ContentslistsavailableatScienceDirect
NeuroImage
journalhomepage:www.elsevier.com/locate/neuroimage
Spatiotemporal
dynamics
of
attentional
orienting
and
reorienting
revealed
by
fast
optical
imaging
in
occipital
and
parietal
cortices
Giorgia Parisi
a,b, Chiara Mazzi
a,b,∗, Elisabetta Colombari
a,b, Antonio M. Chiarelli
c,
Brian A. Metzger
d, Carlo A. Marzi
a, Silvia Savazzi
a,ba Department of Neuroscience, Biomedicine and Movement Sciences, University of Verona, Strada le Grazie 8, Verona, Italy
b Perception and Awareness (PandA) Laboratory, Department of Neuroscience, Biomedicine and Movement Sciences, University of Verona, Strada le Grazie 8, Verona, Italy
c Department of Neurosciences, Imaging and Clinical Sciences, University G. D’Annunzio of Chieti Pescara, Via dei Vestini 31, Chieti, Italy d Department of Neurosurgery, Baylor College of Medicine, 1 Baylor Plaza, Houston, TX, USA
a
r
t
i
c
l
e
i
n
f
o
Keywords: Visuospatial attention Orienting Reorienting Optical imaging EROS Granger causalitya
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Themechanismsofvisuospatialattentionaremediatedbytwodistinctfronto-parietalnetworks:abilateral dor-salnetwork(DAN),involvedinthevoluntaryorientationofvisuospatialattention,andaventralnetwork(VAN), lateralizedtotherighthemisphere,involvedinthereorientingofattentiontounexpected,butrelevant,stimuli. Thepresentstudyconsistedoftwoaims:1)tocharacterizethespatio-temporaldynamicsofattentionand2)to examinethepredictiveinteractionsbetweenandwithinthetwoattentionsystemsalongwithvisualareas,by usingfastopticalimagingcombinedwithGrangercausality.Datawerecollectedfromyounghealthyparticipants performingadiscriminationtaskinaPosner-likeparadigm.Functionalanalysesrevealedbilateraldorsal pari-etal(i.e.dorsalregionsincludedintheDAN)andvisualrecruitmentduringorienting,highlightingarecursive predictiveinterplaybetweenspecificdorsalparietalregionsandvisualcortex.Moreover,wefoundthatboth attentionnetworksareactiveduringreorienting,togetherwithvisualcortex,highlightingamutualinteraction amongdorsalandvisualareas,which,inturn,predictssubsequentventralactivity.Forattentionalreorientingour findingsindicatethatdorsalandvisualareasencodedisengagementofattentionfromtheattendedlocationand triggerreorientationtotheunexpectedlocation.Ventralnetworkactivitycouldinsteadreflectpost-perceptual maintenanceoftheinternalmodeltogenerateandkeepupdatedtask-relatedexpectations.
1. Introduction
Visualattentionconsistsofthosepsychologicalandneuralprocesses whichmediatetheprocessingofbehaviorallyrelevantsensory informa-tion(Capotostoetal.,2012).Sensoryinformationcanbeselectedeither throughvoluntarydeploymentofattentionalcontrol(goal-directed at-tention)orcanbeorientedorreorientedinresponsetonovelor unex-pected,butimportant,stimuli(stimulus-drivenattention).Animportant pointisthatattentioncanbeallocatedinspacenotonlyovertlybutalso covertly,i.e.inabsenceofheadoreyesmovements.Also,covert atten-tioncanbedirectedtowardseitherbehaviorallysignificantlocationsor regionsofspaceincludingunexpectedbutsalientstimuli.Inthecaseof visuospatialattention,goal-directedandstimulus-drivenattention pro-videatypicalsystemofselectionofrelevantinformation:sensory in-putatattendedlocationsisdirectlyenhanced,whereasatunattended positionsareorientingprocessistriggeredtolikelyimportantstimuli (Nataleetal.,2009).
∗Correspondingauthorat:DepartmentofNeuroscience,BiomedicineandMovementSciences,UniversityofVerona,StradaleGrazie8,I-37134Verona,Italy.
E-mailaddress:chiara.mazzi@univr.it(C.Mazzi).
Psychophysical assessment of covert orienting and reorienting is achievable by meansof spatialcueing paradigms (Posner, 1980) in whichacentralsymboliccue(e.g.anarrow)providesrelevant informa-tionaboutthelocationofanupcomingperipheraltarget.Inthemajority oftrials(75–80%probability),thisinformationiscorrect,i.e.the up-comingtargetispresentedatthecuedlocation(validtrials),whereas, intheminorityoftrials(25–20%ofcases),thecuegivesawrong in-dication(invalidtrials)asthetargetispresentedattheuncued loca-tion(Capotostoetal.,2012;Doricchietal.,2010;Nataleetal.,2009; Vosseletal.,2006).Reactiontime(RT)istypicallyfasterinvalidthan invalidtrialsandthedifference(“validityeffect”)representsanindex ofthetimeneededtodisengageandshiftattentionfromanattendedto anunexpected,behaviorallyrelevantlocation(Posner,1980).
Fromaneuroanatomicalpointofview,visuospatialattention mech-anismshavebeenlinkedtoparietalandfrontalcortices(Corbettaetal., 2008; Corbetta andShulman, 2002; Shomstein, 2012; Vossel et al., 2006).Specifically,ithasbeenproposedthatattentionalorientingand
https://doi.org/10.1016/j.neuroimage.2020.117244
Received3April2020;Receivedinrevisedform5June2020;Accepted3August2020 Availableonline14August2020
1053-8119/© 2020TheAuthor(s).PublishedbyElsevierInc.ThisisanopenaccessarticleundertheCCBY-NC-NDlicense. (http://creativecommons.org/licenses/by-nc-nd/4.0/)
reorientingareregulatedbytwoanatomicallydifferent,though func-tionally interconnected, cortical networks: a bilateral dorsal fronto-parietal (DAN) and a ventral fronto-parietal network (VAN). DAN, whichbecomesactivatedastop-downcuesorientattentiontospecific locations(Corbettaetal.,2000,2008),includestheintraparietal sul-cus(IPS),thesuperiorparietallobule(SPL)andthefrontaleyefields (FEF).Incontrast,reorientingattentiontounattendedlocationsengages VAN.Thisnetworkislateralizedtotherighthemisphereandincludes thetemporo-parietaljunction(TPJ)andtheventralfrontalcortex(VFC) whichmainlyincludesportionsofthemiddlefrontalgyrus(MFG)and theinferiorfrontalgyrus(IFG)(Corbettaetal.,2008).
Itis generally accepted that DANand VANarecharacterized by anatomicalsegregationand functionalspecialization so thateach of themsubservesspecificprocessesofallocationofattention(Vosseletal., 2014).
ThereisstrongevidenceabouttheexclusiveroleofDAN(especially IPSandSPL)intop-downattentionorienting,andthatparietalregions exerttop-downattention-relatedmodulationonstriateandextrastriate visualareas(Bressleretal.,2008;Doesburgetal.,2016;Vosseletal., 2012).Conversely,therelationshipbetweenDANandVANandtheir re-spectivecontributionsinthereorientingprocessarestillnotcompletely clear.Moreprecisely,voluntaryattentionalorientingisthoughtto en-gagethedorsalnetworkonlywhileattentionalreorientingwould re-quireaninteractionbetweenthetwoattentionnetworks,however,the exactnatureofthisinteractionisstilldebated(Corbettaetal.,2008; Vosseletal.,2014).
Infact,previousimagingstudieslookingatvisuospatialattentional reorientinginresponsetoinvalidspatialcueshaverevealedactivityin ventralregionsandbilateralIPS(Vosseletal.,2006,2012),andright SPLaswell(Vosseletal.,2009).Inagreementwiththeseresults, tran-scranial magnetic stimulation(TMS)studies (Capotostoet al., 2012; Chicaetal.,2011)haveshownthecriticalroleofrightIPSwhen atten-tionisspatiallyreorientedtounattendedbutrelevantstimuli.Although thesefindingsstronglysupporttheexistenceofaninterplaybetween theDANandVANduringspatialreorienting,littleisknownaboutthe timingofthisinteraction.Sofar,theexactroleofdorsalandventral regionsinattentionalprocessesremainsuncertain,aswellasthe pre-dictiveconnectionsbetweenthem,especiallyinthedifferentphasesof attentional reorienting(disengaging, shiftingandengaging attention; Posner,1980).
