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Neural and psychophysiological correlates of human
performance under stress and high mental workload
Kevin Mandrick, Vsevolod Peysakhovich, Florence Rémy, Evelyne Lepron,
Mickael Causse
To cite this version:
Kevin Mandrick, Vsevolod Peysakhovich, Florence Rémy, Evelyne Lepron, Mickael Causse. Neural
and psychophysiological correlates of human performance under stress and high mental workload.
Biological Psychology, Elsevier, 2016, vol. 121, pp. 62-73. �10.1016/j.biopsycho.2016.10.002�.
�hal-01402108�
Neural
and
psychophysiological
correlates
of
human
performance
under
stress
and
high
mental
workload
Kevin
Mandrick
a,
Vsevolod
Peysakhovich
a,
Florence
Rémy
b,
Evelyne
Lepron
b,
Mickaël
Causse
a,∗aISAE(InstitutSupérieurdel’Aéronautiqueetdel’Espace),Toulouse,France
bCentrederechercheCerveauetCognition,UniversitédeToulouseUPSandCNRS,Toulouse,France
Keywords: Mentaleffort Stress Prefrontalcortex Cardiovascularactivity Pupilresponse
Functionalnear-infraredspectroscopy
a
b
s
t
r
a
c
t
Inouranxiogenicandstressfulworld,themaintenanceofanoptimalcognitiveperformanceisaconstant challenge.Itisparticularlytrueincomplexworkingenvironments(e.g.flightdeck,airtrafficcontrol tower),whereindividualshavesometimestocopewithahighmentalworkloadandstressfulsituations. Severalmodels(i.e.processingefficiencytheory,cognitive-energeticalframework)haveattemptedto provideaconceptualbasisonhowhumanperformanceismodulatedbyhighworkloadandstress/anxiety. Thesemodelspredictthatstresscanreducehumancognitiveefficiency,evenintheabsenceofavisible impactonthetaskperformance.Performancemaybeprotectedunderstressthankstocompensatory effort,butonlyattheexpenseofacognitivecost.Yet,thepsychophysiologicalcostofthisregulation remainsunclear.Wedesignedtwoexperimentsinvolvingpupildiameter,cardiovascularandprefrontal oxygenationmeasurements.ParticipantsperformedtheToulouseN-backTaskthatintensivelyengaged bothworkingmemoryandmentalcalculationprocessesunderthethreat(ornot)ofunpredictable aver-sivesounds.Theresultsrevealedthathighertaskdifficulty(highernlevel)degradedtheperformance andinducedanincreasedtonicpupildiameter,heartrateandactivityinthelateralprefrontalcortex, andadecreasedphasicpupilresponseandheartratevariability.Importantly,theconditionofstressdid notimpacttheperformance,butattheexpenseofapsychophysiologicalcostasdemonstratedbylower phasicpupilresponse,andgreaterheartrateandprefrontalactivity.Prefrontalcortexseemstobea cen-tralregionformitigatingtheinfluenceofstressbecauseitsubservescrucialfunctions(e.g.inhibition, workingmemory)thatcanpromotetheengagementofcopingstrategies.Overall,findingsconfirmed thepsychophysiologicalcostofbothmentaleffortandstress.Stresslikelytriggeredincreased moti-vationandtherecruitmentofadditionalcognitiveresourcesthatminimizeitsaversiveeffectsontask performance(effectiveness),butthesecompensatoryeffortsconsumedresourcesthatcausedalossof cognitiveefficiency(ratiobetweenperformanceeffectivenessandmentaleffort).
1. Introduction
1.1. Mentaleffortandstress
Inouranxiogenicandstressfulworld,themaintenanceofan optimalcognitiveperformanceisaconstantchallenge.Itis par-ticularlytrueincomplexworkingenvironments(e.g.flightdeck, airtraffic controltower), where individuals have sometimesto
∗ Correspondingauthorat:ISAE−SUPAERO,DCAS,10Avenue EdouardBelin, 31055Toulouse,France.
E-mailaddress:mickael.causse@isae.fr(M.Causse).
copewitha highmental workload(Borghini,Astolfi,Vecchiato, Mattia,&Babiloni,2014)andstressful(Causse,Dehais,&Pastor, 2011) or unexpected situations (Causse et al., 2013). Accord-ing toseveral authors, contextsof high mental workload (e.g.,
Causse,Peysakhovich,&Fabre,2016;Durantin,Gagnon,Tremblay, &Dehais,2014)and/orstress(e.g.Arnsten,2009;Qin,Hermans, Marle, Luo,&Fernández,2009; Schoofs,Wolf,&Smeets, 2009) mayresultin transientimpairmentsof workingmemory(WM) andexecutivefunctions(Starcke,Wiesen,Trotzke,&Brand,2016). Also,assuggestedbyDavis,Walker,MilesandGrillon(2010)the expectancyofanunpredictableanduncontrollablestressor(inthis paper,“stress”standsfortheemotionaltensionassociated with asustainedstateofanxietyinresponsetothethreatofa
nega-tiveevent)issufficienttocreateathreateningcontextandmay deliveranemotionaltensionassociatedwithasustainedanxiety (Breieretal.,1987;Lupien,Maheu,Tu,Fiocco,&Schramek,2007), atleastwhenthependingstimulusissufficientlyaversive(Grillon, Baas,Lissek,Smith,&Milstein,2004).Forexample,threat induc-tionusingaversiveloudsoundshasbeenshowntoactuallyinduce highertonicandphasicstresscomparedtopredictablesituations (Barrett&Armony,2006;Breieretal.,1987).
Literature shows that there is no straightforward effect of stressoncognitiveperformance,andhumanbraindoesnotseem defenseless against adverse effects of stressful situations. For example,stresscandisruptWM,and,reciprocally,WMcan mod-ulateanxiousresponse(Schmeichel,Volokhov,&Demaree,2008). Twoimportantmodels(theprocessingefficiencymodelandthe cognitive-energeticalframework)haveattemptedtoprovidea con-ceptualbasisonhowhumanperformanceismodulatedbyhigh workloadandstress/anxiety.Firstly,theprocessingefficiency the-ory(Eysenck&Calvo,1992)proposesthatadverseeffectsofanxiety arenotalwaysvisibleonperformanceoutcome.Theauthorsposit thatworriesaretriggeredinstressfulsituationsandthattheyhave twomaineffects.Thefirsteffectinvolvescognitiveinterferenceby preemptingtheprocessingandstoragecapacityofworking mem-ory.Thesecondeffectinvolvesincreasedmotivationtominimize theaversiveanxietystate.Thislatterfunctionpromotesenhanced effortand useof auxiliary processing resourcesand strategies. Thus,potentialperformanceimpairmentscausedbythe preemp-tionofworkingmemoryresourcescanbecompensatedifauxiliary processingresourcesareavailable.Thetheorydiscriminates per-formance effectiveness(qualityof performance)and processing efficiency(ratiobetweenperformance effectivenessand mental effort). Given the triggeringof compensatory mechanisms(e.g. enhancedeffort;increaseduseofprocessingresources),impaired performanceeffectivenessislesslikelytooccurbutatthecostof reducedefficiency.Attentionalcontroltheory(Eysenck,Derakshan, Santos,&Calvo,2007),amajordevelopmentofEysenckandCalvo’s (1992)model,assumedthatanxietyeffectsonprocessingefficiency concernprimarilytwocentralexecutivefunctionsinvolving atten-tionalcontrol:inhibitionandshifting.However,theauthorsposited thatanxietyalsoimpairsprocessingefficiency(andsometimes per-formanceeffectiveness)ontasksinvolvingtheupdatingfunctionof workingmemorywhentheconditionsarestressful.
