ProbingbehavioralresponsestofoodDevelopmentofafoodspecigonogotaskTh - PDF document

1 Probingbehavioralresponsestofood:Develop
Probingbehavioralresponsestofood:Developmentofafood-specigo/no-gotaskTheresaTeslovich,EveK.Freidl,KatrinaKostro,JuliaWeigel,JulietY.DavidowMeganC.Riddle,ChelseaHelion,MichaelDreyfuss,MichaelRosenbaum Contentslistsavailableatjournalhomepage:www.elsevier.com/locate/psychresPsychiatryResearchhttp://dx.doi.org/10.1016/j.psychres.2014.04.0530165-1781/2014ElsevierIrelandLtd.Allrightsreserved. Correspondingauthor.Tel.:12125435741.E-mailaddresses:tteslovich@gmail.com(T.Teslovich),lsm16@columbia.edu(L.Mayer). PsychiatryResearch219(2014)166170 circuitstothesamedegreeashealthycontrols(Marshetal.,2009Clinically,patientswithanorexianervosadisplayaremarkableabilitytocontroltheirfoodintakebehavior(Mayeretal.,2012anddemonstrateenhancedabilitytodelaymonetary(e.g.non-food)rewards(Steinglassetal.,2012Whenstudyingeatingdisorders,itisimportanttobeabletodistinguishbehavioraldifferencesinfood-specicself-controlfromcharacteristicdevelopmentaldifferencesinoverallimpulsivity.Eatingdisordersoftenrstmanifestduringadolescence,butnotuncom-monlypersistintoadulthood,whereasimpulsecontrol,graduallyimprovesfromchildhoodtoearlyadulthood.Additionally,subjectivesensitivitytoappetitivecuesinourenvironmentgreatlyinourabilitytoexertself-control.Sensitivitytoenvironmentalcueshasbeenshowntodifferacrossdevelopmentandwithinpopulationsandcandrivedifferencesseeninself-control,whereoverallimpulsivitymeasuresareunabletocapturethisvariability.Othershavemodiedthetraditionalgo/no-gotasktoexamineimpulsecontrolusingfoodcues(Batterinketal.,2010;Mobbsetal.,2011;Jasinskaetal.,2012;Loeberetal.,2012;Meuleetal.,2012;Loeberetal.,2013);however,thetasksvaryindesign,andresultsareinconsistentacrossstudies.Someusingvegetables(gotarget)anddesserts(no-gonon-target)havefoundpositiveassociationsbetweencommissionerrorstohigh-caloriefood(dessert)cuesandbodymassindex(BMI)(Batterinketal.,2010),however,thelackofaneutralcontrolconditionmakeitdifculttoestablishwhethertheassocia-tionwasduetolowerinhibitorycontrolingeneralorwasfood-mediated.Othershaveusedfoodandnonfoodwordsinhungryhealthy(Loeberetal.,2013)andobese(Mobbsetal.,2011;Loeberetal.,2012)populationstoshowdiminishedinhibitorycontrolinresponsetofood-associatedcues.Theuseofwordsastargetsandnontargets,however,greatlylimittheapplicationofthesetasks.Forexample,whenfoodcuesarewordsratherthanpictures,develop-mentaldifferencesinreadingabilityandabstractthoughtwilluenceperformance.Suchtaskswouldbedifculttouseearlyindevelopmentwhenchangesineatinghabitsbegintoemerge.Recently,variantsofthego/no-gotaskusingpictureshavefoundrateofcommissionerrorstobeassociatedwithaspectsofunhealthyeating(specically,emotionaleating)(Jasinskaetal.,2012),aswellasfasterreactionstimesonamodiedgo/no-go-attentiontaskwhenfoodpictureswerepresentedbehindthetargets(Meuleetal.,2012).Thesendingsareconfounded,however,byalackofneutralcomparisonconditionorhomogeneityoffoodstimuli(onlyhigh-caloriedesserts),respectively.Withoutthesecomparisons,itisculttodeterminetheextenttowhichthedecreaseininhibitorycontrolisdrivenbyfoodandmorespecicallytypesoffoodthatarecommonlyassociatedwithunhealthyeatingbehaviors.Whilethesestudiesexemplifyhowpsychologicaltaskscanbeedtomeasureimpulsesrelevanttoeatingbehavior,thefollowingstudyattemptstoaddresspotentiallimitationsofexist-ingfoodgo/no-gotasks.Weintroduceanupgradedfoodgo/no-gotaskthatusespicturesoflow-andhigh-caloriefoodstimuliandinterestingnonfoodstimulitotestthespecicinuenceofappetitivefoodcuesonself-control.BasedonpreviousstudiesCaseyetal.,1997;Durstonetal.,2002;Somervilleetal.,2011),wehypothesizedthatoverallimpulsecontrolwouldincreaseacrossagegroupsandthatparticipantswouldexhibitmorebehavioralinterferencetotheappetitivefoodcuescomparedtotheneutralnonfoodcues,especiallytothehigh-caloriefoodcues.2.Methods2.1.ParticipantsParticipantswere147normal-weight,healthyvolunteers(96females)betweentheagesof5and30years.Heightwasmeasuredincentimeterstothenearest0.1cmusingawall-mountedstadiometer(Detecto3PHTROD-WM),andweightwasmeasuredinlightclothingoneitherabeambalancescale(Detecto)oradigitalmedicalscale(HealthOMeter349KLX)tothenearest0.1kg.Participantswereaskedtoremovetheirshoesforbothmeasurements.BMIwascalculatedasweight(kg)dividedbyheight(m)squared.PotentialparticipantswerescreenedwithabriefclinicalinterviewconductedbyanMD-orPhD-levelclinician.Healthyindividualswithnosignicantmedicalillness,neurologichistoryoforactiveAxisIpsychiatricdisorder,andBMIlessthan30kg/mwereincluded.ParticipantswithknownAttentionDecitHyperactivityDisordersorlearningdisabilitywereexcludedduetoknownperformancedifferencesonstandardgo/no-gotasks.ThisstudywasapprovedbytheNewYorkStatePsychiatricInstitute/ColumbiaUni-versityDepartmentofPsychiatryInstitutionalReviewBoard.ParticipantswererecruitedthroughstreetfairsandstudyyerspostedthroughouttheNewYork-PresbyterianHospitalsofColumbiaUniv

2 ersityMedicalCenterandWeillCornellMedica
ersityMedicalCenterandWeillCornellMedicalCenter.Priortostudyparticipation,allchildandadolescentparticipantsassentedandtheirparentsandadultparticipantsprovidedwritteninformed2.2.StimuliThesetofstimuliconsistedof30colorimagesofcommonhigh-(8)andlow-calorie(7)foodsandcommontoys(15)(seeSupplementalFig.1).Priortotheexperiment,anindependenttestgroupratedeachimageonvalence(e.g.Howprettyisthisimage?Howfamiliaristhisimage?),andarousal(e.g.Howexcitingisthisimage?)ona7-pointlikertscale.Intra-classcorrelationcoefcientsandCronbach'salphawerealsousedasmeasuresofinter-raterreliabilityingeneratingnalstimulusset.ThesedataarereportedinSupplementalTable12.3.BehavioralparadigmThego/no-gotaskwasprogrammedandadministeredusingE-Prime2.0pre-sentationsoftware(PsychologySoftwareTools,Inc.Pittsburgh,PA).Thetarget)stimuliappearedin75%ofthetrials,inordertodevelopaprepotentresponsepattern,andnontargetsappeared25%ofthetime.Thetaskwasadministeredacrossfourrunswitheachcuetypeservingasbothatargetandnontarget.Becauseofthepotentialvariabilityacrossindividualsofdifferentagesinconsistentlyidentifyingfoodsashigh-orlow-calorie,participantswerenotaskedtodistinguishbetweenhigh-andlow-caloriefoods.Rather,foodimagesweregroupedbycalorielevel(highorlow)andpresentedinseparateruns.Thatis,participantswerepresentedwiththegeneralinstruction:Pressthespacebarwhenyouseefood.Don'tpressforanyotherpictures,onlyfood.Goasfastasyoucanwithoutmakinganymistakes.Withinagivenrun,thefoodimagespresentedwereeitherallhigh-calorieoralllow-calorie.Stimuliwerepresentedfor500ms,withavariable,inter