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Neuropsychologia49 (2011) 3648–3655

ContentslistsavailableatSciVerseScienceDirect

Neuropsychologia

jo u r n al h om ep a ge :w ww . e l s e v i e r . c o m / l o c a t e / n e u r o p s y c h o l o g i a

The

neural

basis

of

the

Enigma

illusion:

A

transcranial

magnetic

stimulation

study

Manuela

Ruzzoli

a,b,∗,1

, Simone

Gori

c,d,1

, Andrea

Pavan

e,1

, Cornelia

Pirulli

b

,

Carlo

A.

Marzi

a

,

Carlo

Miniussi

b,f

aDepartmentofNeurological,Neuropsychological,MorphologicalandMotorSciences,UniversityofVerona,Italy bCognitiveNeuroscienceSection,IRCCSSanGiovannidiDioFatebenefratelli,Brescia,Italy

cDepartmentofGeneralPsychology,UniversityofPadua,Italy

dDevelopmentalNeuropsychologyUnit,ScientificInstitute“E.Medea”,BosisioParini,Lecco,Italy eSISSA,CognitiveNeuroscienceSector,ViaBonomea265,34136Trieste,Italy

fDepartmentofBiomedicalSciencesandBiotechnologies,NationalInstituteofNeuroscience,UniversityofBrescia,Italy

a

r

t

i

c

l

e

i

n

f

o

Articlehistory:

Received26April2011

Receivedinrevisedform9September2011 Accepted10September2011

Available online 19 September 2011

Keywords:

Enigmafigure Motionillusion

Repetitivetranscranialmagnetic stimulation(rTMS)

V1 V5/MT

a

b

s

t

r

a

c

t

Theaimofthisstudywastotesttheroleofthevisualprimary(V1)andthemiddletemporalarea(V5/MT) intheillusorymotionperceptionevokedbytheEnigmafigure.TheEnigmafigureinducesavisualillusion thatischaracterizedbyapparentrotatorymotioninthepresenceofastaticfigure.Bymeansofrepetitive transcranialmagneticstimulation(rTMS)weshowthatV5/MTiscausallylinkedtotheillusoryperception ofmotion.WhenrTMSwasappliedbilaterallyoverV5/MTjustpriortopresentationoftheEnigmafigure, theperceptionofillusorymotionwasdisruptedforapproximately400msresultinginadelayedillusion onset.Incontrast,rTMSappliedoverV1didnothaveanyeffectontheillusoryperceptionofmotion.These resultsshowthatV5/MT,avisualcorticalareaassociatedwithrealmotionperception,isalsoimportant fortheperceptionofillusorymotion,whileV1appearsnottobefunctionallyinvolvedinillusorymotion perception.

© 2011 Elsevier Ltd. All rights reserved.

1. Introduction

Enigma,devisedbyLeviant(1981 – Palaisdela Découverte,

Paris)isafigurethatelicitsthespontaneousperceptionofrotary

motionintheabsenceofrealmotion.Theimageconsistsofablack

andwhiteraypatternwithnarrowlyspacedradiallines,ontowhich

threechromaticringsaresuperimposed(Fig.1).Thepresenceof

illusorymotionseenontheringssuggestedthename“TheEnigma”.

Theillusorymotionoftheannulialternatesbetweenclockwiseand

counter-clockwiserotation(Gori,Hamburger,&Spillmann,2006;

Leviant,1996).

Enigmaisa peculiarmotionillusionwhichmakesthisfigure

veryinterestingtostudy.Whilemostothermotionillusions

repre-sentamisperceptionofmotiondirection(Gori&Hamburger,2006;

Gori&Yazdanbakhsh,2008;Gori,Giora,&Stubbs, 2010; Pinna &Brelstaff, 2000; Wallach,1935; Yazdanbakhsh &Gori, 2008),

theillusorymotionintheEnigmafigureis presentunderstatic

viewingconditions;thatis,nomotionoftheobserverorofthe

∗ Correspondingauthorat:CognitiveNeuroscienceSection,IRCCSSanGiovanni diDioFatebenefratelli,viaPilastroni,4,25123Brescia,Italy.

E-mailaddress:manuela.ruzzoli@cognitiveneuroscience.it(M.Ruzzoli).

1 Equallycontributedauthors.

stimulus is necessary to perceive the illusory rotary motion.

Anothermotionillusion,theRotatingSnakes(KitaokaandAshida,

2003),elicitsmotionunderstaticviewingconditions,butitdoes

notshowmotionreversalsastheEnigmafiguredoes.Allofthese

characteristicsmaketheEnigmafigureaveryuniqueandintriguing

motionillusion.

Severalhypotheseshavebeenformulatedonthemechanisms

underlying the illusory motion induced by the Enigma figure.