Previous imaging studies have not provided enough information aboutthe time-courseof attentional processing,along withaccurate localizationofspecificallyactivatedcorticalareas.Toaddressthis is-sue,techniqueswith bothgood temporalandspatialresolutionsare needed. Todate, themost widely employedtechniques can achieve highresolutioninjustonedimension(i.e.spaceortime)andtheonly optionhasbeentocombinedifferentmethodologies(Gratton,2010). Unfortunately,becauseoftheoreticandtechnicalmismatchesbetween distincttechniques(Luck,1999),thisoptioncannotfulfillthegoalof providingbothspatialandtemporalinformationonthecognitive pro-cessunderstudy.Toovercomethisproblem,opticalimagingmethods havebeguntobeemployed.Inparticular,arelativelynovelapproach, namedEvent-RelatedOpticalSignal(EROS)orFastOpticalSignal(FOS) (Chiarelli etal.,2013, 2014;Gratton etal., 1995;Gratton and Fabi-ani,2001)representsanappropriatetooltoaddressthisquestion.Its mainadvantageistheabilitytodetectvariations(i.e.fastoptical sig-nals)inopticalscatteringtypicaloftheneuraltissuewhenitisactive, asopposedtowhenitisnot(Gratton,2010).EROS,availingof near-infraredlight(NIR),detectsreductioninthelight-scatteringwhichis associatedwithchangeinmembranepotentialsandwithanincrement ofbrainactivities(Grattonetal.,1995).Thus,itprovidesameasure of neuronalactivitywith ahigh temporallocalizationpowerof less than50ms(Baniquedetal.,2013),whichisclosetowhatcanbe ob-tainedwithelectroencephalography(EEG)and magnetoencephalogra-phy(MEG).Moreover,thankstothegeometryoftheopticalprobes, thediffusionofdetectedNIRlightthatpassedacrossthebrainis
re-strictedenoughtoobtainasufficientlylocalizedsignal(ontheorderof cm),obtainingaspatiallocalizationpowersuperiortoEEGandMEG andwhichrevealsactivityfromextensiveareasofthecorticalsurface (Gratton,2010).Thisrelativelynewtechniquehasbeenvalidatedby manystudies(Baniquedetal.,2013;Huangetal.,2013;Sableetal., 2007;Toscanoetal.,2018)supportingitsfeasibilityandreliabilityin investigatingthedynamicsof brainactivationsofspecificcortical re-gionsduringtheperformanceofcognitiveoperations(Grattonetal., 1997, 2000;Rykhlevskaiaetal.,2006;Tseetal.,2013).Inaddition, theadvantagesofthistechniquecanbemaximizedbycombiningEROS analyseswithGrangercausality.Thisassociationallowsustoexplore, notonlythetimingofactivationsofdistinctbrainareasbutalsoto deter-minewhetheractivityinoneseedareaispredictiveofsuccessiveactivity inotherregions.Importantly,Grangercausalitycalculateswhetherdata fromadefinedareaofinterestinaspecifiedtemporalwindowcan pre-dictthevaluesofanotherregionactivatedinasubsequenttimeframe (Roebroecketal.,2005),thusrevealingthedirectionofinfluences be-tweenselectedregionsofinterest(ROIs).Granger’ssuitabilityfor inves-tigatingdirectionalrelationshipsbetweenbrainregionsinhuman cog-nitionhasalreadybeenassessedinpreviousfMRI,EEGandMEGstudies (Bressleretal.,2008;Doesburgetal.,2016;Proulxetal.,2018). Con-sideringthatitisastatisticalmeasureofdirectionalinfluencesbetween ROIsbasedsolelyontheirtemporalprecedence(Roebroecketal.,2005), itsapplicationtoEROS,thathashightemporalandspatiallocalization power,isidealtoimproveourunderstandingabouthowinformationis sharedbetweenbrainregionsengagedinspecificcognitivetasks.
Inthepresentstudy,anendogenousspatialcueingparadigmwas administeredtohealthyparticipants.Inthiskindoftask,processingof valid andinvalidtrialsstarts withtheinterpretation ofthesymbolic cue,followedbyavoluntaryallocationofattentionandacue-related orienting-response.Thisimpliesdifferentoperations:disengagingfrom afixationpoint,shiftingandengagingattentiontothesignaledlocation. Inthecaseofinvalidtrials,themismatchbetweenattendedandactual locationofthetargetrequiresfurtherattentionalmechanisms,namely, disengaging,shiftingandre-engagingattentiontothecorrectlocation (Nataleetal.,2009).
BycouplingthisbehavioralapproachwithEROSandGranger causal-ity,capableofidentifyingthetimingofactivationindefinitebrain re-gionsandtounveilthepredictiverelationshipamongthem,thepresent studyaimsatcharacterizingtheneuralspatio-temporaldynamicsof at-tentionalprocesses.Inparticular,exclusivelyfocusingonparietaland temporalcortices,wesoughttotracethetime-courseofbrainactivations inposteriornodesoftheDANandVANtoclarifythedifferentrolesof dorsalandventralregionsinattentionalorientingandreorienting. 2. Materialandmethods
2.1. Participants
Atotaloftwenty-nineright-handed(asassessedbytheEdinburgh Handedness Inventory,Oldfield, 1971)adults, wererecruitedfor the studyandreceivedcompensationfortheirparticipation.Allreported normalorcorrected-to-normalvisualacuityandnohistoryof neurolog-icalorpsychiatricdisorders.Allbuttwo(authorsG.P.andE.C.)were naïvetothegoalsofthestudy.
Allparticipantsgavetheirwritteninformedconsentbefore partici-patinginthestudy,whichwasconductedinaccordancewiththe2013 declarationofHelsinkiandapprovedbytheEthicsCommitteeofthe Eu-ropeanResearchCouncilandoftheVeronaAziendaOspedaliera Univer-sitariaIntegrata(AOUI).Datafrom8participantswereexcludedfrom theanalysisbecauseoftechnicaldifficultiesduringimagingdata acqui-sition,suchasdigitizationissues(2participants),lowscattering param-etersduetodarkskinandhair(2participants)oraninsufficient num-berofgoodchannelscausedbydetectorovervoltage(4participants). Therateof participants’exclusion,duetoimagingacquisitionissues, appearstobehigherthanthattypicallyfoundinEROSstudies.Inthis
case,EROSsetupandopticaldatarecordinghaverequiredalittle re-finementduringthefirstperiodofdatacollection,thusengenderinga higherrateofdataexclusionthanusual.
Moreover,datafromother3participantswerediscardedas behav-ioraltaskoutliers.Thefinalsamplewasthuscomposedofeighteen par-ticipants(3males,meanage±standarddeviation:24±3.7).
2.2. Experimentalprocedure
Thewholeexperimentincludedtwosessionsperformedover two separatedays.Thesesessionswereidenticalinsettingandbehavioral conditions(typeoftask,numberofblocksandtrials),exceptforEROS montages(seebelow).Theexperimentwasdividedintotwosessionsin ordertoobtainanadequatenumberoftrialswhileavoidingfatiguefor participants.
Intotal,eachsessionlastedaboutthreeandahalfhours,which in-cludedEROSsetup,opticaldatarecordingduringthebehavioraltask, andco-registrationproceduresconsistingofthedigitizationofoptode scalplocations.
2.3. Behavioraltask
Participantsweretestedinadarktestingroom.Duringthe exper-imentalsessions,theysatinfrontofa17in.LCDmonitor(resolution 1920×1080,refreshrateof144Hz)placedataviewingdistance of 57cm,withheadlayingonanadaptablechinrestsothateyescouldbe alignedwiththecenterofthescreen.
A modified version of an endogenous spatial attention cueing paradigm(Posner,1980),wasemployed(seeFig.1A).