-trialintervalof20004000ms(Fig.1).Theorderofthefourconditionsofhigh-caloriefoodwithtoy,low-caloriefoodtoy,toywithhigh-caloriefood,andtoywithlow-calorie,werecounter-balancedacrossparticipants.Participantswerepre-sentedwithathree-minutepracticesessiontoensuretheyunderstoodandcouldfollowtheinstructions,followedby192trials(12min). Fig.1.Schematicoffoodgo/no-gotask.Examplesoffood,nonfoodtrials.Here,participantswereinstructedtopressthespacebartofood(top:high-calorie;bottom:low-calorie).T.Teslovichetal./PsychiatryResearch219(2014)166170167 2.4.StatisticalanalysisAgeandBMIscoreswerecomparedacrossthethreeagegroupsof539),1317(49)and1859)yearoldsusingananalysisofvariance(ANOVA,SPSSversion20,IBMCorporation).ThreeseparateANOVAswereusedtocompareeachprimaryoutcomevariableusingbetween-subjectfactorsofagegroup(children,adolescents,adults)andgender(male,female),andwithin-subjectfactorsofcuetype(toy,low-caloriefoodorhigh-caloriefood).ABonferronicorrectionformultiplecomparisonswasemployedforthethreeANOVAs(0.016).Primaryoutcomevariablesincluded:(1)overallreactiontime(RT)inmillisecondsduringcorrecttrials,(2)rateofomissionerrors(missedtrials),and(3)falsealarmrate(rateatwhichparticipantserroneouslypresstoano-gostimulus).Withineachsubject,RTsgreaterorlessthanthreestandarddeviationsoftheirmeanwereexcludedfromtheanalyses.ThetworunsinwhichtoyswerethetargetswereaveragedtoderivemeanRTsandrateofomissionerrorsforthetoyconditionforeachparticipant.Similarly,thetworunsinwhichtoyswerethetargetswereaveragedtoderivemeanfalsealarmratestotoysforeachparticipant.Post-hoctestswereconductedtofurtherinterrogatemaineffectsandBonferronicorrectedformultiplecomparisons.3.ResultsDatafrom146participants(39children,49adolescentsand58adults)wereincludedintheanalyses.Datafromoneadultwereexcludedduetoamisunderstandingoftheinstructions,whereheonlyrespondedtothepresenceoffruits.DemographicinformationforeachagegroupispresentedinTable1.TherewasamaineffectofagegroupinrawBMIscores((2,121)25.49,0.001),where-testsrevealedthatchildrensignicantlydifferedfrombothadolescents((73)0.001)andadults(7.11,0.001).TherewasnodifferenceinBMIbetweentheadultandadolescentgroups.BMIpercentiles,basedonCDCBMI-for-agegrowthchartsformalesandfemales(Kuczmarskietal.,2002werecalculatedforparticipantsbetweentheagesof5and20forwhomwehadBMImeasures(94)tocontrolforagedifferences.Theresultingpercentilesdidnotcorrelatewithtaskperformancenordidtheyshowanyageeffectsforthishealthynon-obeseandnon-disorderedsample.Next,a3(condition:toys,low-caloriefood,high-calorie3(group:children,adolescents,adults)2(gender:male,female)mixedgenerallinearmodelwasperformedforeachofthefollowingprimaryoutcomevariables:meanreactiontime(RT),rateofomissionerrors,andfalsealarmrate.3.1.MeanreactiontimeThereweremaineffectsofcondition((1,140)31.48,0.001),andagegroup((2,140)13.37,0.001)formeanRT(seeTable2Themaineffectofconditionshowedthatparticipantswerequickertorespondtobothlow-calorie((145)5.98,0.001)andhigh-calorie((145)5.79,0.001)foodsrelativetotoys,buttherewasnodifferenceinRTbetweenlow-andhigh-caloriefoodgotrials((145)0.10,0.9).Themaineffectofagegroupshowedthatchildrenwereslowerthanbothadolescents(4.99,0.001)andadults(3.93,0.001),buttherewasnodifferenceinRTbetweenadolescentsandadults((105)1.65,0.1).Therewerenooth