Gregory(1993,1995)proposedanexplanationintermsof

fluctua-tionsintheeyeaccommodation(“huntingforaccommodation”)

and fixational eye movements (FEMs) (Gregory, 1994;

Mon-Williams&Wann,1996),suggestingthatthesefactorsmayaccount

forthe illusioninduction. Zeki,Watson, andFrackowiak(1993)

showedbymeansofpositronemissiontopography(PET)thatwhen

participantsperceivedillusorymotion,theregionalcerebralblood

flow (rCBF)increasedin thesame brainareas that wereactive

whenparticipantswerelookingataphysicallymovingstimulus

(V5/MT,anextrastriateareahighlyinvolvedinvisualmotion

pro-cessing(Born&Bradley,2005)andadjacentmotionareas,suchas

V3a,V3bandMST),suggestingthereforethattheillusorymotion

couldbemediatedbythesameneuronsasrealmotion.Moreover,

inaddition,duringtheillusorymotionobservation, theauthors

reportedrCBFincreasesinotherareasoutside thevisualcortex

(rightfrontaloperculumandrightanteriorcingulategyrus),which

0028-3932/$–seefrontmatter © 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.neuropsychologia.2011.09.020

(2)

Fig.1.TheEnigmafiguredrawnbyLeviant(1981).

are notusuallyactivatedwhenparticipantsare exposedtoreal

motion.Therefore,alsothesebrainregionscouldbecandidatesfor

mediatingperceptionoftheEnigmafigure.Basedontheseresults,

Zekietal.(1993)arguedthatthegenerationofillusorymotionmay

dependontheactivationoffrontalareasthatarenotactive

dur-ingexposuretorealmotion,thusexcludingretinalinfluencesinthe

illusionperception.Ontheotherhand,acomputationalmodel

con-sistentwithavailableneurobiologicalevidencewasproposedby

Fermuller,Pless,andAloimonos(1997)thatattemptstomakeboth

FEMsandcorticalactivationnecessaryfortheperceptionofmotion

inducedbytheEnigmafigure.Theirmodelproposesthateye

move-mentsarenecessarytotriggertheillusoryrotationintheEnigma

figurebutthathigh-levelcorticalprocessesaremainlyresponsible

fortheillusion.Recently,Hamburger(2007)andKumarandGlaser

(2006)claimedthattheillusorymotionintheEnigmafigureisnot

theresultofmotionoftheimageontheretinaduetomicrosaccades

but rather hasa strictly cortical origin.Gori et al. (2006)

pro-videddatasupportingthecorticalroleofthisillusoryphenomenon

withoutexcludingthepossibilitythatFEMswereinvolvedinthe

generationoftheillusion.Theseauthorshighlightaclear

regular-ityinthereversalsthatsuggeststhepresenceofaneuralsaturation

mechanismatthecorticallevel.Moreover,theyshowedhowreal

motioncaninfluenceillusorymotion,suggestingthatrealand

illu-sorymotioninteractatsomepointalongthemotion-processing

pathway. On the other hand,Troncoso, Macknik, Otero-Millan,

andMartinez-Conde(2008)convincinglydemonstratedthatsmall

eyemovementsareanecessaryconditiontoperceivetheillusory

motion.Theseauthorssetouttoresolvethelong-standingdebate

astowhethertheinitialneuralprocessesthatultimatelyleadtothe

perceptionoftheEnigmaillusionariseintheeyeorinthebrain.

Becausetheillusionwasfoundtobestronglydependentonsmall

eyemovements,theanswerseemstobethattheillusion

percep-tionstartsintheeye,ratherthaninthebrain,evenifthebrain

isnecessarilyinvolvedintheillusoryperception.Troncosoetal.

(2008)found,indeed,thattherateofmicrosaccadesincreasedjust

beforethereportedperceptionoffasterillusorymotion,compared

withadecrementintherateofmicrosaccadeswhenthe

partic-ipantsreportedslowerornoillusorymotionduringaprolonged

viewingoftheEnigmafigure.Therefore,althoughafull

explana-tionofhowtheillusionarisesisstillacontroversialtopic,itseems

reasonablethat,eventhoughtheFEMsprobablytriggerthe

illu-sion,thecortexplaysapivotalroleintheperceptionoftheillusory

motion.

V5/MTinvisualmotionprocessing(d’Alfonsoetal.,2002;Laycock

etal.,2007;Sacketal.,2006;Stevensetal.,2009):anearly

activa-tionbeginningapproximately60mspriortostimuluspresentation

andalatetemporalwindowofactivationbeginningapproximately

130÷150msafterstimuluspresentation(Stevensetal.,2009).In

thefirstexperimentofthepresentstudy,wevariedthetime

win-dowinwhich repetitiveTMS(rTMS)wasdeliveredoverV5/MT,

eitherbeforeoraftertheappearanceoftheEnigmafigureinorder

todefinethetemporalwindowinwhichperceptionoftheEnigma

illusioncouldbeaffected.Inthesecondandthirdexperiment,in

viewofthenumerousfeedforwardandfeedbackprojections

exist-ingbetweenV1andV5/MT(Born&Bradley,2005)weexploredthe

roleoftheV1cortexintheperceptionoftheillusion.