Eachtrial beganwiththepresentationof acentralblackfixation cross,followed500mslaterbyacentralpredictivecuepresentedfor 200msabovethefixationpoint.Afteravariablerandomizedinterval, lastingbetween300and600ms,thecuedisappearedandwas immedi-atelyfollowedbytargetonset(averticalorhorizontal,black-and-white, 2° squaregrating)presentedataneccentricityof2° fromthefixation crosstotheinneredge,alongthehorizontalmeridian.Participantswere instructedtodeploytheir attentiontotheside indicatedbythe cue whilemaintainingtheirgazeonthecentralfixationcrossthroughout theblock.Targetswerepresentedfor150msafterwhich,theywereto discriminateasfastandasaccuratelyaspossibletheorientationofthe targetbypressingoneoftwobuttonsofaresponseboxwiththeindex forhorizontaltargetsorwiththemiddlefingerforverticaltargets.
Ineach block,horizontalandverticalgratingsrandomlyoccurred withthesameprobability.Moreover,trialscouldbevalid(75%),thatis whenthetargetwaspresentedtothecuedvisualhemifield,orinvalid (25%),whenthetargetwaspresentedtotheuncuedvisualhemifield.
Eachexperimentalsessionwascomposedof24blocks(foratotalof 48blocksperparticipant).Thecuedirectionwasconsistentthroughout ablock:inhalfof theblocks(n =12)itpointedtotheright,while, intheotherhalf,totheleftvisualhemifield.Theorderofblockswas alternatedineachexperimentalsession.
Eachblockconsistedof64trialsforatotalof3072trials(2304valid, 768invalid)perparticipant.Participantscouldrestduringinter-block intervalsandcouldinitiatethenextblockbypressingakey.
2.4. Opticalrecording
EROSdatawererecordedfortheentirebehavioralexperiment,using twosynchronizedImagentfrequencydomainsystems(ISS,Inc., Cham-paign,IL).Thirty-twolaserdiodesemittednear-infraredlight(830nm) inatime-multiplexedscheme.Thediodesweremodulatedat110MHz andthelightwasdeliveredintothebrainthrough400μmsilica op-ticfibers.Thediffusedlightwhichexitedfromtheheadwasdetected byeight3-mmfiber-opticbundles,connectedtophotomultipliertubes (PMTs).Sourceanddetectorfibers weresecuredontheparticipant’s headthrough acustom-builthelmet,availableintwodifferent sizes.
ThePMTinputsweremodulatedataslightlydifferentfrequency com-paredtolaserdiodesdeliveringa3125Hzcross-correlationfrequency. FastFouriertransformwasappliedtothePMTsoutputcurrentin or-dertocomputetheDCintensity,ACamplitudeandrelativephasedelay (sourcetodetector)ofthesignal.Inthisstudy,onlychangesinphase delaydata(convertedintopicosecondsdelay)wereanalyzed.
Foreachhelmetsize,twodifferentmontages(seeFig.1C)wereused forthetwosessionsandcombinedduringanalysesprovidingdense cov-erageoftheoccipitalandposteriortemporo-parietalcortices,butnot thefrontalcortex(duetoalimitednumberofavailableoptodes).Each montagewastopermiteachdetectortodetectlightfromupto16 time-multiplexedsources. Ineach montagesourcesanddetectorswere lo-catedinsuchawayasthatasubsetofsourcescouldemitlight simul-taneouslywithoutcausingcross-talk(lightfrommultiplesources simul-taneouslyrecordedatadetector),resultingin128potentialchannels persession(with aminimumandmaximumsource-detectordistance respectivelyof17.5and50mm;Grattonetal.,2000).
Thecyclethrougheachofthe16multiplexedsetsofsourceslasted 25.6ms(eachsourcewasswitchedonfor1.6msandoff for24ms,in afixedsequence)achievingasamplingrateof39.0625Hz.
StructuralMRIscanswereobtainedforeachparticipant.Scanning tookplaceina1.5TeslaPhilipsscannerattheBorgoRomaHospital inVerona,usingastandard15-channelheadcoil.Awholebrain high-resolution3DT1-weightedimagewithmagnetization-preparedrapid ac-quisitiongradientecho(MPRAGE)wasacquiredwiththefollowing pa-rameters:phaseencodingdirection=anteriortoposterior,voxelsize= 0.5×0.5×1mm,RepetitionTime=7.7ms,EchoTime=3.5ms,field ofview=250×250mm,flipangle=8°
FollowingeachEROSsessioneverysourceanddetectorholder loca-tiononthehelmet,aswellasfiducialpoints(nasionandpre-auricular points), were digitized using a neuronavigation software (SofTaxic, E.M.S., Bologna,Italy) combinedwitha 3Dopticaldigitizer (Polaris Vicra,NDI,Waterloo,Canada).
The digitized scalp optical locations were co-registered withthe structuralMRimagesusingamethodimplementedinanOCPsoftware package(OptimizedCo-registrationPackage,MATLABcode)developed byChiarelliandcolleagues(Chiarellietal.,2015),andmainlybasedon scalpforcingandfiducialalignmentprocedures(Whalenetal.,2008). Finally,co-registereddataweretransformedtoMNIspaceforthe fol-lowinganalyses.
ContinuousfastopticaldatawerecollectedusingtheISSCorporation “Boxy” programandpreprocessedbymeansofP-POD(Pre-Processing ofOpticalData,MATLABcode)anin-housesoftware.Themeanphase delaywasadjustedtozeroforeach block.Datawerethencorrected forphasewrappingandde-trendedtoremovelow-frequencydriftsand baselinecorrected.Beforearterialpulseartifactwasremoved(45–200 heartbeatrange)byusingaregressionalgorithm(Grattonand Corbal-lis,1995),thephaseofthemodulatedlightwasconvertedintotime de-layofthedetectedphotons,expressedinpicoseconds.Aband-passfilter wasthenappliedtoremovefrequenciesbelow0.5Hzorabove15Hz. Finally,theresultantdataweresegmentedintoepochstime-lockedto thetargetonsetandaveragedseparatelyforeachparticipant,condition, andchannel.ThelengthoftheepochswasdifferentforthethreeEROS contrasts(seebelowSectionEROSanalysis):1484ms(486msbefore tar-getonsetand998msafter)forvalidvs.baselineandinvalidvs.baseline and1535ms(1280msbeforetargetonsetand255msafter)forallvs. baseline.
Opt-3d custom software package (Gratton, 2000) was employed tocomputestatistics onfunctionaldata.Opticalsignalsfrom source-detectorchannelswhosediffusionpathintersectedagivenvoxelwere averaged(Wolfetal.,2014).Phasedelaydatawerebaselinecorrected usingeithera200mspre-targetintervalora200mspre-cueinterval (dependingontheconsideredanalysis,seeDataanalysissection)and spatiallyfilteredwithan8-mmGaussiankernel.Group-levelt-statistics werecomputedacrossparticipantsandthenconvertedtoz-scoresfor eachvoxelateachofthetimepoints.Z-scoremaps,calculatedfromthe
Fig.1. Methodandbehavioralresults.
(A)Experimentalparadigm.Afixationcrosswaspresentedfor500msfollowedbyacentralinformativecuelasting200ms.Participantswereinstructedtocovertly directattentiontothesideofspacedepictedbythecue.Thetargetstimulusappearedafterarandomintervalrangingfrom300to600msandpresentedfor150ms. Participantswerethengiven1500mstodiscriminatethetargetorientation(i.e.verticallyorhorizontallyorientedgratings).Inthisexample,avalidtrialisshown (i.e.thecuepointstothesamevisualhemifieldinwhichthetargetsubsequentlyoccurs).(B)Behavioralresults.Meanresponsetimes(left)andpercentageofcorrect responses(right)areplottedasafunctionofwhetherthetargetappearedintherightorlefthemifield(x-axis)andasafunctionofwhethertheattentioncuewas validorinvalid(separatelines).Errorbarsrepresentstandarderrors.(C)Opticalmontages.Tworecordingmontageswereusedforeachhelmetsize.Infraredoptical sources(yellowdots)anddetectors(bluedots)wereplacedtomaximizerecordingcoverageoverparietalandoccipitalcortex.Hereweshowsourceanddetector locationsplottedontotheanatomicalscanofarepresentativeparticipant.(D)SelectedROIs.EstimatedboundariesoftheselectedROIsusedforEROSandGranger analyses.ROIsaredisplayedincoronal(visualregions),axial(dorsalregions)andsagittal(ventralregion)viewsasconsideredforstatisticalanalysesandtheir coordinatesarereportedinTable1.
p-valueforeacht-test,werecorrectedformultiplecomparisonsbased onrandomfieldtheory(Kiebeletal.,1999;Worsleyetal.,1995). Subse-quently,Z-scoreswereweightedandorthogonallyprojectedontoimages ofthecoronal,sagittaloraxialsurfaceofatemplateMNIbrain, accord-ingtothephysicalhomogenousmodel(ArridgeandSchweiger,1995; Gratton,2000).SeeSupplementaryMaterial:Fig.1foraschematic rep-resentationofthedifferentstepstocollectandprocessthedata.