3 ersignicantmaineffectsorinteractions.3.2
ersignicantmaineffectsorinteractions.3.2.MeanomissionerrorsThereweremaineffectsofagegroup((2,140)14.89,0.001,Table2)andgender((1,140)7.97,0.005)formeanaccuracyongotrialswithgreateraccuracyinadultsrelativetochildren(0.001)andadolescents((105)4.1730.001).Therewasonlyatrendfordifferencesbetweenchil-drenandadolescents(1.981,0.051).Femalesperformedbetterthanmales((144)0.01).Therewerenoothercantmaineffectsorinteractions.3.3.MeanfalsealarmrateThereweremaineffectsofcondition((1,140)21.76,0.001),agegroup((2,140)42.77,0.001),andgender((1,140)6.01,0.015)withmorefalsealarmstobothlow-((145)6.73,0.001)andhigh-calorie((145)5.14,0.001)foodsthannonfoods(seeTable2).AswasthecaseinRT,therewasnodifferenceinfalsealarmratesbetweenthetwocategoriesoffoodstimuli((145)1.45,0.15).Themaineffectofagegroupshowedthatadultshadfewerfalsealarmsonno-gotrialsthanadolescents((105)6.10,0.001)orchildren(10.610,0.001)andadolescentshadfewerfalsealarmsthanthechildren(4.13,0.001).Femalesmadefewerfalsealarmsthanmales((144)2.482,0.015).Therewerenoothersig-cantmaineffectsorinteractions.4.DiscussionThecurrentstudyintroducesataskthatutilizesbothappetitiveandneutralcuestoexaminebehavioralinhibitioninthefaceofrewardingfoodcuesrelativetononfoodcues.Ourfood-specicgo/no-gotaskmanifeststhedevelopmentally-expectedagediffer-encesintaskperformanceanddemonstratesaneffectofstimulustype,namelyfoodversustoytargets,onbehavior.Reactiontimeswereexpectedlyslowerinchildrencomparedtoadolescentsandadults,consistentwiththeirstageofbrainandmotordevelopment.However,acrossallagegroups,reactiontimestofoodcueswereconsistentlyfastersuggestingincreasedsalienceoffoodrelativetononfoodcues.Interestingly,thedifferenceinreactiontimesbetweenfoodsandtoysremainedessentiallyconstantacrossgroups,suggestingthatsensitivitytofoodcues(relativetononfooditems)developsearlyandismaintainedacrossdevelopment.Thoughonemightexpectthechildrentobemoremotivationallydrivenbythetoys(oratleastequallydrivenbyfoodsandtoys),thisearlyemergingsensitivitytofoodcuesspeakstotheroleoffoodasapotentprimaryreinforcerthroughoutdevelopment.Itisnotablethatthestudysamplewas Table1ChildrenAdolescentsAdultsAge(years)9.31(1.98)15.1(1.39)22.52(3.61)305.750.001BMI(kg/m)18.053.04)22.29(3.35)22.26(2.32)25.490.001BMI(Percentiles)58.7(32.5)65.0(26.3)52.7(24.1)Gender(%female)69%51%76%MeanBMIofadolescentsandadultssignicantlygreaterthanmeanBMIofchildren.Ages1720(19).T.Teslovichetal./PsychiatryResearch219(2014)166170168 withinanormalweightrange.Itispossiblethatresponsestofoodrelativetononfooditemswouldbedifferentacrosstheweightandeatingdisorderedspectrum.Falsealarmrates,whichserveasanindexofimpulsecontrol,differedacrossagegroups,suggestingdifferencesinoverallimpulsivity.Thesendingsareconsistentwithpreviousstudiesthathaveshownthatcognitivecontrolisaprocessthatcontinuestodevelopintoadulthood(Somervilleetal.,2011).Ourindicatethatsalientfoodcuesinterferewithbehavioralinhibitionmorethannonfoodcues.Falsealarmrateswerehigherontrialswhenfoodwasthenontarget,consistentwiththeinter-pretationthatthesecuesweremoresalient.Thus,theabilitytoregulateimpulsiveresponsesisalteredinthecontextoffoodcues.Inourgroupofhealthy,normalweightindividuals,calorielevel(i.e.highorlow)didnotappeartoalterbehavioralperformance.Therewerenodifferencesinfalsealarmratesorreactiontimesbetweenhigh-calorieandlow-caloriefoodcues.Thisresultisnotentirelysurprising,inthatoursampleconsistedofhealthynormal-weightindividualswhowerescreenedforanyaberranteatingbehaviorspriortoparticipating.Ourresultssuggestthatinyoung,healthy,non-eatingdisordered,non-obeseindividuals,high-andlow-caloriefoodselicitsimilarbehavioralresponsesandmayreectasmuchofapreferenceforlow-calorieashigh-caloriefoods.Futurestudiescouldexplorethisndingbytargetingpopulationswithknownpredispositiontohigh-calorie/high-fatfoods,suchasindividualswithPrader-WilliSyndromeorcarriersoftheriskalleles(Ceciletal.,2008;Wardleetal.,2009)orinpatientswitheatingdisorders(e.g.strongaversionstohigh-fat/high-caloriefoods,suchasinanorexianervosa).4.1.LimitationsWhileourtaskwasmodeledonwell-establishedgo/no-gotasksandincludedappetitivefoodandnonfoodcues,wedidnotvalidatethistaskagainstastandardgo/no-gotaskwithoutappetitivestimuli.Itisnotable,however,thatperformanceonthistaskisconsistentwithperformanceseeninothergo/no-gotasks(i.e.overallaccuracyandreactiontimes)(Durstonetal.,2002;Hareetal.,2005;Somervilleetal.,2011;Caseyetal.,2007),whichspeakstothevalidityofthetaskasago/no-goparadigmwithinanormalpopulation.Additionally,giventhevariabilityinbehavioralresponses(e.g.falsealarmrates),particularlyintheyoungeragegroup,alargersamplemighthaveshownagebyconditioninteractions.Athirdlimitationcouldbeinourchoiceofhigh-andlow-caloriefoods.Itispossible,thatourhigh-andlow-caloriefoodswerenotsufcientlydistinct,thusourlackofbehavioraldifferencetocalorielevelwasnotbecau

4 sehigh-andlow-caloriefoodsareequallyappe
sehigh-andlow-caloriefoodsareequallyappetitivetonormalweightindividuals,butbecauseournormalweightindividualscouldnotcorrectlyidentifyhigh-andlow-caloriefoods.Separatingtherunsintodistincthigh-calorietargetsandlow-calorietargetsshouldhaveminimizedtheeffectthatdifcultyincalorieidenticationmighthavehadonperformance.Thoughthecurrentstudyusescaloriecontentasamethodofclassifyingfoodcues,recentstudieshavesuggestedtheuseofpalatabilityovercaloriecontentasasuperiorclassier(Houbenetal.,2012).Namely,thatbehavioralbiasestohigh-caloriefoodsmaybeduemoretothepalatabilityofthefoodthantheactualcaloriccontent.Duetothepotentialsubjectivityofthismeasureacrossourlargeagerange,however,caloriccontentwasstillused.High-andlow-caloriecategories,itcouldbeargued,offeredasomewhatmoreobjectivedistinctionbetweenourfoodgroups.Nonetheless,theselimitationsexistandshouldbeconsideredinthecontextofthendings.Similarly,whilethestimulussetusedwasmatchedonarousalandoverallappealoftheitems,othervisualcharacteristicslikecolorandvisualcomplexitycouldpotentiallybiastheappetitivenatureofcertainimages(MeuleandBlechert,2012)andthesemeasuresshouldbeconsideredinfutureapplicationsofthetask.4.2.ConclusionsSelf-control,orlackthereof,hasbeenlinkedtoamyriadofbehavioralmeasuresandhealthoutcomes.Thedevelopmentofage-appropriateandclinicallyrelevanttasksthatmeasureimpulsecontrolinthefaceofalluringcuesiskeyinunderstandingthecorecomponentsofself-controlwithreliabilityandspecicity.Clinically,impulsivityinthecontextoffood-speciccuesisanimportantaspectofthestudyofeatingandweightdisorders,includingobesityaglobalepidemic.Wehavesuccessfullydevelopedataskthatshowscleardevelopmentaldifferencesamonggroups,suggestingthatourtaskmaybeusedtostudydevelopmentaltrajectoriesineatingbehaviorandthedevelopmentofeatingdisordersamongabroadrangeofages.Thisfoodgo/no-gotaskmaybeusedtolearnmoreaboutdifferentpopulationsincludingindividualswithanor-exianervosa,bulimianervosa,bingeeatingdisorderandobesity.AcknowledgmentsTheresearchreportedinthisarticlewassupportedbyfundingfromtheDiabetesandEndocrinologyResearchCenter5P30 