2. Experiment1:rTMSoverV5/MT

2.1. Materialsandmethods 2.1.1. Participants

Sixteennaïvehealthyparticipants(sevenmales,20÷28yearsold),tookpartin theexperimentaspaidvolunteers.Allofthemhadnormalorcorrectedtonormal visualacuity.Noneofthemhadneurological,psychiatricorotherrelevant medi-calproblemsoranycontraindicationtorTMS(Rossietal.,2009).Allparticipants gaveinformedconsentandtheexperimentalprotocolwasapprovedbytheEthics CommitteeofIRCCSSanGiovannidiDio,Fatebenefratelli,Brescia,Italy.

2.2. Stimuliandapparatus

Stimuliweredisplayedona19-inchmonitorwitharefreshrate

of60HzthatwasgeneratedwithMatlabPsychtoolbox(Brainard,

1997; Pelli,1997). Thescreen resolution was1024×768.Each

pixelsubtended∼1.9arcmin.ThegrayscaleEnigmaillusionused

byHamburger(seeFig.2AinHamburger,2007)servedasstimulus

(Fig.2A).Asacontrolstimulus(Fig.2B),thesameversionofthe

Enigmafigurewasused,exceptthattheradiallineswerereplaced

byablackhomogeneousbackground(seeFig.2Iin Hamburger,

2007). According toHamburger (2007), this stimulus does not

induceillusory motion. Both Enigmaand controlfigures had a

Michelsoncontrastof98%.Thefiguressubtended15.4×18.3◦ of

visualangleand were presentedat thecenter of thescreen. A

blackcentralfixationpoint(0.22◦)overlappedwiththecenterof

thefigures.

2.3. TMSprotocol

TMS was applied simultaneously and bilaterally over

V5/MT using two Magstim Super Rapid Magnetic Stimulators

(50Hz—biphasic, four boosters) and two figure-of-eight coils

(custom double 50mm; Magstim Company Limited, Whitland,

(3)

Fig.2. (A)Theexperimentalstimulus(Enigmafigure).(B)Thecontrolstimulus.

positions of severalreference points (e.g., Cz,Oz, O1, O2 from

theInternational10/20EEGsystem)werereproduced.Individual

targetarealocations weredetermined bya functionalmethod,

i.e.,searchingthepositionsforwhichreliablemovingphosphenes

wereinducedbyasingleTMSpulseappliedwithcoilspositioned

onbothhemispheres.Thisprocedurewasperformedstartingfrom

5cmlateraland3cmabovetheinion.Theseareasweremarked

onthecapastheparticipant’sstimulationsitesforthestudy.The

meancoil positionfor left V5/MTstimulation wasidentified at

5.28cm (±0.33) lateralto theinionand 3.57cm (±0.88) above

the inion. The mean coil position for right V5/MT stimulation

wasidentifiedat4.87cm(±0.45)lateraltotheinionand3.30cm

(±0.66)abovetheinion;weplacedthejunctionofthetwocoil

wingsabovetheselocations.Thecoilwaspositionedtangentially

withrespect tothe scalp. The control conditionwas an active

stimulationoverthevertex(Cz,fromtheInternational10/20EEG

system), a location that corresponds to thecaudal part of the

frontalcortex,thatis,abrainareathatisnotinvolvedinvisual

processing. During the experiment, the stimulating coils were

fixed by two articulated mechanical holding arms (Manfrotto

Magicarmswithtwoclampseach)andtwoheavy-dutytripods.

Thepulseintensitywasfixedforalltheparticipantsat50%ofthe

outputofthestimulatorsforbothcoils.DuringtheTMSsessions,

sevenTMSpulsesweredeliveredata frequencyof15Hz.These

parametersareconsistentwithsafetyrecommendationsforrTMS

(Rossietal.,2009).

Weplannedtwoperiodsofstimulationwithinthetargetareas.

InoneTMScondition,thepulsesweredischargedduringfixation,

i.e.,from−400to0msbeforetheappearanceoftheEnigma

fig-ure(conditionTMS-before).Inanothercondition(TMS-during),the

pulsesweredischargedfrom0to400msafterstimulusonset.

TheorderofthefourTMSconditions(TMS-before,TMS-during

bytwolocationsMT/V5and Cz)wasrandomizedacross

partic-ipants. The interval betweenone condition and theother was

approximately 10minutes, during which the participants were

askedtoansweraquestionnaire(Fertonani,Rosini,Cotelli,Rossini,

&Miniussi,2010)aboutpossiblediscomfortsinducedbyTMSin

theprecedingcondition.