ROIs forthe statistical analysiswere selectedboth by inspection ofthefunctionaldataand,moreimportantly,byselectingthoseareas foundselectivelyactivatedintheliteratureonattentional control,in accordancewithareasencompassedbyEROScoverage(Fig.1D).ROIs werethusplacedalongtheposteriorportionofDAN,i.e.leftandright SPL(l/rSPL)andleftandrightIPS(l/rIPS),alongthetemporo-parietal portionofVAN,i.e.leftandrightTPJ(l/rTPJ)andwithintheoccipital lobe,i.e.V1andthedorsalportionofthecuneus.ROIswereidentified relyingonanatomicalcoordinatesofparietal,temporalandoccipital ar-easusedinliterature(e.g.Baniquedetal.,2018)andthecorrespondent
Brodmannareasinwhichtheseregionsareknowntobeincluded(i.e. BA7forSPL,theintersectionofBA7andBA39forIPS,BA39forTPJ, BA17forV1,BA18and19forcuneus).Specifically,theYaleonline search tool (http://sprout022.sprout.yale.edu/mni2tal/mni2tal.html) wasusedtodefineROIsboundariesinordertopreventorreduce over-lap ofdifferent ROIs,giventhattheconsideredareas arecontiguous in thehumanbrain(seeTable1).AlltheROIsweredefinedbya 2-dimensionalbox-shapedstructure(thethirddimensionismissingasthe opticalsignalisprojectedonthebrainsurface).SeeTable1whereonly twodimensionsarelistedforROIsthatwereanalyzedusingseparately axial(x,y),sagittal(y,z)orcoronalprojections(x,z).
2.5. Dataanalysis 2.5.1. Behavioraldata
DatawereprocessedusingMATLAB2013bandanalyzedwithIBM SPSSStatisticsforWindows,version22.
Table1
MNIcoordinatesofselectedROIs.
Region Projection Coordinates Involved BA
Right SPL Axial x = y = 0 − 84 20 − 64 7 Left SPL Axial x = y = − 20 − 84 0 − 64 7 Right IPS Axial x =
y = 26 − 87 40 − 59 7–39 Left IPS Axial x =
y = − 36 − 87 − 22 − 59 7–39 Right TPJ Sagittal y = z = − 69 21 − 49 41 39 V1 Coronal x = z = − 10 − 4 10 16 17 Cuneus Coronal x = z = − 10 20 10 40 18–19
Foreachparticipant,horizontalandverticaltrialswere systemati-callycollapsed.Meanreactiontimes(RTs),accuracyratesandthe cor-respondingstandarddeviations(SDs) weremeasuredforeachof the fourbehavioralconditions(righttargetvalid– invalid,lefttargetvalid – invalid)acrossparticipants.TrialswithRTsexceeding±3SDsfromthe mean,ineachcondition,wereconsideredasoutliersandremovedfrom theanalyses.
MeanRTsandmeanpercentageofcorrectresponseswerethen en-teredintwoseparaterepeated-measuresanalysesofvariance(ANOVA) withcueside(right/left)andtargetside(right/left)aswithin-subject fac-tors.
2.5.2. Functionaldata
EROSanalysis:thedependentvariableforopticaldataanalyseswas changeinphasedelayfrombaseline,averagedforeachparticipantand condition.One-tailedtestswerecarriedoutonthevoxelwiththe max-imumdelayvalueineachROI,ateachlatency.Significantactivitywas foundifROIpeakZscoresreachedstatisticalsignificance(p<0.05), adjustedformultiplecomparisons(Kiebeletal.,1999;Worsleyetal., 1995).
Trialswithhorizontalandverticalgratingswerecollapsedandthree maincontrastswerechosenforstatisticalanalyses:all(validand in-valid)versusbaseline,validversusbaseline,andinvalidversus base-line.Inthefirstcontrast(allversusbaseline),inwhichlatenciesranging between−332msand0mswereconsidered,alltrialswerecollapsed togetherandcontrastedagainstbaseline(i.e.a200mstimewindow pre-cedingcueonset:from−1024to−819ms).Generally,sinceattentional deploymentprocessesbeginatabout200msaftercuepresentation,and ourcue-targetintervalwasvariablyrandomizedamongtrials(from300 to600ms),inourpre-targetanalysisweselectedthatspecifictime win-dowinorder tobe sureitwasenoughhomogenoustotheorienting response.Intheothertwocontrast(validversusbaselineandinvalid versusbaseline),inwhichfunctionalactivitywasobservedfrom0ms to767ms,validtrialsandinvalidtrialswerecontrastedagainst base-line(the200msprecedingthetargetonset),independentlyfromvisual hemifield.
Grangercausality:forwardGrangercausalityanalysiswascomputed inorder toexaminethepredictive relationshipamongactivationsin differentareasatdifferenttime-lags.Thisanalysisreliesonthe extrap-olationofameaningfulseedwithinanROIconsistingofatimewindow thatwillbecomparedtoanotherwindowofthesameduration. Specif-ically,thisapproachinvestigateswhethertheactivityoftheseedROI predictstheactivityintheotherROIsatalatertime-lag,onthebasisof thesimilarityindatashape.Inotherwords,usingtwodifferentlinear regressionmodels(therestrictedandtheunrestrictedmodel),Granger causalitycalculatestheimprovementinthepredictionofonebrain re-gion’ssignalresultsfromanothertemporallyearlierregion’ssignal. Im-portantly,thisisdoneattheindividuallevelallowingforvariabilityin timingbetweensubjectsandensuringtheidentificationofcomplex
pat-ternswhichmaynotbeevidentintheacross-participantsconventional EROSanalyses.Theresultingstatisticalmapsarethusbasedonthe av-erageofindividualvaluescalculatedseparatelyperROIandcontrast. Mapswerederivedfromcomputationoftstatisticsandtransformation intoz scores, runningthis procedureforeachlag. Then,acorrection formultiplecomparisonswasappliedwithineachROI,bymeansofthe samerandomfieldtheorytechniques(Worsleyetal.,1995;Kiebeletal., 1999)usedforEROSanalysis.PredictedROIactivitywasobservedin 15time-lagswhichcorrespondtothesametimepointsusedinEROS analyses.Startingfromlag0(correspondingto0ms)alltheotherlags weredividedby25.6ms,namelythesamplingrate,untilreachingthe lastlagwhichcorrespondsto358ms.Ifasignificantpredicted activa-tionataspecificlag(i.e.z-scoreexceededthecriterionvaluep<0.05) wasfound,onthebasisofthatlagandtheselectedseed,thepredicted andsubsequenttimewindowcontainingthepredictedROIpeak acti-vation,wasmeasured.Forvalidandinvalidversusbaselinecontrasts, theconsideredcriticaltimewindowstartedfromtargetonsetonwards, accordingtotheselectedseed.Astotheallversusbaselinecontrast,the timepointscomprisingthe400msbeforetargetonsetweretakeninto account.EventhoughwefirstlyfocalizedonlagsinlinewithourEROS results,wethencarriedoutexploratoryanalysestoprobeeffectsineach lagandROI.
3. Results
3.1. Behavioralresults
Therepeated-measureANOVAconductedonmeanRTsshoweda sig-nificantmaineffectoftargetside(F(1,17)=7.528,p<0.05,ƞp2=0.307),
withparticipantsfasterindiscriminatingthetargetontheright(514ms) thanontheleftsideofthescreen(522ms).Nosignificantdifferenceof cuesidewasfound(F(1,17)=1.163,p=0.296,ƞp2=0.064). Impor-tantly,theinteractionbetweencuesideandtargetsidewassignificant (F(1,17)=101.486,p<0.01,ƞp2=0.857).Tofurtherinvestigatethis
effect,apaired-samples(two-tailed)t-testwascarriedoutbycomparing meanRTsforvalid(499ms)andinvalidtrials(538ms).Thisanalysis reachedstatisticalsignificance(t(17)=−10.074,p<0.01)indicating thatthevalidconditionwasassociatedwithfasterRTs,thusshowingan attentionalorientingbenefitintargetdiscrimination(Fig.1B).