Theprocessingefficiencymodelhassimilaritieswiththe sec-ondmodel,thecognitive-energeticalframework.Thislattermodel positstheexistenceofcompensatorycontrolintheregulationof humanperformance understress andhighworkload (Robert & Hockey,1997).Thecognitive-energeticalframeworkalsopredicts thatperformancemaybeprotectedunderstressbytherecruitment offurtherresources,butonlyattheexpenseofincreased subjec-tiveeffort,andbehavioralandphysiologicalcosts.Evenwhenno primarytaskdecrementsaredetected,performancemayshow dis-ruptionofsubsidiaryactivitiesortheuseoflessefficientstrategies. Additionalcostsincludeincreasedpsychophysiologicalactivation, strain,and fatigueafter-effects.Otherwise, coststability canbe achievedbyreducingperformancegoals.Beyondtheirrespective theoreticalconstructs, the commonidea in theprocessing effi-ciencytheory(Eysenck&Calvo,1992)andthecognitive-energetical framework(RobertandHockey,1997)isthatstresslikelytriggers increasedmotivationandtherecruitmentofadditionalcognitive resourcesthatminimizeitsaversiveeffectsontaskperformance (effectiveness). However, these compensatory efforts consume resourcesandthus,causealossofcognitiveefficiency.
The impact of stress seems to also depend on task diffi-culty (Robinson, Vytal, Cornwell, & Grillon, 2013). Patel et al. (2015)recentlyshowedthatthethreatofanaversiveloudscream impactedWMperformanceatlowandmediumbutnothighload conditions.Consistently,ClarkeandJohnstone(2013)foundthat
thethreatof shocksignificantlydisrupted thecognitive perfor-manceunderlowWMloadwhereasnosignificantinterference(and evenatrendforperformanceimprovement)occurredinthehigh WMloadcondition.Suchresultsmaybeinterpretedasareduced distractoreffect(Hu,Bauer,Padmala,&Pessoa,2012),when atten-tionisshiftedawayfromtheaffectivestimulus(Pessoa,McKenna, Gutierrez,&Ungerleider,2002; VanDillen,Heslenfeld,&Koole, 2009),andsuggesttheexistenceofadynamicbalancebetween emotionandcognition(Drevets&Raichle,1998).Suchabalance isalsosupportedbyresultsfromBerggren,Richards,Taylorand Derakshan(2013).Intheirstudy,emotionwasdeleteriousto per-formanceinthelowloadcondition(tonesrecognition)duringa modifiedemotional antisaccadetask(aconditioninwhichgaze towardsemotionalstimulishouldbeinhibitedandparticipantshad tolookawayfromtheimageandmovetheireyestothe oppo-siteendofthescreen).Onthecontrary,emotiondidnotinfluence performanceunderthehighloadcondition(recognitionofspecific tonepitch),supportingrecentevidencethatmorecomplex cogni-tiveprocessescanreduceemotionalinfluencesonattentionand cognition.
1.2. Psychophysiologicalactivityrelatedtocognitionandemotion AccordingtoRyuandMyung(2005),physiological measures can be classified into three major categories as a function of thephysiological organs involved:brain-related measures, eye-related measures,and heart-relatedmeasures.Prefrontalcortex (PFC)relatedactivityismodulatedbyWMload,forexample,Owen, McMillan,LairdandBullmore(2005)meta-analysisof24n-back studies hasshown that higher workload is consistently associ-atedwithgreatercorticalactivation,includingcriticalPFCregions. RecentstudiesalsoshowedthatactivationsofthePFCobserved viafunctionalnearinfraredspectroscopy(fNIRS)reflectWMload duringn-backtasks(Fishburn,Norr,Medvedev,&Vaidya,2014;
Gateau,Durantin,Lancelot,Scannella,&Dehais,2015;Herffetal., 2014;Peck,Afergan,Yuksel,Lalooses,&Jacob,2014;Satoetal., 2013;Yukseletal.,2015).ItisalsoclearthatthePFCisoneof themostsensitivebrainregionstothedetrimentaleffectsofstress (Arnsten,2009), becauseithasa criticalrole in theintegration ofcognitiveandaffectivebehavior(Cerqueira,Almeida,&Sousa, 2008).Inparticular,theorbitalandmedialPFCareknowntobe involvedinregulationofemotionviaextensiveconnectionswith limbicregions(Hänsel&Känel,2008;SeoandSinha,2011(ch9)). Interestingly,dorsolateralPFCisalsolikelytoindirectlycontribute toemotionregulationthroughitsinteractionwiththeorbitofrontal cortexandtheanteriorcingulatecortex,andviatheseareas,with theamygdala(Salzman&Fusi,2010a,2010b).Inaddition,the dor-solateralPFCmaybealsoinvolvedinemotionregulationbecause itplaysacrucialroleintheneuralnetworksubservingWM func-tions(LevyandGoldman-Rakic,2000).AssuggestedbySchmeichel, Volokhov andDemaree(2008),WMcapacitycontributes tothe controlofemotionalresponseassubjectswithhigherWM capac-itysuppressedexpressionsofnegativeandpositiveemotionbetter thansubjectswithlowerWMcapacitydid.SeveralfNIRSstudies haveinvestigatedtheimpactofemotiononthePFCduringa stress-fulsituation(Doi,Nishitani,&Shinohara,2013; Morinagaetal., 2007;Tanida,Katsuyama, &Sakatani,2007;Tupaketal.,2014).
Tanidaetal.(2007)indicatedthatmentalstressinduceda predom-inanceoftherightPFCactivation,revealedbyanincreaseofHbO2
signalwithaconcomitantdecreaseoftheHHbsignal.Inaddition,
Morinagaetal.(2007)showedhigheractivationoftherightPFC activation(anincreaseofHbO2)duringanticipationofshocks.
Thepupildiameterisawell-establishedmeasureofWMload (Andreassi,2000;Beatty,1982;seealsoLaeng,Sirois,&Gredebäck, 2012,fora recentreview).Firstviewedasasimple measureof “intensity”ofattentionandmentalactivity(Kahneman&Beatty,
1966;Kahneman,1973),itisnowadmittedthatpupildiameter isalsoarelevantindicatorofaffectiveandemotionalprocessing (Bitsios,Szabadi,&Bradshaw,1998;Bradley,Miccoli,Escrig,&Lang, 2008;Clarke&Johnstone,2013;Partala&Surakka,2003).Cohen, MoyalandHenik(2015)usedpupildilationmeasurementsto mon-itortheemotionalresponsegeneratedbyaversivestimuli(pictures andsounds).Theyshowedthatemotionalresponsewasattenuated, asindexedbylowerpupildilation,whentheaversivestimuliwere precededbyincongruentflankerstimulus,providingevidencethat thephysiologicalresponseassociatedwithemotionalstimulation dependsonsituationaldemands,suchasprioractivationof exec-utivecontrolprocesses.However,theauthorsdidnot explicitly manipulatethementalworkloadintheirparadigm.