2.4. Procedure

Theparticipantswereseated57cm awayfromthescreen.A

chinrestwasusedtostabilizethehead.Theyfirstfamiliarized

themselveswiththestimuliandwiththescalelevelsforranking

thestrengthoftheillusion.Subsequently,theyperformeda

train-ingblocktopracticethetask.Eachtrialstartedwithapuretone

of500ms.Afixationpointthenappearedandlasteduntiltheend

ofthetrial.Theparticipantswereinstructedtomaintaintheir

fix-ationatthecenterofthescreen.Theywererequiredtopressthe

spacebaronakeyboardassoonastheyperceivedthemotion

illu-sion(Gorietal.,2006).Ifnoresponsewasprovided,thestimulus

automaticallydisappearedafterfiveseconds.Afterresponse,the

participantswereaskedtorankthestrengthoftheillusionona

five-levelscale(Kumar&Glaser,2006)bypressingoneoftheindicated

buttons(0=noillusoryperception,1=weakperception,2=average

perception,3=clearperception,and4=vividperception).The

fol-lowingtrialstartedtensecondsaftertheresponserelatedtothe

strengthoftheillusorymotionwasgiven.

Afterthefirsttrainingblock,inwhichparticipantsperformed

thetaskwithoutanystimulation(i.e.,No-TMScondition),the

tar-getareas(bilateralV5/MTandCzconditions)wereidentified(as

previouslydescribed)andmarkedontheskullcap.Thepositionsof

thecoilsweremonitoredbytheexperimentersduringtask

execu-tion.Eachexperimentalblockconsistedof40trials.Thirtyofthese

consistedofEnigmafiguredisplays,whereastheremainingten

tri-alsconsistedofcontrolstimulusdisplays(catchtrials),asshownin

Fig.2B.

2.5. Results

Theresultsofthereactiontimes(RTs)areshown inFig.3A.

Becausethecatchtrialsneverproducedillusorymotion,the

anal-yseswereconductedexclusivelyonthetrialsinwhichtheEnigma

figurewasdisplayed.Apaired-sample t-testdidnotrevealany

significantdifference betweenthe two Cz TMS conditions (i.e.,

CzTMS-beforevs. CzTMS-during)(t7=−0.69, p=0.52).For this

reason, in the other analysis, we considered the Cz TMS

con-ditions as a single control condition (i.e., with no distinction

betweenCzTMS-beforeandCzTMS-during).ThemeanRTswere

as follows: No-TMS condition,2.50s (SE:0.24); Cz TMS

condi-tion,2.52s(SE: 0.25); V5/MT TMS-before condition,2.93s (SE:

0.25);andV5/MTTMS-duringcondition,2.46s(SE:0.25).A

one-wayrepeated-measuresanalysesofvariance(ANOVA)performed

on the RTs and considering the following conditions—Cz TMS,

V5/MTTMS-beforeandV5/MTTMS-during—revealedasignificant

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Fig.3.(A)ResultsofExperiment1.RTsareplottedasafunctionoftheTMScondition.WhenrTMSwasdeliveredoverV5/MT-beforetheappearanceofthestimulus,theRTs weresignificantlylongerwithrespecttotheCzTMSconditionandV5/MT-duringTMScondition.(B)ThestrengthoftheillusionisplottedasafunctionoftheTMScondition. rTMSoverV5/MT-beforethestimulusappearanceslightlyreducedtheperceivedstrengthoftheillusionwhencomparedwiththeCzTMSconditionbutthedifferencewas notsignificant.Errorbarsindicatestandarderrors.

Pairwisecomparisons(Bonferronicorrected)revealedasignificant

differencebetweentheV5/MTTMS-beforeconditionand theCz

TMScondition(t15=3.83,p=0.004)andbetweentheV5/MT

TMS-beforeconditionandtheV5/MTTMS-duringcondition(t15=3.56,

p=0.008).In summary,theRTs weredelayedbyapproximately

400mswhenTMSwasappliedbilaterallyoverV5/MTbeforethe

appearanceoftheEnigmafigure,comparedwithbothCzTMSand

V5/MTTMS-duringconditions.

Fig.3Bshowstheresultsoftheperceivedstrengthofthe

illu-sion.Apaired-samplet-testdidnotrevealanysignificantdifference

betweenCzTMS-beforeandCzTMS-during(t7=−0.54,p=0.60).As

forRTs,weconsideredtheCzTMSconditionsasasinglecontrol

condition.Inordertoprovideaparallelwiththeresultsobtained

with theRTs,we conducted a seriesof t-tests(Bonferroni

cor-rected)consideringtheCzTMSandV5/MTTMS-beforeconditions.