Therepeated-measure ANOVAon meanpercentageof correct re-sponsesshowedsignificantmaineffectsofbothcue(F(1,17)=9.435, p<0.01,ƞp2=0.357)andtarget (F(1,17)= 10.557,p<0.01,ƞp2=
0.383),indicatingthatparticipantsweremoreaccuratewhenthecue pointedtotheleftsideofthescreen(left98.6%,right98.2%)andthe targetwasontheright(left98.2%,right98.6%,),inlinewiththeresults observedintheRTsanalysis.However,theinteractionbetweencueand targetwasnotstatisticallysignificant(F(1,17)=1.077,p=0.314,ƞp2=
0.060).
3.2. Functionalresults 3.2.1. Orientingprocess
Toinvestigatethespatiotemporaldynamicsofattentionalorienting, weconductedtwoEROScontrasts:allversusbaseline(Fig.2A)andvalid versusbaseline(Fig.2B).Intheformer,wefoundasignificantlylarger activationwithintheselectedROIsfrom300mspriortotargetonset.In thelatter,wefoundgreateractivationsyieldedbyvalidtrialscompared tothebaselinecondition,inthetimewindowrangingfromtargetonset to767msposttarget.
Priortotargetonset:wefirstlookedattheallversusbaselinecontrast. Relativetobaseline,wefoundasignificantincreaseofactivationinV1 at204ms(z=2.88;zcrit=2.55)beforetargetonset(Fig.2A).This wasfollowedbysignificantactivityinlSPLatabout−180ms(z=2.35; zcrit=2.29),increasedactivityinrSPL(z=2.78;zcrit=2.76),lSPL (z=2.5;zcrit=2.38),andlIPS(z=2.53;zcrit=2.35)153msbefore targetonset,andfinallygreateractivitywasobservedinlSPLat−76
Fig.2. EROSorientingeffectsandGrangerresults.
(A)EROSorientingeffectsbeforethetargetonset.Significantstatisticalparametricmapsofthez-scoredifferencebetweenalltrialsandbaseline(correspondingto the200mstimewindowprecedingthecueonset)aredepicted(activationthresholdz-score=2.0uncorrected).Eachmaprepresentsa25.6msinterval,withinthe 384msprecedingtargetonset,inwhichsignificanteffectsoccurredinselectedROIs(greenboxes).ThewhitecrosswithineachROIshowsthepeakvoxel.(B)EROS orientingeffectsaftertargetonset.Significantstatisticalparametricmapsofthez-scoredifferencebetweenvalidtrialsandbaseline(correspondingtothe200ms precedingthetargetonset)aredepicted(activationthresholdz-score=2.0uncorrected).Eachmaprepresentsa25.6msintervalofthe767msaftertargetonset,in whichsignificanteffectsoccurredinselectedROIs(greenboxes).ThewhitecrosswithineachROIshowsthepeakvoxel.(C)Grangercausalityresultsonallversus baselinecontrast,(D)Grangercausalityresultsonvalidversusbaselinecontrast.FortheseanalysesalldorsalandvisualROIswerechosenasseedsatdifferenttime lags.Intheseschemes,eachcoloredboxcorrespondstoaspecificROI.Eacharrowindicatesasignificantpredictivelinkbetweenthestartingbox,representingthe seedROIataprecisetimelag,andthematchedbox,representingthepredictedROIatasubsequenttimelag(seeTable2).Thevaluesreportedonthetimelinerefer tothepeakactivitywithintheconsideredtimeintervalforeachROI.
(z=2.67;zcrit=2.39)and0ms(z=2.67;zcrit=2.42).See Supple-mentaryMaterial:Fig.2Afortimetracesofthemeanactivationofeach ROIinallversusbaselinecontrast.
After target onset: when valid trials were contrasted versus base-line,there wasanincreaseof activationinthedorsal portionofthe cuneusatboth128 (z =2.41;z crit =2.36)and281 ms(z =2.66; zcrit=2.25)aftertargetonset(Fig.2B).Subsequently,rIPSrevealed strongeractivationatalatencyof307ms(z=3.27;zcrit=2.62),while at332ms(z=2.46;zcrit=2.42)asignificantincreaseofactivation waselicitedinlSPL. Finally,greater cuneusactivitywasobserved at 358ms(z=2.5;zcrit=2.31).SeeSupplementaryMaterial:Fig.2Bfor timetracesofthemeanactivationofeachROIinvalidversusbaseline contrast.
Overall,these resultsarein keepingwith evidencethat orienting ofattentionengagesabilateraldorsalsystemalongwithvisualareas. Inthiscontrast,visualareasrevealamore sustainedactivitypattern comparedtothetimeintervalprecedingtargetonset,asitcanbeseen bygreater activationsincuneusatseveral timelags,which,indeed, donotsignificantlyemergeinthepreviousEROScontrastinvestigating activitypriortotargetonset.
Grangercausality-priortotargetonset:weperformedGranger causal-ityanalysestobetterunderstandthepredictiveinterplaybetweenareas. SinceGrangercausalityenablesustodetectalsosignificantactivity pat-ternsnotshownbytypicalEROSanalysis,weintegratedEROSdataby usingasseedsthoseROIswhichactivitywasfoundtobepredictedby activityinotherROIsusedasseedsinearliertimepoints.Inthis man-ner,wecouldhighlightthecascadeofpredictiveactivityamong neu-ralareasbyfollowingthedifferenttimingsoftheirengagement.With Grangercausalityonallversusbaselinecontrast,weassessedthe predic-tiveinteractionsovertimeinthecue-to-targetinterval.Resultsrevealed aconsistentcontinuousreciprocalpatternofpredictionbetweendorsal andvisualareas (Fig.2C). Specifically,activityinrIPS(peak activa-tion−384ms)waspredictiveofactivityinV1anddorsalcuneus(peak activation−204ms),whichinturnwaspredictiveofactivityin dor-salparietalareasincludinglSPL(peakactivation−179),lIPS,andrIPS (peakactivation−153).Thisstreamofpredictiveinfluencesterminates invisualareas(suchasV1andcuneus)andinlSPLinwhichpredicted orientingactivitycorrespondstoapeakat−51,−102and−76ms re-spectively(seeTable2forsignificantlagsandthecorrespondingtime windows).
Table2
Grangeranalyses– orientingresults.
Seed ROI Seed Interval (ms) Peak Activity (ms) Predicted ROI(s) (PR) PR Interval (ms) PR Peak Activity (ms) Sig. Lag Statistics Prior target onset
rIPS 512 - 332 384 V1 307 - 128 204 179 z = 3.14 z crit = 2.68 Cuneus 256 - 102 204 127 z = 2.49 z crit = 2.38 Cuneus 256 - 102 204 V1 307 - 128 204 25 z = 3.48 z crit = 2.65 lIPS 204 - 76 153 25 z = 2.72 z crit = 2.57 lSPL 153 - 25 76 25 z = 3.38 z crit = 2.56 V1 307 - 128 204 lSPL 179 25 z = 3.83 z crit = 2.55 rIPS 230 - 102 153 25 z = 3.02 z crit = 2.74 lIPS 204 - 76 153 V1 179 - 76 128 25 z = 2.88 z crit = 2.65 lSPL 153 - 25 76 25 z = 3.97 z crit = 2.69 rSPL 230 - 102 153 Cuneus 153 - 51 102 76 z = 2.90 z crit = 2.73 lSPL 153 - 25 76 25 z = 2.90 z crit = 2.58
rIPS 230 - 102 153 Cuneus 153 - 51 102 76 z = 2.90 z crit = 2.73
lSPL 153 - 25 76 25 z = 2.90 z crit = 2.58
V1 179 - 76 51 25 z = 3.12 z crit = 2.68
After target onset
rIPS 51 - 204 127 V1 230 - 358 281 76 z = 3.24 z crit = 3.11 Cuneus 25 - 179 127 lSPL 204 - 307 256 204 z = 3.24 z crit = 3.11 lSPL 281 - 384 332 230 z = 3.31 z crit = 3.19 Cuneus 204 - 332 281 lSPL 281 - 384 332 76 z = 3.27 z crit = 3.12 lIPS 409 - 537 486 230 z = 3.40 z crit = 3.01 rIPS 255 - 383 307 lSPL 281 - 384 332 25 z = 3.10 z crit = 3.02 lSPL 281 - 384 332 Cuneus 307 - 409 358 25 z = 4.22 z crit = 3.19
Grangercausality-aftertargetonset:Grangercausalityconductedon validversusbaselinecontrast(analyzingthetimewindowaftertarget onset)revealedasimilar recurrentactivationpatternin whichdorsal andvisualareasmutuallypredicteachother(Fig.2D).Inparticular, ear-lierintime,activityinrIPSandcuneus(peakactivation127ms)were predictiveofactivityinV1andlSPL(peakactivation256and281ms, respectively).Givenpeakactivationof281incuneus,thispredictspeak activationfirstlyinlSPL(at332mspost-targetonset),which,inturn, predictspeakactivationincuneus(at358mspost-targetonset),and sec-ondly,inlIPSatalaterlag(at486mspost-targetonset;seeTable2for significantlags,thecorrespondingtimewindows,andstatistics).