Also, task-relatedpsychophysiologicalcosts havebeen stud-iedwiththeanalysisofthecardiovascularactivity(Riese,1999). Subjectsreacttosustainedheavytaskdemandsbyaninitial reac-tioncalledthedefensereaction.Thisreactionis supposedtobe causedbyincreasedactivationofthesympatheticnervoussystem andinhibitionofthevagalsystem,inducingclassical cardiovas-cularreactions:anincreaseinbloodpressureandheartrate(HR) andadecreaseinheartratevariability(HRV)(Riese,1999;Causse, Baracat,Pastor,&Dehais,2011).Itisalsowelldemonstratedthat HRandHRVprovidesensitivemarkerstoemotionalprocesses(e.g.
Brosschot&Thayer, 2003;Laneetal.,2009;McCraty,Atkinson, Tiller,Rein,&Watkins,1995;Quintana,Guastella,Outhred,Hickie, &Kemp,2012).Forexample,BrosschotandThayer(2003)showed thatmoderateincreaseofHR(approximatively1beatperminute) canlastupto5minafternegativeevents.
Becausetherelationshipbetweenpsychologyand psychophys-iologicalreactionisnotalwaysone-to-one(e.g.onepsychological operationassociatedwithonepsychophysiologicalreaction),but alsomany-to-one, one-to-many, ormany-to-many (Cacioppo& Tassinary,1990),asZhou,Qu,HelanderandJiao(2011)wesuggest thatasinglepsychophysiologicalmeasureisnotadequatetogive afullpictureoftheongoingpsychologicalprocesses,particularly whenbothcognitiveandemotionalvariablesaremanipulated.In thepresentstudy,combinedeye-related,heart-related,and brain-relatedmeasureswereconducted.
1.3. Presentstudy
We studied the effects of stress (induced by the threat of unpredictableaversiveloudsounds)onWMperformanceunder variationsoftaskdifficulty.Wedesignedanewtask,theToulouse N-backTask(TNT),combiningtheclassicaln-backtaskwith math-ematicalprocessingtoinducedifferentlevelsofmentalworkload. ThetaskallowselicitingbothasustainedhighWMandprocessing load,whichmimicsthemultidimensionalhighmentalworkload existinginmany safety-criticaloccupations.Thepurposeofthe presentstudywastoexplicitlyinvestigatetheimpactofmental effortandstressinahighlydemandingtask,byassessing perfor-manceaswellasthepsychophysiologicalcostinvolved.Inaddition tothewelladmitteddeleteriousimpactofhighmentalworkload (Causseetal.,2016;Durantinetal.,2014),wemayhypothesize thattaskperformancewouldbeimpactedbystress.Ontheother hand,various modelssuch as processing efficiency theory and thecognitive-energeticalframeworkalsosuggestthatwemaynot observeanybehavioraleffectofstress:cognitiveperformancemay beprotectedunderstressthankstocompensatoryeffortsandthe useof cognitivecoping strategies,but onlyat theexpenseof a psychophysiologicalcost(Robert&Hockey, 1997).Yet,reduced cognitiveefficiencyand/orthecostofstrategiestocopewithstress aregenerallyexaminedthroughvariationintaskperformance(eg. longerreaction times), but their psychophysiologicalcorrelates remainunclear.Wehypothesizedthatpupildiameter,HR,and pre-frontalcortexoxygenationwouldbehigherintheconditionofhigh
mental workloadand alsoin theconditionofstress. Finally,as suggestedbyvariousauthors,wemayalsoobserveaninteraction betweenmentalworkloadandstressinawaythatthehighWM loadconditioncouldmitigatetheimpactofstress.Thislowered impactofemotionmightbeindexedbybehaviorand psychophys-iologicalmeasurements.
2. Materialsandmethods
2.1. Participants
We recruited fourteen healthy volunteers (5 women, age 25.8±3.8years) for study 1 and twenty healthy volunteers (5 women,age24.6±4.8years)forstudy2.Pupillometryrecordings wereperformedinStudy1andfNIRSrecordingswereperformed inStudy2.Cardiovascularactivitywasrecordedinbothstudies. Participantsweresplitintotwoseparatestudiesassimultaneous functionalnear-infraredspectroscopyandpupillometry measure-ment is complex becausethese two techniques overlap in the near-infraredwavelengthband.AllwerestudentsatNationalCivil AviationSchool(ENAC)and HigherInstituteof Aeronauticsand SpaceEngineeringSchool(ISAE)inToulouse,France.Nonereported neitheraffectiveoranxietydisorder,noranyneurologicalor car-diovasculardisease.Nonewasundermedicationthatmightaffect thebrainorautonomicfunctions.Allvolunteersreportednormal auditoryacuityandnormalorcorrected-to-normalvision.All par-ticipantsgavewritteninformedconsentinaccordancewithlocal ethicalboardcommittee.Thestudycompliedwiththe Declara-tionofHelsinkiforhumanexperimentationandwasapprovedby medicalCommittee(CPPduSud-OuestetOutre-MerIV,n◦ CPP15-010b/2015-A00458-41).
2.2. MentalarithmeticN-backtask(ToulouseN-backtask)
Thenewn-backtask,calledTNT,wasdevelopedforthisstudy inordertocombineaclassicaln-backtaskwithmentalarithmetic (Fig.1).Insteadofmemorizingandcomparinguniqueitems,asin theclassicaln-backtask,theparticipantshadtomemorizeandto comparetheresultsof arithmeticoperations,computed before-hand.Ineachtrial,volunteerswererequiredtocomputetheresult andcompareitwitheitherafixednumber(0-back)ortheresult obtained1(1-back)or2(2-back)trialsbefore.Arithmetic opera-tionswereeitheradditionsorsubtractions,ofwhichallsummands werea multipleof 5 (e.g.,15+40, 90–35). Therefore, WMload wasvariablebetweenconditions,withthe2-backtaskgenerating thehighestload.Duringtherestingperiods,screenswith“00+00” operationswerepresentedandvolunteersdidnothavetogiveany response.
Operationsweredisplayedinthecenterofagraybackground. Participantsweregivena2-buttonCedrusresponsepad(RB-740, CedrusCorporation,SanPedro,CA)andwereaskedtopresseither agreenbuttoniftheresultmatchedthetargetnumberorared buttonifnot.Participantshadtogivetheirresponseasquicklyas possible.ThetaskwasimplementedinMatlab(MathWorks)using thePsychophysics Toolbox(Psychtoolbox3,Kleiner,Brainard,& Pelli,2007).