Paired-samplet-testsrevealedanon-significanteffectbetweenthe

V5/MTTMS-beforeconditionandtheCzTMScondition(t15=−1.55,

p=0.14).Alltheotherpaired-samplet-testsdidnotreachthe

sig-nificancelevel.

Theresultsofthediscomfortquestionnaireshowedthatcoil

pressureandnoisewerethemostdisturbingeffectswithno

dif-ferenceforthelocationofthecoil(V5/MTorCz).

3. Experiment2:rTMSoverV1

Inthepreviousexperiment,wefoundthatTMSapplied

bilat-erally overV5/MTfrom−400msto0msbeforetheappearance

oftheEnigmafiguredelayedthetimenecessarytoreliably

per-ceivetheillusorymotion.Someauthors(Laycocketal.,2007;Sack

etal.,2006;Stevensetal.,2009)foundthatthedisruptionprofile

ofV5/MTTMSforglobalmotionperceptionconsistsoftwo

dis-tinctepochs(i.e.,anearlyactivationandalateractivation)during

whichglobaldirectionjudgmentsareimpaired.Whilethelate

acti-vationdoesnotappearcontroversial,differentexplanationshave

beenproposedtoexplaintheroleoftheearlyactivation.Sacketal.

(2006)referredtoitasaTMS-inducedartifact,suggestingthe

possi-bilitythatTMSmightinduceeyeblink,asalsoreportedbyCorthout,

HallettandCowey(2003).Onthecontrary,Laycocketal.(2007)

proposedtwoalternativehypotheses.Inparticular,they

hypothe-sizedthatTMScoulddisruptmotionprocessingdirectlythroughan

antidromicinterferencewiththelateralgeniculatenucleusofthe

thalamus(LGN)(deLabraetal.,2007),bypassingcorticalactivation.

Alternatively,theyhypothesizedthatthedeficitinmotion

percep-tioninducedbyV5/MTTMSpriortostimulusappearancemightbe

aconsequenceofadisruptedattentionalmechanismor

expecta-tion(Laycocketal.,2007).Finally,Stevensetal.(2009)suggested

afeed–forward–feedbackmodelinwhichtheearlyimpairmentof

performanceissupposedtobeduetoanindirect(backward)effect

ofTMSonV1.

Inthelightofthesecontroversies,inthisexperiment,we

inves-tigatedwhetherV1 isinvolvedin theperceptionoftheEnigma

illusionandwhetherthereisatemporalwindowofactivationthat

iscomplementarytothatofV5/MT.

3.1. Materialsandmethods

Thesameparticipantsfromthepreviousexperimentparticipatedinthesecond experimentafteratleastonemonthhadpassed.Thestimuli,apparatusand proce-duresofthesecondexperimentwerethesameasinthefirstexperiment,withthe exceptionofthestimulationsite,whichchangedfromV5/MTtoV1.

3.2. TMSprotocol

TMSwasappliedoverV1usingaMagstimSuperRapidMagnetic

Stimulatorand one figure-of-eight coil (customdouble 70mm;

MagstimCompanyLimited,Whitland,UK).Becausethemagnetic

fieldsfromtwocoilsinteractwithoneanotherifthecoilsareplaced

tooclosetogether,wedecidedtouseasinglebiggercoil,insteadof

two50mmcoils,aswasdoneinthepreviousexperiment.Before

theexperiment,individualtargetarealocationsweredetermined

bysearchingthepositionatwhichreliablestaticphospheneswere

inducedbyasingleTMSpulse.Thisprocedurewasperformed

start-ingfrom1cmabovetheinionandmovingslightlyinalldirections.

Thetargetareawasmarkedonthecapastheparticipant’s

stimula-tionsiteforthestudy.ThemeancoilpositionforV1stimulation

wasidentified at2.15cm (±0.55)abovetheinion. Alltheother

conditionswerethesameasinExperiment1.

3.3. Results

Fig.4AshowstheRTresultsforExperiment2.Becausewetested

thesame participantsof Experiment1, we usedthe datafrom

thesamecontrolconditions(No-TMSandCz-TMS)oftheprevious

experiment.InExperiment2,themeanRTfortheV1TMS-before

(5)

Fig.4.(A)ResultsofExperiment2.MeanRTsforeachTMScondition.NoeffectoftheTMSconditionwasobserved.(B)Thestrengthoftheillusionisplottedasafunctionof theTMScondition.rTMSoverV1didnotreducetheperceivedstrengthoftheillusionwithrespecttotheCzTMScondition.Errorbarsindicatestandarderrors.

was2.62s(SE:0.25).Aone-wayrepeated-measuresANOVA

con-sideringthefollowingconditions—CzTMS,V1TMS-beforeandV1

TMS-during—didnotrevealanysignificanteffectoftheTMS

con-dition(F2,30=0.13,p=0.87,2=0.009).Fig.4Bshowstheresultsof

theperceivedstrengthoftheillusion.AsinExperiment1,we

con-ductedat-test(Bonferronicorrected)consideringtheCzTMSand

V1TMS-beforeconditions.Apaired-samplet-testrevealedno

sta-tisticaldifferencebetweentheV1TMS-beforeconditionandthe

CzTMScondition(t15=1.3,p=0.20).Alloftheotherpaired-sample

t-testsperformeddidnotreachthesignificancelevel.

