits 411 Fundingsources 310 Acetylcholineanatomyandcircuitry 411 References 310 Acetylcholinemediated behaviors 416 vii CONTENTS Reward-related signaling:mesopontine tegmentumto Fundinganddisclosure 478 VTAcircuit 417 References 478 Cholinergic circuitsintheNAc 422 Roleofacetylcholineinthebasolateral 13. Circadian circuits amygdala 426 MackenzieC.GambleandRyanW.Logan Roleofacetylcholineintheprefrontal cortex 427 Aversion-related signaling: habenulato Introduction 497 interpeduncularcircuit 427 Circadianrhythms 498 Septalcircuits 432 Molecularclocks, reward,andsubstanceuse 504 Cerebellum 434 Circadianmodulation ofneuralcircuitryinvolvedin Conclusions 434 substancereward 509 References 435 Environmentalcircadianperturbations andsubstance use 512 12. Gut-brain axis Chronotypeimpactsreward neuralcircuit functions 515 KellyM.AbshireandLorenzoLeggio Lossofrhythmsandloss ofcontrol 515 Introduction 445 Conclusions 516 Thegut-brainaxis 446 References 517 Gastrointestinal neuroendocrinepathways 446 Microbiome 467 Index 535 Conclusions 477 This page intentionally left blank Contributors Kelly M. Abshire Clinical Psychoneur- Sara Y. Conley Neuroscience Curriculum, Uni- oendocrinology and Neuropsychopharma- versity of North Carolina at Chapel Hill, cology Section, Translational Addiction ChapelHill,NC,UnitedStates Medicine Branch, National Institute on Drug AnthonyM.Downs BowlesCenterforAlcohol AbuseandNationalInstituteonAlcoholAbuse Studies,UniversityofNorthCarolinaatChapel and Alcoholism, National Institutes of Health, Hill,ChapelHill,NC,UnitedStates Baltimore,MD,UnitedStates M. Flavia Barbano National Institute on Drug Nii A. Addy Department of Psychiatry, Yale Abuse (NIDA/NIH), Baltimore, MD, United School of Medicine, New Haven, CT, United States States; Yale Tobacco Center of Regulatory Sci- Elizabeth A. Flook Vanderbilt Center for ence,YaleSchoolofMedicine,NewHaven,CT, Addiction Research, Vanderbilt University United States; Department of Cellular and SchoolofMedicine,Nashville,TN,UnitedStates MolecularPhysiology,YaleSchoolofMedicine, New Haven, CT, United States; Inter- Francisco J. Flores-Ramirez Department of departmental Neuroscience Program, Yale Molecular Medicine, The Scripps Research University,NewHaven,CT,UnitedStates;Wu Institute,LaJolla,CA,UnitedStates TsaiInstitute,YaleUniversity,NewHaven,CT, Christie D. Fowler Department of Neuro- UnitedStates biologyandBehavior,UniversityofCalifornia, Madigan L. Bedard Department of Pharmacol- Irvine,Irvine, CA,UnitedStates ogy, University of North Carolina at Chapel Mackenzie C. Gamble Molecular and Transla- Hill,ChapelHill, NC,UnitedStates tional Medicine, Graduate Medical Sciences, Isabel M. Bravo Bowles Center for Alcohol Department of Medicine, Boston University Studies,UniversityofNorthCarolinaatChapel SchoolofMedicine,Boston,MA,UnitedStates; Hill,ChapelHill, NC,UnitedStates Department of Pharmacology and Exper- imentalTherapeutics,BostonUniversitySchool Jordan A. Brown Vanderbilt Center for Addic- ofMedicine, Boston,MA,UnitedStates tion Research, Vanderbilt University School of Medicine,Nashville,TN,UnitedStates Olivier George Department of Psychiatry, University of California San Diego, La Jolla, Lieselot L.G. Carrette Department of Psychia- CA,UnitedStates try,UniversityofCaliforniaSanDiego,LaJolla, CA,UnitedStates MatthewC.Hearing DepartmentofBiomedical Sciences, Marquette University, Milwaukee, Samuel W. Centanni Vanderbilt Center for WI,UnitedStates Addiction Research, Vanderbilt University School of Medicine, Nashville, TN, United Christine Ibrahim Translational Addiction States ResearchLaboratory,CentreforAddictionand Mental Health, Toronto, ON, Canada; Depart- Elizabeth S. Cogan Bowles Center for Alcohol mentofPharmacologyandToxicology,Faculty Studies,UniversityofNorthCarolinaatChapel of Medicine, University of Toronto, Toronto, Hill,ChapelHill, NC,UnitedStates ON,Canada ix