2005b The primate amygdala neuronal representations of the v

Abstract—The primate amygdala is implicated in the control of behavioral responses to foods and in stimulus-reinforcement learning, but only its taste representation of oral stimuli has been investigated previously. Of 1416 macaque amygdala neurons record

Neuroscience132(2005)33–48

THEPRIMATEAMYGDALA:NEURONALREPRESENTATIONSOFTHEVISCOSITY,FATTEXTURE,TEMPERATURE,GRITTINESSANDTASTEOFFOODS

M.KADOHISA,J.V.VERHAGENANDE.T.ROLLS*

UniversityofOxford,DepartmentofExperimentalPsychology,SouthParksRoad,OxfordOX13UD,UK

Abstract—Theprimateamygdalaisimplicatedinthecontrolofbehavioralresponsestofoodsandinstimulus-reinforcementlearning,butonlyitstasterepresentationoforalstimulihasbeeninvestigatedpreviously.Of1416macaqueamygdalaneu-ronsrecorded,44(3.1%)respondedtooralstimuli.Ofthe44orallyresponsiveneurons,17(39%)representtheviscosityoforalstimuli,testedusingcarboxymethyl-celluloseintherange1–10,000cP.Twoneurons(5%)respondedtofatinthemouthbyencodingitstexture(shownbytheresponsesoftheseneu-ronstoarangeoffats,andalsotonon-fatoilssuchassiliconeoil((Si(CH3)2O)n)andmineraloil(purehydrocarbon),butnoorsmallresponsestothecelluloseviscosityseriesortothefattyacidslinoleicacidandlauricacid).Ofthe44neurons,three(7%)respondedtogrittytexture(producedbymicrospheressus-pendedincellulose).Eighteenneurons(41%)respondedtothetemperatureofliquidinthemouth.Someamygdalaneuronsrespondedtocapsaicin,andsometofattyacids(butnottofatsinthemouth).Someamygdalaneuronsrespondtotaste,tex-tureandtemperatureunimodally,butotherscombinetheseinputs.Theseresultsprovidefundamentalevidenceabouttheinformationchannelsusedtorepresentthetextureand avoroffoodinapartofthebrainimportantinappetitiveresponsestofoodandinlearningassociationstoreinforcingoralstimuli,andarerelevanttounderstandingthephysiologicalandpathophys-iologicalprocessesrelatedtofoodintake,foodselection,andtheeffectsofvarietyoffoodtextureincombinationwithtasteandotherinputsonfoodintake.©2005PublishedbyElsevierLtdonbehalfofIBRO.

Keywords:appetitivelearning,Pavlovianconditioning,obesity,foodintake,reward.

Theamygdalaisimplicatedinemotionandmotivationbylesion,singleneuronrecording,andneuroimaginginvestiga-tions(Sangheraetal.,1979;Nishijoetal.,1988a;Davis,1994;Francisetal.,1999;Rolls,1999;Schoenbaumetal.,1999;LeDoux,2000;Rolls,2000).Partofthefunctionoftheamygdalainmotivationandemotionappearstobeinasso-ciatingpreviouslyneutral(e.g.auditoryorvisual)stimulitoprimary(unlearned)reinforcerssuchastasteandsomato-sensoryincludingpainfulstimuli(Davis,1994;Rolls,1999,2000;LeDoux,2000),andinprimates,forexample,rewarddevaluationlearningdependsontheamygdala(Murrayetal.,

*Correspondingauthor.Tel: 44-1865-271348;fax: 44-1865-310447.E-mailaddress:edmund.rolls@psy.ox.ac.uk(E.T.Rolls).

Abbreviations:BJ,blackcurrantjuice;CMC,carboxymethylcellulose;CO,coconutoil;GR,grittytexturestimulus;LaA,lauricacid;LiA,linoleicacid;MO,mineraloil;SaO,saf oweroil;SC,singlecream;SiO,siliconeoil;VO,vegetableoil.

0306-4522/05$30.00 0.00©2005PublishedbyElsevierLtdonbehalfofIBRO.doi:10.1016/j.neuroscience.2004.12.005

1996).Thisassociativefunction(RollsandTreves,1998)impliesarepresentationofprimaryreinforcerssuchasthetasteoffood,andindeedtasteneuronshavebeendescribedintheamygdala(Sangheraetal.,1979;Nishijoetal.,1988a,b;Scottetal.,1993;YanandScott,1996)andtasteresponsivenessinthehumanamygdala(O’Dohertyetal.,2001).Almostnothingisknown,however,aboutwhetheraspectsoffoodotherthantasteandsmellarerepresentedintheamygdala.Thetextureoffoodisimportantinitspalatabil-ityandacceptability(Bourne,2002,considere.g.dampce-realorpotatochips),andtemperaturemayalsobeimportant(Zellneretal.,1988).Wedescribehereforthe rsttimetheresponsesofprimateamygdalaneuronstooraltextureandtemperaturestimuli,andshowthattheyarecombinedinsomeneuronswithresponsivenesstothetasteoffood.Theinvestigationwasperformedinmacaquesinordertomakeitasrelevanttounderstandingtheoperationofthissysteminhumansaspossible,andinthecontextthatthetastesystemisdifferentlyconnectedinrodentsandprimates,withtastepathwaysinprimatestotheamygdalaonlyaftercorticalprocessing(Norgren,1984;Rollsetal.,2003).Understand-ingthefactorsthatdeterminethepalatabilityoffoodiscur-rentlyofgreatinterest,giventheroleofpalatabilityinthecontroloffoodintake,andtherapidlyincreasingincidenceofobesitywhichisaccompaniedbyserioushealthrisks(Berthoud,2003;SteinbergerandDaniels,2003).Thefactorsinvestigatedincludedthetextureoffoodasre ectedbyvis-cosity(testedparametricallywithaviscosityseriesmadewithcellulose);oralfat;oralfattyacidswhichmightsignalthepresenceoffatinthemouthifsalivarylipasewaspresent(Gilbertson,1998);oraltextureasmanipulatedbyinertmi-crospheres;oraltemperature;taste;andtheeffectsofcap-saicin,anoralirritantpresentinanumberoffoods.

EXPERIMENTALPROCEDURES

Subjects

Therecordingsweremadeinthreehemispheresoftworhesusmacaques(Macacamulatta;onefemaleweighing2.6–3.3kgandonemaleweighing6.1–6.7kg).Toensurethatthemacaqueswerewillingtoingestthetestfoodsand uidsduringtherecordingsessions,theywereonmildfood(150gofnutritionallybalancedmashplusfruits,boiledchickeneggs,nuts,seedsandpopcorn)and uid(1h/dayadlibitumwater)deprivation,inthatbothwereprovidedafterthedailyrecordingsession.Themonkeysshowedsteadyincreasesinbodyweight.Allprocedures,includingprepar-ativeandsubsequentones,werecarriedoutinaccordancewiththeNationalInstitutesforHealthGuidefortheCareandUseofLaboratoryAnimals,andwerelicensedundertheUKAnimals(Scienti cProcedures)Act,1986,andweredesignedtominimize

33

Abstract—The primate amygdala is implicated in the control of behavioral responses to foods and in stimulus-reinforcement learning, but only its taste representation of oral stimuli has been investigated previously. Of 1416 macaque amygdala neurons record

34M.Kadohisaetal./Neuroscience132(2005)33–48

thenumberofanimalsusedandmaximizetheirwelfarebyadopt-ing,forexample,grouphousing,andenvironmentalenrichments.

Recordings

…… 此处隐藏：60043字，全部文档内容请下载后查看。喜欢就下载吧 ……