Theresultsofthediscomfortquestionnaireshowedthatcoil

pressureandnoisewerethemostdisturbingeffectswithno

dif-ferenceamongcoillocations(i.e.,V1,CzorV5/MTofExperiment

1).

4. Experiment3:rTMSoverV1withsmallerstimuli

InthepreviousexperimentwefoundthatrTMSappliedoverV1

didnotdelaytheperceptionoftheillusorymotionincomparison

totheCzTMScondition.However,itcouldbepossiblethatthe

stimuluswastoolargetobeaffectedbyrTMS(asitcoveredan

areaof15.4×18.3◦).Thatis,rTMSoverV1mayhavenotaffected

asufficientportionofV1tointerferewiththewholeextentofthe

stimulus.Inordertocontrolforthispossibilityweperformedan

additionalexperimenthalvingthesizeofthestimuli.

4.1. Materialsandmethods 4.1.1. Participants

Anewsampleofsixnaïvehealthyparticipants(threemales,25÷37yearsold), participatedintheexperimentaspaidvolunteers.Theyallmetthesamecriteriaas theparticipantsofthepreviousexperiments.

4.2. Stimuli,apparatus,TMSprotocolandprocedure

Thestimuliwerethesameofthepreviousexperimentsbutthe

figuressubtended7.7×9.15◦ofvisualangle.Thestimulisizewas

chosenbasedonthesmalleststimulusstillconveyingavivid

illu-soryeffect.Apparatus,TMSprotocolandprocedurewerethesame

ofExperiment2.

4.3. Results

Fig.5AshowstheRTresultsforExperiment3:meanRTforthe

V1TMS-beforeconditionwas2.20s(SE:0.23),fortheV1

TMS-duringconditionwas2.18s(SE:0.24)andforCz(averagedbetween

beforeandduring)conditionwas2.64(SE:0.22).TheCzTMS

con-ditionshowedthelargestdelayfortheillusorymotiononset:there

wasnodisruptiveeffectduetorTMSonV1.Aone-way

repeated-measuresANOVAconsideringthefollowingconditions–CzTMS,

V1TMS-beforeandV1TMS-during– revealedasignificanteffectof

TMS(F2,10=5.38,p=0.026,2=0.52).Howevernoneofthe

paired-samplet-tests(Bonferronicorrected)reachedthesignificancelevel.

Fig.5Bshowstheresultsoftheperceivedstrengthofthe

illu-sion.AsinExperiment1and2,weconductedat-test(Bonferroni

corrected)consideringtheCzTMSandV1TMS-beforeconditions.

Apaired-samplet-testrevealednostatisticaldifferencebetween

theV1TMS-beforeconditionandtheCzTMScondition(t5=0.63,

p=0.9).Alloftheotherpaired-samplet-testsperformeddidnot

reachthesignificancelevel.

Theresultsof thediscomfort questionnaireshowedthat coil

pressureandnoisewerethemostdisturbingeffectswithno

dif-ferenceamongthelocationsofthecoil(i.e.,V1,CzorV5/MTofthe

Experiment1).

5. Discussion

Inthepresentstudy,weaimedatassessingaselectivecortical

involvementintheperceptionoftheEnigmaillusionbyapplying

rTMSovervisualareasV1andV5/MT.TheresultsshowedthatrTMS

deliveredoverV5/MTbeforetheonsetoftheEnigmafigure

dis-ruptedtheillusorymotionperceptionforapproximately400ms,

comparedwiththeconditioninwhich rTMSwasappliedatthe

onsetoftheEnigmafigureorwhenrTMSwasdeliveredoverCz.In

addition,wefoundthatrTMSappliedoverV5/MTbeforethe

stim-ulusonsetslightly reducedtheperceivedillusorystrength with

respecttotheCzTMScondition,eventhoughthatdifferencedid

notreachsignificancelevel.Thus,itseemsthatV5/MTisdirectly

involvedintheperceptionoftheEnigmaillusion.Thisresultis

con-sistentwithpreviousfindingsreportedbyZekietal.(1993)who,

usingPET,foundanactivationofV5/MTandrightfrontalregions

duringthepresentationoftheillusion.WhileZekietal.(1993)

pro-posedthattheillusorymotionarisesanewinthebrain,weretain

thattheperceivedmotionistriggeredbytheFEMs(Troncosoetal.,

2008)butthesameareathatprocessestherealmotion(V5/MT)is

alsocrucialfortheillusorymotionoftheEnigmafigure.