Table2Summaryofmaineffects.Reactiontime(ms)OmissionerrorrateFalsealarmrateMean(S.D.)Mean(S.D.)Mean(S.D.)Children549(98)13.37nnn0.04(0.05)14.890.46(0.21)42.77Adolescents466(57)0.02(0.03)0.29(0.18)Adults485(62)0.01(0.01)0.13(0.09)TaskconditionLow-calorie484(84)31.480.02(0.04)0.140.32(0.24)21.76High-calorie485(83)0.02(0.04)0.30(0.25)Toys507(84)0.02(0.04)0.23(0.21)Male484(92)0.590.03(0.04)7.980.33(0.22)6.01Female502(71)0.02(0.03)0.24(0.20)0.010.001T.Teslovichetal./PsychiatryResearch219(2014)166170169 DK063608-10andR56/R01DK097399,andinpartbyaMedicalScientistTrainingProgramgrantfromtheNationalInstituteofGeneralMedicalSciencesoftheNationalInstitutesofHealthT32GM007739.WewouldliketothankEveVaggoftheDigitalCommunicationsDepartmentattheNewYorkStatePsychiatricInstituteforheramazingphotography,JanetSchebendachforherfoodphotographyskills,NatashaMehtaforherinput,andourstudyparticipants,formakingthisresearchpossible.AppendixA.SupplementarymaterialSupplementarydataassociatedwiththisarticlecanbefoundintheonlineversionathttp://dx.doi.org/10.1016/j.psychres.2014.04.053Batterink,L.,Yokum,S.,Stice,E.,2010.Bodymasscorrelatedinverselywithinhibitorycontrolinresponsetofoodamongadolescentgirls:anfMRIstudy.Neuroimage52(4),16961703Bruce,A.S.,Lepping,R.J.,Bruce,J.M.,Cherry,J.B.C.,Martin,L.E.,Davis,A.M.,Brooks,W.M.,Savage,C.R.,2013.Brainresponsestofoodlogosinobeseandhealthyweightchildren.TheJournalofPediatrics162(4),759764.e2Casey,B.J.,Epstein,J.N,Buhle,J.,Liston,C.,Davidson,M.C.,Tonev,S.T.,Spicer,J.,Niogi,S.,Millner,A.J.,Reiss,A.,Garrett,A.,Hinshaw,S.P.,Greenhill,L.L.,Shafritz,K.M.,Vitolo,A.,Kotler,L.A.,Jarrett,M.A.,Glover,G.,2007.Frontostriatalconnectivityanditsroleincognitivecontrolinparent-childdyadswithADHD.AmericanJournalofPsychiatry164(11),17291736Casey,B.J.,Somerville,LH.,Gotlib,I.H.,Ayduk,O.,Franklin,N.T.,Askren,M.K.,Jonides,J.,Berman,M.G.,Wilson,N.L.,Teslovich,T.,Glover,G.,Zayas,V.,Mischel,W.,Shoda,Y.,2011.Behavioralandneuralcorrelatesofdelayofcation40yearslater.ProceedingsoftheNationalAcademyofSciencesUSA108(36),1499815003Casey,B.J.,Tottenham,N.,Liston,C.,Durston,S.,2005.Imagingthedevelopingbrain:whathavelearnedaboutcognitivedevelopment?TrendsinCognitiveSciences9(3),104110Casey,B.J.,Trainor,R.J.,Orendi,J.L.,Schubert,A.B.,Nystrom,L.E.,Cohen,J.D,Noll,D.C.,Giedd,J.,Castellanos,X.,Haxby,J.,Forman,S.D.,Dahl,R.E.,Rapoport,J.L.,1997.ApediatricfunctionalMRIstudyofprefrontalactivationduringperfor-manceofaGo-No-Gotask.JournalofCognitiveNeuroscience9,835847Cecil,J.E.,Tavendale,R.,Watt,P.,Hetherington,M.M.,Palmer,C.N.,2008.Anobesity-associatedFTOgenevariantandincreasedenergyintakeinchildren.NewEnglandJournalofMedicine359(24),2558Durston,S.,Thomas,K.M.,Yang,Y.,Ulug,A.M.,Zimmerman,R.D.,Casey,B.J.,2002.Aneuralbasisfo

5 rthedevelopmentofinhibitorycontrol.Devel
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