2.3. Threatusingauditorystressors
Stress(i.e.sustainedanxiety)wasinducedwiththethreatof unpredictableloudsounds(Pateletal.,2015).Theauditory stress-orsoccurrencewasnon-contingentupon thetaskperformance. Wecreatedasetof34aversivesoundsinspiredfromthe litera-ture(Grillon,Pine,Lissek,Rabin,&Vythilingam,2009;Hiranoetal., 2006;Kumar,Forster,Bailey,&Griffiths,2008;Zald&Pardo,2002). Thesoundswereperceivedasmildlystressful,uncomfortableand
Fig.1.ToulouseN-backTask.AnexampleoftrialsfortheTNT,inwhichparticipantscombinedmentalcalculationswithn-backtask.The0-,1-,and2-backtaskblocks lasted36s,interleavedwith18sresting(R)periods.Stimuliwerepresentedfor2swithaninter-stimulusintervalof1s.Participantsrespondedtotargetsandnon-targets bypressingoneoftwodifferentbuttons.Eachblockcontained4targetsinrandompositions.Duringthe0-back(leftpartofthefigure),asimplecomparisonofthecurrent resultwith“50”wasrequired.Duringthe1-back(middlepartofthefigure)andthe2-back(rightpart)tasks,thecurrentresulthadtobecomparedwiththeonecomputed 1or2trialsbefore,respectively.
unpleasantby87participantsduringapilotstudy(ratings>6using a 10-point scale, with 10 meaning “extremely unpleasant and stressfultogether”).
Thestressfulnessofthesoundswasalsovalidatedbya spec-tralfrequency–temporalmodulationanalysis(seeSupplementary material).Soundsweremodifiedtoequalizeloudnessandduration. Eachsoundsamplewaspresentedonlyoncetopreventhabituation andmakethestimulationmoresalientandstressful.Participants wereinformed thattheywould beexposed todifferent unpre-dictableaversiveloudsoundsduringagivenblockorrestingperiod. However,theonsetofsoundswasunknowntoparticipantsinorder tomaintainacontinuousthreat(Grillonetal.,2009;Zald&Pardo 2002).Thesoundswereplayedfor7sviaAKGK171MkIImonitor headphonesinstereomodeandata95-dBsoundpressurelevel, ascontrolledusinganoisemeter(Grillonetal.,2009;Hiranoetal., 2006).
2.4. Subjectivedifficultymeasures
FollowingatrainingperiodwiththeTNT,participantsrated dif-ficultyusingaDP15scale(Delignières,Famose,&Genty,1994).The DP15scaleconsistsina15-pointcategoryscale,with7labels,from 2(extremelyeasy)to14(extremelydifficult),symmetricallyplaced aroundacentrallabel8(somewhatdifficult).
2.5. Subjectiveanxietymeasures 2.5.1. Sensitivitytoauditorystressors
Toassess individualsensitivitytoauditorystressors, partici-pantswererequested tolistento each ofthe 34 aversive loud sounds(presentedwithillustrativeimages)−beforeorafterthe experiment,theorderwascounterbalancedacrossparticipants−
andtorateeachsoundunpleasantnessandinduced-stressusinga 10-pointscale(with10meaning“extremelyunpleasantand stress-fultogether”).
2.5.2. Anxietyquestionnaire
Subjectiveevaluationoftheanxietystatewasobtainedbytwo completionsoftheState-TraitAnxietyInventory(STAIformY-A, Frenchtranslation)(Gauthier&Bouchard, 1993), precedingand followingthewholeexperimentalprotocol.Thistestconsistedofa 20-itemself-administeredquestionnairewith4-pointLikertscale response(Spielberger,Gorsuch,&Lushene,1970).
2.6. Experimentalprocedure
ParticipantswerefirsttrainedforeachleveloftheTNTthrough a shortsequence of5min,in whichaversive loudsoundswere presentedrandomly. Experimentalrunsconsistedofafirst10-s fNIRSbaselinefollowedbyalternatingTNTandrestblocks.Two runsincludedunpredictableaversiveloudsounds(“threat”runs) andonerunwaswithoutanythreats(“safe”run).Theorderofthe TNTblockswithinarunandtheorderof“threat”and“safe”runs werecounterbalancedacrossparticipants.Toavoidfatigue,ashort breaklastingapproximatively5minwasgivenattheendofeach run.BeforeandduringTNTblocks,a3-sinstructionscreenwas displayedtoinformtheparticipantaboutupcomingTNTdifficulty (“0-back”,“1-back”,“2-back”)andaboutthreatcondition(safevs. threat)(Fig.2).During thesaferun,participantswerereminded thatnosoundwillbeplayed.Duringthreatruns,participantswere remindedthataversiveloudsoundsmayoccuratanytime, includ-ingduringrestingperiods.
Thesaferunincluded12blocks(4blocks ofeachdifficulty). The two threat runs included 9 blocks each (3 blocks of each
Fig.2. Experimentaltimeline.TNTexperimentalblockdesignsessionswithtworunsforthreatconditionandonerunforthesafecondition.Runordersandblockswere counterbalancedandpseudo-randomized.Unpredictableaversiveloudsoundswereplayedrandomlyduringathreatrunandcouldoccurduringrestingperiod.
difficulty).Fortheanalysisofthethreatruns,we discardedthe blockscontainingsounds(6blocksintotal)toexcludeany poten-tialeffectofsounddistractionandtofocusonthestressrelated totheexpectancyoftheunpredictablesounds(Clarke&Johnstone, 2013).Wethuscomparedthe12threatblocksinwhichparticipants expected,butdidnotactuallyhearsounds,withthe12safeblocks. Hence,4blocks(4×12trials)percondition(0-,1-,2-backxSafe, Threat)wereincludedintheanalyses.Forthepupillaryanalyses, 12blocksofrestingperiods(12×6trials)werealsoincluded. 2.7. Behavioralmeasurements
TNTaccuracywascalculatedusingthed-primemeasure, com-putedasfollows:z(hitrate)−z(falsealarmrate).Additionally,the numberofmisses(noresponse)wascomputed,thislattermeasure likelyreflectinganexhaustionofcognitiveresources.