On theotherhand,we foundnoeffect ofrTMS onthe

per-ceptionoftheillusionwhenitwasappliedoverV1,regardlessof

stimulationtimewindowandstimulussize.ThelackofanyrTMS

(6)

Fig.5. (A)ResultsofExperiment3.MeanRTsforeachTMScondition.rTMSoverV1didnotdelaytheillusorymotiononsetwithrespecttotheCzTMScondition.(B)The strengthoftheillusionisplottedasafunctionoftheTMScondition.rTMSoverV1didnotreducetheperceivedstrengthoftheillusionwithrespecttotheCzTMScondition. Errorbarsindicatestandarderrors.

inprocessingtheillusorymotioninductedbytheEnigmafigure.

However,inprinciple,ourresultscannotruleoutaV1

involve-mentintheEnigmaillusion.ApossibleinvolvementofV1inthe

early motionprocessingis suggested by physiological evidence

(Maunsell&vanEssen,1983;Movshon&Newsome,1996;Pack, Conway,Born,&Livingstone,2006)showingthatneuronsinarea

V5/MTaretunedforthedirectionofstimulusmotion,primarilyas

aconsequenceofastrongprojectionfromdirection-selectiveV1

neurons.However,V1direction-selectiveneuronsarethoughtto

sensethemotionoflocalcontours,whileV5/MTneuronsintegrate

this localmotioninformationtoextract globalmotion(Mather,

2011). It could bepossible that the illusory motion of Enigma

depends mainlyonhighlevelofmotionprocessing wherelocal

motionsignalsareintegratedtoextractglobalmotion(i.e.,V5/MT).

Inthiscase,rTMSwouldinterferewiththeillusorymotiononly

whendeliveredovertheextrastriateareaV5/MT.

Analternativeexplanationaboutthelackoftheeffectwhen

stimulating V1 couldbe that Enigma elicits a rotatory illusory

motion. Electrophysiological, human neuroimaging and

psy-chophysical studieshave shown that complex moving patterns

likeradialmovingpatterns(i.e.,contracting/expanding),spiraland

rotationalmovingpatternsareselectivelyprocessedbyhigh-level

visualareassuchasV5/MTandMST(Morroneetal.,2000;Smith,

Wall, Williams, &Singh, 2006;Wall, Lingnau,Ashida, &Smith,

2008).Theseauthors,usingfMRI,foundthatthecorticalareasthat

respondtocomplexmotionandtranslationalmotionwereclearly

distinctwithintheconfinesoftheMT+complex.Thus,itislikely

thatEnigmaelicitsakindofillusorymotionthatisselectively

pro-cessedbyhigh-levelvisualareas.

However,inprincipleonecouldarguethatrTMSisnotableto

selectivelyaffectthemotiondirection-selectiveV1neuronsorat

leastthatitisnotaffectingthemuptoalevelthatproducesa

per-ceptualeffect.Basedonthatpossibilitywecanonlysafelyclaim

that,withourexperimentalsetting,V1seemsnottobeinvolvedin

theillusorymotionperceptionevocatedbyEnigmaandthata

dif-ferentapproachmightbemoreeffective.Thisisforfurtherstudies

toascertain.

Furthermore,inthepresentstudy,a potentialconfoundthat

could lead toa differencebetween theeffect of stimulation of

V5/MT and V1 is the useoftwo coils for theV5/MT condition

andone,bigger,coilfortheV1condition.PotentiallytheV5/MT

condition couldbemore distracting and uncomfortable for the

participants.However,theresultsofthediscomfortquestionnaire

showednodifferencesamongthecoillocations(V5/MT,V1orCZ).

Mostimportantly,ifthedelayobservedintheV5/MT-before

con-ditionwithrespecttotheV1TMSandtheCzTMSconditionswas

merelyduetothediscomfort givenbythetwo coils,thiseffect

shouldbepresentalsointheV5/MTTMS-duringandnotonlyin

theV5/MTTMS-beforecondition,butthiswasnotthecase.Thus,

thispotentialconfoundseemstoberuledout.

Anothercharacteristicofthisstudythatisimportantto

high-lightistheuseofdifferenttimewindowsofrTMS.Theabsenceof

therTMSeffectduringtheEnigmaobservationwasanunexpected

resultthatcouldleadtofuturestudiestoabetterunderstanding

ofthephenomenon.Basedonourresultsitseemsthatthe

pre-activationofV5/MTismoreimportantthantheactivationduring

theEnigmaobservation,atleastforthespecifictaskandstimulus

weemployed.TheactivationofV5/MTduringtheEnigma

observa-tioncouldbemorerelevantinsessionswithlongerexposuretime,

i.e.,whensomespontaneousreversalsarepresent.