Overall,ourfindingssuggestaclearinvolvementofabilateraldorsal systemalongwithvisualareasinattentionalorienting.Specifically,our dataindicateatwo-waypredictiverelationshipamongdorsalandvisual areasactivations,mainlyinvolvingarecursivepredictiverelationship betweenrIPSandV1activationsinbothcontrasts,andbetweencuneus andlSPL,especiallyinthevalidversusbaselinecontrast.
3.2.2. Reorientingprocess
Toinvestigatethespatio-temporaldynamicsofattentional reorient-ing,wecontrastedinvalidtrialsversusbaseline,inwhichtheanalysis timeframerangedfromtargetonset(i.e.0ms)to767mspost-target.
Wefoundgreateractivityincuneusat102(z=2.83;zcrit=2.37) and128ms(z=2.78;zcrit=2.14),inbilateralIPSat204ms(lIPS: z=2.7;zcrit=2.46;rIPS:z=2.36;zcrit=2.13)andinV1at358ms (z=2.68;zcrit=2.65),aftertargetonset(Fig.3A).Moreover,rTPJ andthecuneusrevealedgreateractivityat409(z=2.81;zcrit=2.56) and435ms(z=3.2;zcrit=2.58).Wealsoobservedgreateractivityin rIPSat435(z=2.79;zcrit=2.73),486(z=2.57;zcrit=2.38),537 (z=2.6;zcrit=2.5),and563ms(z=2.9;zcrit=2.55).Finally,we foundsignificantactivityinrTPJactivationat588(z=2.8;zcrit=2.52) and767ms(z=2.64;zcrit=2.43)aftertargetonset.See Supplemen-taryMaterial:Fig.2C fortimetracesofthemeanactivationof each ROIininvalidversusbaselinecontrast.Thesefindingssuggestbilateral recruitmentofdorsalregionsinattentionalreorienting,togetherwith aninvolvementofrightventralandvisualareas.Giventhewell-known importanceattributedtorTPJinattentionalreorienting,wecarriedout anadditionalanalysisinwhichwedirectlycontrastedinvalidagainst validtrials,observingitsfunctionalactivityinthesametimewindow (0–767msposttarget).WefoundsignificantactivationinrTPJat409 (z=3.21;zcrit=2.47),435(z=3.42;zcrit=2.58),588(z=2.47;z
crit=2.4),742(z=2.7;zcrit=2.66)and767ms(z=2.59;zcrit=2.46), inlinewiththeactivationsfoundintheinvalidversusbaselinecontrast. WeusedGrangerCausalityanalysistostudythepredictive connec-tionsamongdorsal,ventralandvisualareas.Followingthesamelogic asthatadoptedforpreviousGrangercausalityanalyses,weselected dif-ferentrelevantseeds,whethersignificantlyactivatedinEROSanalysis, ornot.Datashowedananalogouspatternofpredictiontothatshown inorientingGrangercausality:visualareaspredictactivityindorsal ar-easandvice-versa.Specifically,aseedidentifiedincuneusatarange between51and179ms(peakactivation102ms),predictsactivityin rSPLcorrespondingtoapeakat409ms,whiledorsalregions,suchas lIPS,lSPL,andrIPS(peakactivation204ms)predictreorientingprocess incuneusattwolaterlagsinferringpeaksat307and409ms(Fig.3B). Themostimportantdifferencerespecttotheorientingcontrastsisthe comingintoplayofrTPJ,whichis,instead,absentinorienting process-ing.Indeed,severalseedareas(cuneus,lIPS,lSPL,rSPL,andV1)predict activityinrTPJwithapeakactivationat435ms,which,inturn, pre-dictsactivityinV1andlIPS,bothatthesamelaterlag(peakactivation 486ms;seeTable3forsignificantlags,thecorrespondingtimewindows andstatistics).
Taken together,thesefindings underline,for attentional reorient-ing,amutuallypredictiverelationshipbetweendorsalandvisualareas, whichoccursearlierinourtimewindow.Thislinkbetweendorsaland visualareasisfollowedbyaninvolvementofventralareas,specifically rTPJ,predictedbybothdorsalandvisualregions.
4. Discussion
This study aimed at uncovering thespatio-temporal dynamics of visuospatial attentional orienting and reorienting by means of non-invasiveopticalimagingi.e.atechniquethatcombinesagoodtemporal andspatiallocalizationability,thusrepresentinganidealtooltogather informationonthetime-courseofactivationsof localizedcortical ar-easduringspecificcognitivetasks.Additionally,inordertoassessthe predictiverelationshipsbetweenactivebrainareasatdistinctstagesof attentionalprocessing,weadoptedaGrangercausalityapproachthat enabledustoexplainthepredictiveinterplayamongdifferentregions bystatisticallypredictingdirectedattentionaleffectsofoneROIto an-other,subsequentintime.
Orientingandreorientingofattentionarethoughttobesubservedby distinctneuralsystemsconnectedtosensoryregionsandmainlysituated
Fig.3. ReorientingEROSeffectsandGrangerresults.
(A)EROSreorientingeffectafterthetargetonset.Significantstatisticalparametricmapsofthez-scoredifferencebetweeninvalidtrialsandbaseline(corresponding tothe200msprecedingthetargetonset)aredepicted(activationthresholdz-score=2.0uncorrected).Eachmaprepresentsa25.6msintervalofthe767msafter targetonset,inwhichsignificanteffectsoccurredinselectedROIs(greenboxes).ThewhitecrosswithineachROIshowsthepeakvoxel.(B)Grangercausalityresults oninvalidversusbaselinecontrast.Predictiveconnectionsamongdorsal,visualandventralROIsareillustrated.Again,eacharrowindicatesasignificantpredictive linkbetweenthestartingbox,representingtheseedROIataprecisetimelag,andthematchedbox,representingthepredictedROIatasubsequenttimelag(see
Table3).ThevaluesreportedonthetimelinerefertothepeakactivitywithintheconsideredtimeintervalforeachROI.
Table3
Grangeranalyses– reorientingresults.
Seed ROI Seed Interval (ms) Peak Activity (ms) Predicted ROI(s) (PR) PR Interval (ms) PR Peak Activity(ms) Sig. Lag Statistics
Cuneus 51 - 179 102 rSPL 332 - 486 409 255 z = 3.31 z crit = 3.13
rTPJ 358 - 511 435 255 z = 3.30 z crit = 3.25
lIPS 153 - 281 204 Cuneus 204 - 383 307 25 z = 3.19 z crit = 2.99
rTPJ 358 - 511 435 281 z = 3.27 z crit = 3.12
lSPL 153 - 281 204 Cuneus 204 - 383 307 25 z = 3.19 z crit = 2.99
rTPJ 358 - 511 435 281 z = 3.27 z crit = 3.12
rIPS 127 - 255 204 Cuneus 332 - 511 409 204 z = 3.74 z crit = 3.10
rIPS 307 - 486 409 255 z = 3.68 z crit = 3.09 lIPS 409 - 537 486 358 z = 3.33 z crit = 3.22 V1 230 - 435 358 Cuneus 332 - 511 409 25 z = 4.04 z crit = 2.95 rTPJ 358 - 511 435 25 z = 4.08 z crit = 3.03 rSPL 332 - 486 409 rTPJ 358 - 511 435 25 z = 3.87 z crit = 3.08 rTPJ 358 - 511 435 lIPS 409 - 537 486 51 z = 3.16 z crit = 3.11 V1 435 - 563 486 76 z = 3.22 z crit = 3.04
intheparietalcortex:abilateraldorsalandarightventralnetwork. Althoughthereisstrongevidenceabouttheinteractionbetweenthese systemsduringattentionaltasks(Shomstein,2012),acentralbutstill unresolvedquestionistofindouthowthisinteractionoccursandhow visualareasareinvolved.