2.8. Study1:Pupillometrymeasurements
Participantswereseatedat approximately70cm froma22’ computerscreen (1680×1250 pixels). Ambient luminance was of 10lx.During thewhole experiment, participants’gaze posi-tionandpupildiameterweretrackedusingaremoteSMIRED500 eye-tracker(SensoMotoricInstrumentsGmbH,Germany)ata sam-plingrateof120Hz.Thisdeviceallowstrackingthepupildespite smallheadmovements.Beforeeachrun,participantsperformeda 5-pointcalibrationprocedurevalidatedwith4additionalfixation points.ThedataacquisitionroutineusediViewXSDKto communi-catewithMatlabsoftware.Periodsofsignallossandblinks(both weremarkedaszerosbytheeye-trackingsystem)werelinearly interpolated.Thenthesignalwasfilteredwithatwo-pass9-point filter(low-passwithacutofffrequencyof5.9Hz).Fortonicpupil diameteranalyses,weusedthemedianpupildiametervaluefor each block.We also conducted(event-related) phasicpupillary responseanalyses.Forthisanalysis,thepupillaryrecordingswere segregatedin3-ssegmentscorrespondingtoeachtrial.Forall par-ticipants,anaveragephasicpupillaryresponsewasobtainedfor eachcondition.Atrialwasexcludedifthetotaldurationof sig-nallossorblinkingexceeded50%(1.5s)orifmediangazeposition duringthetrialdeviatedfromthescreencenterofmorethan150 pixels.Anaverageof44.6(SD=8.4)trialsoutof48werevalidated perexperimentalcondition.Anaverageof58.1(SD=14.6)trialsout of72werevalidatedforrestingperiods.Thenumberofvalidated trialswasnon-dependentonthecondition(p>0.05).Median val-uescalculatedonthe500-msperiodprecedingthetrialonsetwere usedasbaselines.Forstatisticalanalysesofphasicpupilresponse, weusedthemaximumpupildiameterintheintervalbetween1 and2spost-stimulus.Restingperiodswereincludedinthe
pupil-Fig.3. fNIRSheadband.Locationoftheoptodesonparticipant’sforeheadwitha flexiblefNIRSsensorpadlabeledfromchannel1tochannel16.Emittersaremarked asEandDindicatesdetectors.Areasunderlyingthechannelareapproximatelyover Brodmann’sareas10and46.
lometryanalysestoconfirmthatthepupillaryreactionwasdueto thepsychophysiologicalphenomenonandnotvisualfactors. Thir-teenparticipantswereincludedin thepupillaryanalyses(pupil datafromoneparticipantwerediscardedduetotechnicalissues duringtherecording).
2.9. Study2:Functionalnearinfraredspectroscopy measurements
Toilluminatetheforehead,aCWfNIRS16-channelheadband model100fNIRSsystem(fNIRSDevicesLLC,PhotomacMD;http:// www.fnirdevices.com)wasusedtoobtainrawlightintensityby specificdualwavelengthsof730nmand850nm(Fig.3).Datawere acquiredatafrequencyof2Hzforall16channels.
Atthebeginningoftheexperiment,participantswereequipped withthefNIRSheadband.The10sbaselinewastakenatrestwith eyesclosed.fNIRS-PFC activitywasrecordedthroughtheentire experiment. COBIStudiosoftware(Drexel University)wasused fordataacquisitionandvisualizationofthe16channelsthenthe version 4.0 of fnirSoft software package was usedfor filtering, convertingandanalyzingdata(Ayaz,2010).First,therawoptical densitysignalswereconvertedtoconcentrationchangesof oxy-genatedhemoglobin(HbO2)anddeoxygenatedhemoglobin(HHb)
usingthemodifiedBeer-lambertlaw.fNIRSdatawerethen band-passfilteredusingaFIRfilteroforder20andcutofffrequenciesof 0.01and0.1Hz.Nodetrendingwasapplied.Then,availableoptodes wereaveragedin3regionsofinterestforeachparticipant;left pre-frontalcortex(optodes1–6),frontopolarprefrontalcortex(optodes 7–10),rightprefrontalcortex(optodes11–16).Eightparticipants hadmissingfNIRSdataina fewmedialoptodesforatleastone experimentalconditionduetopoorcontactwiththeforehead(i.e.
optodes5,7–9,and10).Atmost,3optodesweremissingfor1 par-ticipant,thusameasureofthefrontopolarprefrontalcortexactivity waspossibleforthese8participants.TodissociateeffectsofTNT difficulty(0-backvs.1-backvs.2-back)andthreat(safevs.threat), weextractedthefNIRSresponsefromeachblock.Signalswere nor-malizedtowardszerobysubtractingthecurrentsignalwiththe firstdatapoint.Then,signalswereaveragedonalltrialsforeach condition.
Wecalculatedtheblood-oxygenationresponsedeterminedas thedifferencebetweenHbO2andHHbsignals.ForfNIRSdata
analy-sis,wecomparedtheblood-oxygenationresponsewiththeanalysis oftheresponseamplitude(thedifferencebetweenthemeanvalue ofthefirstandthelast10sofeachblock)(Mandricketal.,2013a, 2013b).SeventeenparticipantswereincludedinthefNIRS anal-yses(fNIRSdataofthreeparticipantswereexcluded,onedueto excessivelynoisysignalandtwoduetorecordingproblems).
2.10. Cardiovascularactivity
Cardiovascular activity (by 1-lead ECG) was continuously recorded in both studies. Signals were sampled at 500Hz in a synchronousmannerusingaBiopacMP150HardwareandBiopac AcqKnowledge4.1.1Software(BiopacSystemsInc.,CA,USA).Signal wasderivedintoRRintervalstoassesstheHR.Datasetswere visu-allycontrolledforoutliersandartifacts.Analyseswereconducted withKubiosHRVsoftware2.2(UniversityofEasternFinland,http:// kubios.uef.fi).WeinvestigatedtotalHRVviatherootmeansquare of successivedifferences (RMSSD) (Task Force of the European SocietyofCardiologytheNorthAmericanSocietyofPacing,1996). Thirty-three participants were included for the analysis of the cardiovascularactivity(HRandHRVdataofoneparticipantwas excludedduetoexcessivelynoisysignal).
Dataanalysis
Results were analyzed using Statistica software (StatSoft). Normality and homoscedasticity of data were assessed using Kolmogorov-SmirnovandLillieforstests,respectively.Pre−post comparisonsofSTAIscoresandprefrontaloxygenationresponses were carried out using Student paired t-test. Other data were analyzedusingrepeated-measuresanalysesofvariance(ANOVA) for normally distributed variables (i.e. pupillometry, HR/HRV, and fNIRSmeasurements)and Friedman’sANOVA testfor non-normally distributed variables (i.e. DP15, d-prime, and% no response). In the case of significant main effect or interaction, significantdifferencesbetweenconditionswereidentifiedusing Tukey’s HSDposthoc testsfor normal distribution orWilcoxon comparisons test for non-normal distribution. p-values were adjustedformultiplecomparisonswiththeHolm-Bonferroni cor-rection(Holm,1979).Asignificancelevelofp<0.05wasusedforall
comparisons.Effectsizeswerereportedusingpartialeta-squared (p2).
3. Results
3.1. Subjectivedifficultyratings
There wasno significant differencebetween Study 1 and 2 (p>0.05)(Mann-WhitneyUtestforeachvariable;p>0.05) regard-ing the perceived difficulty during the familiarization session. Therefore, perceived difficulty data were pooled across studies andstatisticswerealsocalculatedfor34participants.DP15 rat-ingssignificantlyincreasedwithTNTdifficulty(nlevel)(Friedman’s chi-squareANOVA=65.5;p<0.001),withratingsbeinghigherfor 1-backvs.0-back(Z=5.03;p<0.001),for2-backvs.0-back(Z=5.08; p<0.001),andfor2-backvs.1-back(Z=5.01;p<0.001).The0-back taskwasratedas“veryeasy”(averageDP15=4.5±2),the1-back taskas“somewhatdifficult”(averageDP15=7.8±1.9),andthe 2-backtaskas“verydifficult”(averageDP15=11.9±1.6).