Ourresultsshowthatthecriticalperiodofactivationwasbefore

theappearanceofthefigure.Laycocketal.(2007)suggestedthat

TMSdeliveredprior tothestimulusappearance mighthave an

effectby interfering withthesubject’sexpectation or withthe

attentionalprocessing.Moreover,theearlyV5/MTTMSdisruptive

effecthasbeenlinkedtoanindirectnoise inductionintheLGN

(Laycocketal.,2007)orinV1(Stevensetal.,2009)throughfeedback

connectionfromV5/MT.AnotherexplanationcouldbethatTMS

induceseyeblinkingwhenappliedbeforethestimulusappearance

(Corthoutetal.,2003;Sacketal.,2006).However,ifTMSincreased

theRTtoperceivetheillusioninourparticipantsbecauseofeye

blinks,onewouldhaveexpectedastrongeroratleastasimilar

effectwhenstimulatingacorticalareadifferentfromV5/MT(e.g.,

V1inourexperiment).Furthermore,Stevensetal.(2009)directly

addressedthepossibilitythatTMSinduceseyeblinksby

stimulat-ingtheprimarymotorcortexwhiletheparticipantswereengaged

inamotion–directiondiscriminationtaskandconcurrently

record-ingtheeyeblinksthroughavideocameraintwoparticipants.Their

resultsclearlyrefutedtheeyeblinkhypothesis.Itseemslikelythat

theperformanceimpairmentintheearlyperiodofV5/MT

stimula-tionmightbeexplainedbyaninterferingmechanismviafeedback

connectionsfromV5/MTtoV1(Stevensetal.,2009).Incontrastto

thispossibility,inthepresentstudyrTMSoverV1didnotyielda

delayintheperceptionofillusorymotion.

AnotherpossibleexplanationfortheRTdelayfoundwhen

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brainoscillationsplayinvisualperception(i.e.,alpha-band)and

thepossibilityofentrainingaparticularoscillationfrequencyby

brainstimulation(Thut&Miniussi,2009).Romeietal.(2008)found

thatthe restingalpha-band (8–15Hz) powerover the

parietal-occipitalcortexisinverselycorrelatedtotheperceptualoutcomeof

asingle-pulseTMStoinducephosphenes.Moreover,Romei,Gross,

andThut(2010)showedthatshorttrainsofrTMSatalpha

fre-quencyoverthevisualareascausallydeterminedtheperceptual

outcomeofforthcomingstimulusdetection.Inthepresentstudy

weusedastimulationfrequencyof15Hzwhichcanbeconsidered

tobewithintherangeofthealpha-band.Onepossibilityisthat

TMSdeliveredatthistemporalfrequencybeforetheappearance

oftheEnigmafiguremight“entrain”thebrainoscillationwithin

thealpha-band,leadingtoanimpairmentoftheperceptionofthe

illusoryrotatorymotion.However,theroleofbrainoscillationsin

illusoryvisualmotionprocessingwasoutofthescopeofthepresent

studyandfurtherTMS/EEGorMEGstudiesarenecessarytocast

lightonthispoint.

6. Conclusions

Eventhoughfixationeyemovementscanprobablytriggerthe

Enigma illusion(Gregory, 1994; Mon-Williams& Wann, 1996;

Troncosoetal.,2008),clearlycorticalactivityplaysacrucialrole

intheperceptionof illusorymotionevoked bytheEnigma

fig-ure.Ourresultsareinagreementwiththehypothesissuggested

byTroncosoetal.(2008)thatFEMswouldtriggerneural

process-inginmotion-sensitiveareasofthebrain.V5/MT,anareathatis

normallyassociatedwiththeperceptionofrealmotion,appears

tobeimportantalsofortheperceptionofillusorymotion,while

V1doesnotappear tobecausallyinvolved.Theseresultsinvite

futurestudiesaimedatunderstandingwhetherandwhereillusory

andrealmotionsdifferintheircorticalprocessingpathwaysthus

contributingtosolveanotheraspectofthepuzzlenamedEnigma.

Disclosurestatement

Noneoftheauthorshasanypersonalorinstitutionalconflictof

interest.

Thispaperisnotunderconsiderationbyanyotherjournaland

ithasnotpreviouslypublished.

Theprotocolhasreceivedprior approval bythe appropriate

Ethicscommitteeandinformedconsentwasobtainedfromeach

subject.

Allco-authorshaveagreedwiththecontentsofthemanuscript.

Acknowledgement

ThisresearchworkwassupportedbytheItalian Ministryof

UniversityandResearchandbytheMinistryofHealth.

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