4.1. Orienting
Inthepresentwork,attentionalendogenousorienting(i.e. volun-taryallocationof attention)wasinvestigatedbymeansoftwoEROS contrasts.Thefirst,inwhichalltrials(independentlyfromvalidity con-dition)werecomparedwithbaseline,wasintendedtomonitorthe tim-ingofactivationofspecificbrainareasduringdeploymentofattention betweencueonsetandtargetonset.Thesecond,inwhichacomparison betweenvalidtrialsandbaselinewasperformed,wasintendedtostudy thespatio-temporaldynamicsrelatedtovoluntaryattentionalorienting followingtargetonset.Resultsfromthetwoanalyseswerejointlytaken intoaccounttoachieveamoreexhaustivecomprehensionofthe orient-ingandreorientingprocesses.Ourfindingsarelargelycongruentwith theliterature(Chicaetal.,2011;Corbettaetal.,2008;Kincadeetal., 2005)byexhibitinganexclusiveinvolvementofbilateraldorsalregions inendogenousorienting.Theventralnetworkdidnotshowany signif-icantactivationinthisprocesswhilevisualareas(BA17,18,19)were activelyinvolved,especiallyaftertargetonset.Withrespecttothe ex-ploredcue-targetintervalwhichprovidesinsight intotheattentional engagementtothecuedspatiallocation,wefoundearlyactivationof V1followedbybilateraldorsalparietalactivation.Thesefindings sug-gestthattheattentionalengagementtothecuedlocationiscarriedout bybilateraldorsalregions,whichpre-activateV1beforethevisual tar-getappears.Neuralactivityisdetectedagaininbilateraldorsalregions andincuneusaftertargetonset.
Thecontributionsofdorsalparietalandvisualareasduring atten-tionalorientingcanbebetterexplainedbytheirpredictiveconnections. PreviousfMRI(Bressleretal.,2008;Lauritzenetal.,2009)andEROS experiments(Parksetal.,2015)havestudiedtheconnectivitybetween parietalandvisualregionsrevealingatop-downinfluencefromparietal (especiallyIPS)toearlyvisualareas duringsustained attention. Our Grangercausalityresults areinaccordancewiththese findings high-lightingsimilarpredictivepatterns.Specifically,wefoundarecurrent tendency,fordorsalandvisualareastointeractbothinthecue-target andinthepost-targetperiod,inwhich,startingfromrIPS,dorsaland visualregionsmutuallypredicteachother.Thus,thepresentevidence isinfavoroftheproposalofVosselandcolleagues(2012).Byapplying DynamicCausalModeling(DCM)tofMRIdatatheauthorssuggesteda reciprocalcausalinfluencefrombilateralIPStothecorresponding bi-lateralvisualareas.Inlinewiththistheoreticalaccountderivedfrom modeltesting,thecontinuousmutualpredictionbetweenrIPSandV1 isthemoreconsistenttrendemergingfromouranalyses.Interestingly, IPShasbeenshown(Jerdeetal.,2012)tocompriseprioritizedmaps ofspacewhichareorganizedinaretinaltopographicmanner,thus sug-gestingIPSasareliablecandidateinmaintainingattentioncovertly.Itis highlyplausiblethat,thankstothiscommonretinotopicorganizationof IPSandV1,thepredictivecommunicationbetweentheseareasandthe top-downinfluenceexertedbyIPSonV1couldbethoughtastheneural markersofsustaineddeploymentofattentiontowardapreviouslycued location.Moreover,theothertwoareas,lSPLandcuneus,havebeen foundtopredictoneanother’sactivityatdifferenttime-lagsaftertarget onset.Thisisinlinewithpreviousevidenceaboutthecriticalroleof cuneusinvisuospatialattentioncontrol(Doesburgetal.,2016), accord-ingtowhichthecuneusappearstobethetargetofatop-downattention informationflowderivingfromareasimplicatedintheorientingprocess (includingdorsalareas).
Therefore,we suggestthattwo mainflows ofinformation areat workduringthe orientingprocess: one,subserving theinterplay be-tweenIPSandV1codesattentionalorientinginaretinotopicmanner andanother,subservingtheinterplaybetweenSPLandthedorsal
por-tionofthecuneus(BA18and19)codesorientinginamorespatiotopic manner,toprovideinformationforthevisuo-motorbehaviorelicitedby thepresentationofthetarget.
Takentogether,ourresultssuggestapredictivepatternbetween dor-salandvisualregionsthatpersistsinboththeanalyzedfunctional con-trasts,substantiatingtheexistenceofadorsalandvisualnetwork in-volvedinthesupervisionandelaborationofdifferentprocessesof at-tentionalorienting.
4.2. Reorienting
Inthepresentexperiment,wealsoinvestigatedattentional endoge-nousreorienting,i.e.thecognitiveprocessbywhichspatialattention isredirectedtouncuedlocationwherebehaviorallyrelevanteventsare presented.Inordertoanalyzeandseparatetheneuraldynamics under-lyingattentionalendogenousreorientingweimplementedafunctional contrastinwhichinvalidtrialswerecomparedtothebaselineina post-targettimewindow.Ourresultsareinkeepingwithpriorstudies indi-catingarecruitmentofboththedorsalandventralattentionalnetworks (Capotostoetal.,2012;Doricchietal.,2010; Vosseletal., 2009)in conjunctionwithvisualareas.However,whilethereisrobustevidence foraninterplaybetweenthetwoattentionalsystemsin the reorient-ingprocess(Vosseletal.,2014),itremainsunclearhowtheyinterface witheachother.Inthecurrentstudy,weendeavoredtoshedlighton thisissuebyestimatingtheexacttimingofactivityinbrainareas pos-tulatedtobecriticalinattentionalreorienting.Moreover,wesoughtto understandthepredictiverolesoftheseareasdependingonthe differ-entreorientingsub-processes.Dorsalandvisualactivationduring atten-tionalreorientingappearstofollowapathalongvisual(BA17,18,19) anddorsalregions(bilateralIPS)whichshowsignificantactivationsin alternatingtimeintervals.Ventralactivityduringattentional reorient-ingshowedgreateractivityinrTPJoccurringatseveraltime-lags,quite laterintime.Thesefindingscouldbeexplainedbyreferringtodifferent functionsinendogenousreorienting:dorsalandvisualareasareengaged inearlierreorientingsub-processes(e.g.detectingamismatchbetween cuedandtargetlocation)whilerTPJisresponsibleforprocessesthat occurlaterintime,thusnotinvolvedintriggeringreorientingitself.