3.2. Subjectiveanxietyratings
Subjectiveratings ofinducedstress forthe34 aversive loud soundsaregiveninSupplementarymaterial.Based onthis sub-jectivereport,ameanratingof5.4±2.4wasobserved,confirming thatsoundsweremildlystressful.
TherewasnosignificantdifferencebetweenStudy1and2 (t-testforeachvariable;p>0.05),therefore,anxietyratingsdatawere pooled acrossstudiesandstatistics werecalculated for 34 par-ticipants.Participants’anxietyscoremeasuredbySTAIY-Awere significantlyhigherattheendoftheprotocol,relativetothe begin-ning(29.1±5.9versus33.3±7.1,respectively;t=3.85;p<0.001). Thisoutcomeshowsthattheexperimentproducedanincreased anxiety.
3.3. Behavioraldata
There wasno significant differencebetween Study 1 and 2 regardingthebehavioralperformance(Mann-WhitneyUtestfor eachvariable;p>0.05).Therefore,behavioraldatawerealsopooled acrossstudiesandstatisticswerecalculatedfor 34participants. Cognitivescoresforeachn-backconditionwereassessedusing d-primeandpercentageofmiss(“noresponse”)(Fig.4).Participants showedlowerd-primescoreswithincreasedtaskdifficulty (Fried-man’schi-squareANOVA=115.7;p<0.001).Post-hoccomparison revealedsignificantdifferences(p<0.001)foralln-backlevelas summarizedinFig.4.Similarresultswereobservedforthe per-centageofomittedresponses,whichmonotonicallyincreasedwith
Fig.4. Behavioralperformance.TNTscoresforeachlevelofdifficulty(0-,1-,and2-back)andthreatcondition(safeandthreat).ErrorbarsareS.D.Left-d-primecalculated asz(hitrate)−z(falsealarmrate).Right-thepercentageof“noresponse”.n=34.
Fig.5.Cardiovascularactivity.Cardiovascularactivityforeachlevelofdifficulty(0-,1-,and2-back)andthreatcondition(safeandthreat).ErrorbarsareS.E.Left-Heartrate. Right-Heartratevariability.n=33.
Fig.6. Tonicpupildiameter.Barheightshowsmeantonicpupildiameterforeach levelofdifficulty(rest,0-,1-,and2-back)andthreatcondition(safeandthreat). ErrorbarsrepresentS.E.n=13.
taskdifficulty(Friedman’schi-squareANOVA=57.9;p<0.001).The threatofunpredictableauditorystressorsdidnotimpact behav-ioralperformance(p>0.05).
3.4. Cardiovascularactivity
Therewas no significant differencebetween study 1 and 2 (p>0.05)regardingcardiovascularactivity.Therefore,HRdatawere alsopooled acrossstudiesand statistics werecalculated for 33 participants. There was a significant elevation of the HR with increasedTNT difficulty(F2,62=20.5; p<0.001;p2=0.40),with
a monotonical increased across each level of difficulty (small-est p-value=0.019). HR was also impacted by stress, it was higher under the threat of the unpredictable aversive sounds (F1,32=4.35;p<0.05;p2=0.12)(Fig.5).Therewasalsoa
signif-icantdecreaseinHRV(RMSSD) withtaskdifficulty(F2,62=12.1;
p<0.001;p2=0.28),HRVwassmallerin0-backvs.1-and2-back
(smallestp-value<0.001)(Fig.5).Finally,HRVwasnotimpacted bystress(p>0.05).
3.5. Pupillometry
3.5.1. Tonicpupildiameter
Tonicpupildiametersignificantlyincreasedwithtaskdifficulty (F3,36=26.27;p<0.001;p2=0.69)(Fig.6).Post-hoctestsshowed
thatpupildiameterwassignificantlyhigherduring1-and2-back vs.restingperiod(p<0.01andp<0.001respectively)and
signifi-Fig.7. Phasicpupilresponse.Grand-averageofphasicpupilresponsealignedto thestimulusonsetforeachlevelofdifficulty(rest,0-,1-,and2-back)andthreat condition(safeandthreat).Verticallinesindicatethetimeintervalusedforpeak computation.n=13.
cantlyhigherduring2-backcomparedto0-and1-back(p<0.001 inbothcomparisons).Therewasnoeffectofthreatontonicpupil diameter(F1,12=0.75;p2=0.06), neitheranydifficultyxthreat
interaction(F3,36=1.27;p2=0.10).
3.5.2. Phasicpupilresponse
Phasicpupilresponseamplitudes(Fig.7)significantlydecreased with n-back task difficulty (F3,36=12.05; p<0.001; p2=0.50).
Moreprecisely,asignificantlyhigherdilationwasobservedin0-, 1-,and2-backtaskscomparedtorest(p<0.001,p<0.01andp<0.05 respectively)anddilationwasgreaterin0-backvs.2-back(p<0.05) conditions.Smalleramplitudeswereobservedinthreatconditions (F1,12=6.38;p<0.05;p2=0.35).Therewasnothreatxdifficulty
interaction (F3,36=0.33; p>0.05; p2=0.03). We conducted an
additionalanalysis in ordertoassess thepotentialinfluence of thepre-stimulusbaseline(medianofpre-stimulus500ms,used tocomputethephasicresponse)ontheresults.Therewasaneffect ofn-backtaskdifficulty(F3,36=25.38;p<0.001;p2=0.68),butno
anyeffectofthreat(F1,12=0.15;p2=0.01)orthreatxdifficulty
interaction(F3,36=0.56;p2=0.04)onpupildiameterduringthe
Fig.8.Braintopographymaps.AnteriorviewofthefrontalcortexshowingregionswherePFCbloodoxygenation(HbO2−HHb)increasedwithn-backtaskdifficulty(0-,1-,
and2-back)andthreatcondition(safeandthreat).n=17.
3.6. Prefrontalcortexoxygenationchanges
Brain topography of PFC blood oxygenation is illustrated in
Fig.8.PFCbloodoxygenationwasdependentonn-backtask dif-ficulty (F2,34=4.14; p<0.05; p2=0.20). More precisely, it was
significantlyhigherin1-backvs.0-backcondition(p<0.05)and marginallyhigher in 2-backvs. 0-backcondition(p=0.06).PFC bloodoxygenationwasnotdifferentin1-backvs.2-back condi-tion(p=0.96).Thetaskdifficultyxregionofinterestinteraction wassignificant(F4,68=3.02;p<0.05;p2=0.15).HSDrevealedthat
difficultyhadnosignificanteffectonthefrontopolarregionofthe prefrontalcortex(p>0.05);onthecontrary,oxygenationwas sig-nificantlyhigherintheleftandrightprefrontalcortexin1-back vs.0-backandin2-backvs.0-back(smallestp-value=0.001).As showedFig.8,PFCbloodoxygenationwasalsosignificantlyhigher inthreatvs.safeconditions(F1,17=4.81;p<0.05;p2=0.22).The
taskdifficultyxstress interactionwasnot significant(p>0.05), however,thevisualinspectionofFig.8highlightsalargereffectof threatontheprefrontalactivityinthe0-backconditionin com-parisontothe 1-backand 2-backconditions. Coherently,effect sizes(independentlyoftheregionsofinterest)showedthatthe strengthoftheimpactofthethreatconditionwasclearlylargerin 0-backcondition(p2=0.39)comparedto1-back(p2=0.04)and
2-backconditions(p2=0.04).Itsuggeststhatincreasingsample
sizemightrevealamitigationoftheeffectofstresswithincreasing workingmemoryload.HRwasnotcorrelatedwithprefrontal activ-ityinnoneoftheexperimentalconditions(smallestp-value>0.05), increasedprefrontaloxygenationcannotbeassociatedwitha gen-eralincreaseofthesystemiccardiovascularactivity.
4. Discussion
Usinganovelmentalarithmeticn-backtask(i.e.Toulouse N-backTask),weexaminedintwoseparatestudieshowmentaleffort andstressimpactedtaskperformance,pupilresponse(study1), cardiovascularactivity(study1and2),andprefrontalcortex oxy-genation(study2).Highertaskdifficulty(highernlevel)increased perceiveddifficulty,degradedtheperformanceandprovokedan increasedtonic pupildiameter,HR and oxygenationin the lat-eralprefrontalcortex,andadecreasedphasicpupilresponseand
HRV.Importantly,theconditionofstressdidnotimpactthe per-formance, but at the expense of a psychophysiological cost as demonstratedbylowerphasicpupilresponse,increasedHRand greaterprefrontaloxygenation.Thesefindingsconfirmedthe psy-chophysiologicalcostofbothmentaleffortandstressandsupport thecommonideaoftheprocessingefficiencytheory(Eysenckand Calvo,1992)andthecognitive-energeticalframework(Robertand Hockey,1997),namely,thefactthatstresscanreducehuman cog-nitiveefficiency,evenintheabsenceofavisibleimpactonthetask performance.Stresslikelytriggeredincreasedmotivationandthe recruitmentofadditionalcognitiveresourcesthatminimizedits aversiveeffectsontaskperformance,butthiswasassociatedwith alossofcognitiveefficiency.
4.1. Thepsychophysiologicalcostofmentaleffort
The increase of subjective perceived difficulty, thedecrease ofperformance(d-primescore)andtheincreaseinthe percent-ageofmissedresponsesacrossthethreen-backlevelsconfirmed thatmentaleffortwasefficientlymodulated.Thishigherdifficulty causedanincreasedtonicpupildiameterandHRandadecreased phasicpupilresponseandHRV.Classically,highertonicpupil diam-eter(Beatty,1982;Causse,Sénard,Démonet,&Pastor,2010;Reiner &Gelfeld,2014;Peysakhovich,Causse,Scannella,&Dehais,2015), increasedHR,anddecreasedHRV(Riese,1999;Causseetal.,2011a) arefoundunderconditionsofhighload.Interestingly,thephasic pupilresponsediminishedwithincreaseddifficulty,ina similar fashionthanthecommonlyobservedreducedamplitudeof elec-troencephalographyevent-relatedpotentialswhenresourcesare consumedbyahighmentalworkload(VanDillen&Derks,2012;
Giraudet,St-Louis,Scannella,&Causse,2015;Causseetal.,2016). Contrary totonicpupildiameterthat is usedtomeasure men-taleffortthroughoutthedurationofatask,event-relatedphasic changesinpupildiameterrelatetoacutetaskdemands(Brunyé etal.,2016).Astonicloadonmemoryincreasedwiththenlevel, itislikelythatfewerresourceswereavailabletoprocessthe arith-meticoperationswhichinturnprovokedareducedphasicpupil responsetotheseoperations.
TheTNTincreaseddifficultyalsoyieldedgreaterPFC oxygena-tion.ThisisconsistentwithpreviousstudiesshowingthatfNIRS
issensitivetoWMload(Fishburnetal.,2014;Gateauetal.,2015; Herffetal.,2014;Pecketal.,2014;Yukseletal.,2015),ormental workload,forexampleduringanarithmetictask(Mandricketal., 2013a).Asinpreviousworks(Fishburnetal.,2014;Owenetal., 2005;Satoetal.,2013),thisincreasedoxygenationwasrather local-izedinleft/rightlateralregions,whichconfirmsthecrucialroleof thelateralregionsoftheprefrontalcortexinworkingmemory pro-cesses(Curtis&D’Esposito,2003;Owen,Evans,&Petrides,1996;
DePisapia,Slomski,&Braver,2007)andmentalarithmetic(Gruber, Indefrey,Steinmetz,&Kleinschmidt,2001).
4.2. Thepsychophysiologicalcostofstress
AssuggestedbyDavisetal.(2010)theexpectancyofan unpre-dictableanduncontrollablestressorshouldbesufficienttocreate athreateningcontextandtodegradetaskperformance(Barrett& Armony,2006),atleastwhenthependingstimulusissufficiently aversive(Grillonetal.,2004).Ithasbeenpreviouslyshownthat even quitemild stresscancause a rapidloss of cognitive abil-ities (Arnsten, 2009, 2015). However,in the present study, we didnot observea significanteffectoftheauditorystressorson taskperformance.Yet,thesurveysconductedpriortothe exper-iment,theratingsof theparticipantsin thepresentstudy, and theresultfromthespectralfrequency–temporalmodulation anal-ysissuggest that ourauditory stimuli should beconsidered as mildlystressful.Importantly,inthelight oftheprocessing effi-ciencytheory(Eysenck&Calvo,1992)andthecognitive-energetical framework (Robert and Hockey,1997), ourpsychophysiological resultsmightbeinterpretedasareducedcognitiveefficiencyas participantsmighthaveemployedcognitivestrategiesand com-pensatoryeffortduringthestressconditioninordertomaintain theirperformance (Eysenck &Calvo,1992; Eysenck,Derakshan, Santos,&Calvo,2007).Wearguethatthecognitiveperformance effectiveness(qualityofperformance)inthetaskwasnotimpaired bythestressorsthankstotheenhancedeffortanduseofauxiliary processingresourcesandstrategies,butinturn,theprocessing effi-ciency(performanceeffectivenessdividedbyeffort)wasmarkedly reduced.Thisreducedprocessingefficiencywasreflectedbythe decreasedphasicpupilresponse,whichlikelyindexedthedecline oftheavailableresourcestocomputethearithmeticoperations. TheincreasedHRfoundinthethreatconditionconfirmedthatthe threatofunpredictableaversiveloudsoundsprovokedasignificant elevationofthelevelofstress/anxiety.TheamplitudeoftheHR elevationwasconsistentwithresultsfromBrosschotandThayer (2003)studythatrevealedanincreaseofHRofapproximatively1 beatperminuteafternegativeevents.