Toextenduponthefunctionalresults,weappliedGrangercausality toourEROSreorientinganalyses.Atfirstglance,wenoticedasimilar activitypatterncomparedtothatfoundwithEROS:earlyintime,visual (BA17,18,19)anddorsalregions(bilateralIPSandSPL)show signif-icantactivityalternatinginsubsequenttimewindows.Inaddition,the datasuggestafunctionallinksuchthatvisualanddorsal regions in-fluenceeachotherinapost-targettimewindowrangingbetween100 and400ms.Withrespecttothepredictiverelationshipwithactivity in rTPJ,almostallactivatedareas (withtheexceptionof rIPS)exert predictiveeffectsonrTPJ,whichitselfpredictsactivityinvisualand dorsalregions.Thesedataarepartiallyinlinewiththepreviouslycited fMRIstudybyVosselandcolleagues(2012).Forattentionalreorienting, theseauthors,bymeansofDCM,havereportedsignificantconnectivity fromvisualareastorTPJandfromrTPJtorIPS.Ontheonehand,we concurwithVosseletal’sresultsaboutthedisappearanceofthe recur-siverelationshipbetweenV1andrIPSfoundtobefundamentalinthe orientingprocessandthegeneraltrendofconnections.Ontheother, Vosselandcolleagues(2012)havenothighlightedanearlierfunctional linkbetweenvisualanddorsalregionsbuthaveproposedan interpre-tationoftheroleofrTPJnamely,toinformthedorsalnetworkofthe violatedtop-downexpectancy,whichdoesnotfitwithourresults.In theliterature,thereis astrongdebate onthepreciseroleplayedby rTPJwithregardtoitsinteractionwiththedorsalnetworkin endoge-nousattentionalreorienting.Anearlytheoryofhowthetwonetworks interactduringattentionalreorientingcomesfromCorbettaand Shul-man(2002)anddescribesrTPJasacircuitbreaker,interruptingthe ongoingselectioninthedorsalnetworkwhich,inturn,reorients atten-tiontotheunexpected,butrelevantinformation.Ifthatwerethecase, fast-latencysignalsfromtheventralnetworkshouldbesenttotheDAN
toreorientattention.However,thereislittleevidenceintheliterature offast-latencyresponsesintheVANprecedingresponsesfromtheDAN (Corbetta etal., 2008).Onthecontrary,duringattentional reorient-ingthesignalfromrTPJtendstoariselaterintimecomparedtothat ofdorsalregions(GengandVossel,2013).Importantly,rTPJismainly correlatedwiththeP3b,asub-componentoftheP300,which gener-allyoccursinalatepost-targettimewindow(300–500ms).Moreover, P3bisusuallyelicitedbyunexpected,butimportant,task-relatedevents, corroboratingtheproposedlinkbetweenP3bandrTPJ.Byextension, anotherfunctionalsignificancehasbeenascribedtoP3b,namelythat of“contextualupdating” (DonchinandColes,1998;Polich,2007). Ac-cordingtothistheory,rTPJshouldperformanupdatingoftheinternal modelofthecurrentenvironmentalcontextasafunctionofincoming novelandunexpectedinformation.Thisthesisfitswithevidenceabout rTPJactivityinPosnerattentionaltasksinwhichinvalidtargets(strictly connectedwithrTPJactivation),beingtypicallyinfrequentand unex-pected,yieldtheupdatingoftarget-responsepatternrelatedtothe like-lihoodofoccurringofthesubsequenttargets(GengandVossel,2013). Ourresultsareinfavorofthispost-perceptualinterpretationofrTPJ, rulingouttheideaoftheventralsystemasa“circuit-breaker” ora trig-gerofreorientingprocess.Infact,thefirstsignificantEROSactivationof rTPJduringattentionalreorientingwasfoundlaterintimethanvisual anddorsalactivations.Moreover,withGrangercausality,werealized thatallvisualanddorsalregionspredictrTPJ,likelycodingthe occur-renceofsomethingunexpected.Fromthesedata,itappearsthatthe pre-dictiveandmutualinterplaybetweenvisualanddorsalareasoccurring earlierintimecodesthemismatchbetweenexpectancyandrealityand, atthesametime,promotesthesubsequentdisengagementofattention fromthecuedlocationbytriggeringreorientationtotheunexpected tar-getlocation.rTPJ,predictedbyvisualanddorsalregions,doesnottake partinthisreorientingprocessbyemerginglaterintime.Rather,it initi-atesapost-perceptualevaluationoftargetinformationintegratingnovel informationwiththepreexistinginternalmodel.Thisinterpretationof theroleoftherTPJiscorroboratedbyevidenceshowingthatitis re-peatedlyactivatedatlatertimeframes.Actually,thelastsignificantrTPJ EROSactivationsoccurabout600msaftertargetonset,thus support-ingthecontextualupdatingtheory,andsuggestingthatrTPJterminates theupdatingprocessatthosetime-lagsbymodifyingfuturetask-related expectations.
5. Conclusions
Thenoveltyofthepresentpaperreliesonthemethodusedfor in-vestigatingthedynamicsunderlyingattentionalprocesses.The combi-nationofEROSandGrangercausalityallowedustounravelfunctional relationshipsamongspecificbrainareas,dependingontheirexact tim-ingofactivationintheprocessesofendogenousorientingand reorient-ing.Withrespecttoattentionalorienting,ourresultssuggestapredictive patterninvolvingdorsalandvisualregionsbothbeforeandaftertarget onset,suggestingtheexistenceofadorsalandvisualnetworkengagedin thesupervisionandmanipulationofthevariousorientingsub-processes. Astoreorienting,ourresultssupportamutualinteractionbetween vi-sualanddorsalareaswhich,afterencodingofthemismatchbetween expectationandreality,disengageattentionfromthecuedlocationby triggeringreorientationtotheunexpectedtarget.Incontrast,the ven-tralnetworkplays apost-perceptualroleinupdating thepreexisting internalmodelasafunctionofnovelincominginformationonthe unex-pectedtargetposition,promotingadjustmentsaboutfuturetask-related expectations.Inconclusion,ourfindingsrefineandextendtheexisting knowledgeoftheneuralbasesofattentionalprocesses.
Thepresentstudyislimitedbytheextentoftheinvestigatedareas: ourEROSmontages,becauseof thenumberof sourcesanddetectors atourdisposal,werenotsufficienttocoverthefrontalcortexnot per-mittingtoexaminetheactivityofFEFandVFC,whichareembedded inDANandVAN,respectively.Evidenceabouttheirrelevancein at-tentionalprocessesandtheirconnectiontoparietalregions,provides
furtherdetailsintheunderstandingoforientingandreorienting mech-anisms.Inparticular,FEFisgenerallyconsideredtocooperatewithIPS intransmittingtop-downmodulationtothevisualcortexduring atten-tionalorienting(Bressleretal.,2008;Vosseletal.,2012),althoughthe effectivedirectionofthiscooperationremainsunclear.Asforthe contri-butionoffrontalregionstoattentionalreorienting,rightMFGandright IFGemergetobeactivatedbyinvalidtrialsonly(Vosseletal.,2006). Moreover, imaging evidence, revealed spontaneous activity in right MFGlinkedtobothdorsalandventralregions,showingthepresence ofneuronalpopulationsrelatedtobothattentionalnetworks(Foxetal., 2006)andprovidingfurtherinputtoexplainthefunctionalinteraction betweensystemsunderlyingvisuospatialattention.
Future studiesshould thus try toextend EROSmontage tosuch frontalareasinordertoinvestigatetheirroleinbothorientingand re-orientingprocessesandtorevealtheirpossiblepredictiverolein trigger-ingorientingresponsestowardsotherareasalongthedorsalandventral networks,alsotakingintoaccountthepossibilitytocombineEROSand Grangercausalitywithotherneuroimagingtechniques(Tseetal.,2018; Xiaoetal.,2020).
DeclarationofCompetingInterest
Theauthorsdeclarethattheresearchwasconductedintheabsence ofanycommercialorfinancialconflictofinterest.
CRediTauthorshipcontributionstatement
Giorgia Parisi: Software, Formal analysis, Investigation, Writing -originaldraft.ChiaraMazzi:Conceptualization,Methodology, Soft-ware,Formalanalysis,Writing-review&editing,Project administra-tion.ElisabettaColombari:Software,Formalanalysis,Investigation, Writing-review&editing.AntonioM.Chiarelli:Software,Writing -review&editing.BrianA.Metzger:Conceptualization,Methodology, Software,Formalanalysis,Writing-review&editing.CarloA.Marzi: Conceptualization, Methodology, Writing - review & editing. Silvia Savazzi: Conceptualization,Methodology,Software,Formal analysis, Writing-review&editing,Supervision,Projectadministration. Funding
This study was supported by European Research Council (ERC) [Grantnumber339939"PerceptualAwareness"P.I.CAM].Thefunders hadno rolein thecollection,analysis,andinterpretationof data,in thewritingofthereportandinthedecisiontosubmitthearticlefor publication.
Supplementarymaterials
Supplementarymaterialassociatedwiththisarticlecanbefound,in theonlineversion,atdoi:10.1016/j.neuroimage.2020.117244. References
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