PFCoxygenationwasalsomoreimportantduringthreat condi-tion.Thissupportstheideathatcompensatoryeffortwasengaged tocopewiththethreat.Previousneuroimagingstudiesshowed thatPFC is sensitivetoemotion (Doi etal., 2013;Tupak et al., 2014),andthatthisbrainregioncontributestoregulationof cog-nitiveprocesseswithemotion(Beer,Knight,&D’Esposito,2006;
Hänsel&Känel, 2008;Seo and Sinha,2011(ch9)).Interestingly, dorsolateralPFCseemstohaveapivotalroleinthecognitive con-trolofemotion(Cerqueiraetal.,2008;Miller andCohen,2001; Robinsonetal.,2013;SeoandSinha,2011(ch9))andrecent liter-aturealsosupportsthehypothesisthatdorsolateralPFCregions subservescrucialfunction,suchasexecutivecontrolandworking memory,thatcontributetotheregulationofemotion(Okon-Singer, Pessoa,&Shackman,2015).Theexecutivecontrolwouldactasa shieldtoprotectcognitionfromtheinfluenceofemotional dis-tractors(Clarke&Johnstone,2013;Robinson etal.,2013).Also, someauthorshavepostulatedthatPFCexertsacontrolondeep brainlimbic regions, suchas the amygdala, in order to modu-latetheeffectsofthreat.Forexample,Vytal,Overstreet,Charney, Robinson and Grillon(2014) showed that PFC(particularly the
bilateraldorsomedialportion)sustains defensivereadiness dur-inganxietybymaintainingsynchronizedandcoupledinteraction withthebilateralamygdala.Authorsstatedthattheconnectivity betweenPFCandamygdala“mayservetokeeptheamygdalain aprimedstateduringuncertainthreatandthendriveoramplify amygdalareactivity whenanexplicitthreatisencountered”.As fNIRSdeviceusedinthisstudycouldnotmeasuredeepregions ofthebrain,theassumptionthatdorsolateralPFCpossibly partici-pateincognitivestrategiestocopewiththeaversiveeffectofstress, throughmodulationofsubcorticalandlimbicregions(forexample, hypothalamus,hippocampus,andamygdala),shouldbeconfirmed byafuturefMRIstudy.
Contrarytostudiesshowingthattheimpactofstressis miti-gatedbytaskdifficulty(Clarke&Johnstone,2013;Pateletal.,2015; Robinsonetal.,2013), andotherworkshowingthat distracting effectsarereducedwhenattentionisstronglyengagedinatask(Hu etal.,2012;Pessoaetal.,2002;VanDillenetal.,2009),orauthors thatputforwardtheideaofadynamicbalancebetweenemotion andcognitioninthebrain(Drevets&Raichle,1998),theimpactof thethreatonbehaviorandpsychophysiologywasnotsignificantly modulatedbytaskdifficultyinourstudy.Yet,visualinspectionof theprefrontalcortexactivationsuggestsalargereffectofthreaton theprefrontalactivityinthe0-backconditionincomparisonto 1-backand2-backconditions.Coherently,effectsizes(irrespectively oftheregionsofinterest)showedthatthestrengthoftheimpactof thethreatconditionwereclearlylargerin0-backcondition com-paredto1-backand2-backconditions.Anincreasedsamplesize mighthaverevealedasignificantmitigationoftheimpactofstress onprefrontalactivitybytaskdifficulty.
5. Conclusion
Toourknowledge,thisisthefirststudytoinvestigatethe reg-ulationof humanperformance under stressand highworkload using pupil diameter, cardiovascular and prefrontal oxygena-tionmeasurements.ParticipantsperformedtheToulouseN-back Task, which mimics the multidimensional high mental work-loadexistinginmanysafety-criticaloccupations.Duringthetask, weinducedsustainedanxietyusingthethreatofunpredictable loudsounds,proventobemildlystressfulbysurveysconducted priorand duringtheexperimentand byresultsfroma spectral frequency–temporalmodulationanalysis.Weconfirmedthathigh mentaleffort(generatedbyanincreasedlevelofworkingmemory load)provoked increasedsubjective perceiveddifficulty, lower-ingoftheperformance,increasedtonicpupildiameterandheart rate,decreasedphasicpupilresponseandheartratevariability,and finallyincreasedprefrontaloxygenation,particularlyinthe dor-solateralPFCregions. Thethreatof unpredictableaversive loud soundsdidnotimpact taskperformance. We suggest that cog-nitiveperformance maybeprotectedfromstress thankstothe triggeringofcognitivestrategiesandcompensatoryeffortinorder toperformthetaskadequately, but mostlikely attheexpense ofapsychophysiologicalcostassuggestedbylowerphasicpupil response,andincreasedheartrateandprefrontaloxygenation.In fine,mildstressmightreducehumancognitiveefficiency(because ofthecompensatoryeffort),evenintheabsenceofavisibleimpact ontaskperformance(effectiveness).ThePFCseemstobeacentral regionformitigatingtheinfluenceofstresssinceitsubserves cru-cialfunctionsthatsustaincopingstrategies(Arnsten,2009),such asexecutivecontrolandworkingmemory(Schmeicheletal.,2008; Okon-Singeretal.,2015).Finally,wemightpostulatethatamore intensestress,whichwouldhavecausedastrongelevationofthe HR,mayhavefinallyprovokedadeclineofperformanceinthetask. Thus,thepresentpaperalsocallsintoquestionthepossibilityto
studyvisiblealterationoftheperformanceunderstresswiththe useofthethreatofaversiveloudsounds.
Authorcontributions
MK,VP,LE,RF,andCMdesignedtheresearch,andMKandVP performedtheexperiments.MKandVPanalyzedthedata.MK,CM, VPpreparedthefiguresandwrotethemanuscript.LE,RF,andCM reviewedthemanuscript.
Conflictofintereststatement
Theauthors declarethat theresearchwasconducted inthe absenceofanycommercialorfinancialrelationshipsthatcouldbe construedasapotentialconflictofinterest.
Acknowledgements
This work was supported by the French Research National Agency and the French Defence Procurement Agency via the Accompagnement Spécifique des travaux de Recherches et d’InnovationDéfense(ASTRID).
AppendixA. Supplementarydata
Supplementarydataassociatedwiththisarticlecanbefound,in theonlineversion,athttp://dx.doi.org/10.1016/j.biopsycho.2016. 10.002.
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Furtherreading
Chi,T.,Ru,P.,&Shamma,S.A.,2005.Multiresolution spectrotem-poral analysis of complex sounds. The Journalof the Acoustical SocietyofAmerica.118(2)887–906.doi:10.1121/1.1945807.
Kumar,S.,Kriegstein,K.,Friston,Von,&Griffiths,K.2012. Fea-turesversusfeelings:Dissociablerepresentationsoftheacoustic featuresandvalenceofaversivesounds,TheJournalofNeuroscience, 32(41)14184–14192.doi:10.1523/jneurosci.1759-12.2012.
Shamma,S.2003.Encodingsoundtimbreintheauditorysystem IETE,JournalofResearch,49(2-3)145-156
