Somatosensory extinction for meaningful objects in a patient with right hemispheric stroke

\PERGAMON Neuropsychologia 26 "0888# 222Ð232

S9917Ð2821:88:, ! see front matter Þ 0888 Elsevier Science Ltd[ All rights reservedPII] S 9 9 1 7 Ð 2 8 2 1 " 8 7 # 9 9 9 6 6 Ð 2

Somatosensory extinction for meaningful objects in a patient withright hemispheric stroke

Anna Bertia\�\ Susan Oxburyb\ John Oxburyb\ Paola A}annic\ Carlo Umiltaa\Laura Orlandia

a Dipartimento di Psicolo`ia Generale\ Universita| di Padova\ Via Venezia 7\ 24020 Padova\ Italyb Department of Neurolo`y\ The Radcliffe In_rmary\ University of Oxford\ UK

c Centro Medico Sociale Don Gnocchi\ Parma

Received 6 December 0886^ accepted 7 June 0887

Abstract

Implicit\ high level processing of extinguished objects has often been described in the visual modality[ In the tactile domain\however\ research on this topic is meagre and it is still uncertain whether processing of tactually presented stimuli can be a}ected bythe same attentional disorders as visual stimuli[ In this paper we describe a patient\ ENM\ with visual neglect and light touchextinction who\ in a naming task of objects presented in the tactile modality\ simultaneously to both hands\ showed extinction forleft hand objects[ He was\ nevertheless\ able to make above chance Same:Di}erent judgements on the two stimuli[ We also testedtwo neurologically intact subjects who performed the test wearing a ski!glove on the left hand to impair the recognition of left handobjects[ In these subjects\ Same:Di}erent judgements were at chance level when recognition rate was as low as that found in patientENM[ This happened when either the objects\ although sharing the same name were di}erent in shape "conditions SameÐDi}erent#or when the two objects were di}erent with respect to the category name but were actually physically similar "conditions Di}erentÐSimilar#[ However\ when the objects were either identical or completely di}erent\ i[e[\ in a condition where judgement could be basedsimply on the physical analysis of the object shape "condition SameÐIdentical and Di}erentÐDissimilar#\ their Same:Di}erentjudgements were above chance\ despite the tactual de_cit[ Our conclusion was that patient ENM showed implicit recognition of lefthand objects\ at least in the SameÐDi}erent and in the Di}erentÐSimilar conditions\ whereas\ in the same conditions\ normal subjectswith an arti_cial sensory impairment did not[ Our results also show that Same:Di}erent judgements may be\ in some conditions\less demanding than naming tasks\ as suggested by Farah et al[

Furthermore\ patient ENM performed the test both with uncrossed and crossed hands[ We found that extinction always a}ectedthe hand controlateral to the brain damage\ although there was a tendency for a decrement of the ipsilesional hand performance inthe crossed condition[ We discuss these _ndings with reference to the most recent theories on the existence of a body centered spatialframe of reference[ Þ 0888 Elsevier Science Ltd[ All rights reserved[

Keywords] Tactile extinction^ Visual extinction^ Implicit processing^ Brain damage patient

0[ Introduction

Extinction is a relative frequent neurological symptom\often associated with right parietal damage ð2Ł[ Althoughit has been described in di}erent modalities "auditory\olfactive\ visual and tactile# visual and tactile extinctionsare the most known forms in clinical practise[ Patientswith visual extinction can detect a stimulus when pre!sented in isolation\ but fail to report contralesional stim!uli when two stimuli are simultaneously presented\ onein each hemi_eld[ Some patients report having brief visual

� Corresponding author[ Tel[] 9928 38 716 5490^ fax] 9928 38 7165599^ e!mail] ambertiÝpsico[unipd[it

experience "e[g[\ they say they can perceive a light# butare not aware of the identity of the stimulus "e[g[\ ð1\3\ 10Ł#[ Similarly\ tactile "or somatosensory# extinctionpatients report single light touch stimulation deliveredto one side of the body\ but fail to detect light touchstimulation on contralesional body parts when anotherstimulus is simultaneously delivered to ipsilesional bodyparts[ Sometimes\ although perceiving that something ispresented to the contralesional hand\ they are not able tojudge the quality aspect of the sensation ð05Ł[ In thedomain of active tactile sensation "haptic stimulation#\patients can be aware that something is presented to thecontralesional hand and can explore with active move!ments the stimulus\ but are not aware of the identity of

A[ Berti et al[:Neuropsycholo`ia 26 "0888# 222Ð232223

the stimulus ð01Ł[ Although tactile extinction is phen!omenically similar to\ and frequently associated with\visual extinction ð19Ł\ most of the knowledge on thisphenomenon has been derived from experiments carriedout in the visual domain[

For a number of reasons\ visual extinction is con!sidered to be the result of an attentional de_cit[ Thenormal detection of single stimuli presented contralateralto the lesion shows that the lack of detection of thecontralesional visual events in double stimulation trialscannot be simply ascribed to hemianoptic de_cits[Indeed\ the capacity of reporting single stimuli presentedcontralaterally to a brain damage has always been relatedto the presence of intact somatosensory areas devoted torelatively low!level information processing[ Other data\such as the di.culty in disengaging from ipsilesionalstimuli once attention has been drawn to them or theamelioration of the detection of contralesional stimuliwhen the patient is instructed to ignore the ipsilesionalstimuli ð3Ł and the modulation of extinction by stimuluscharacteristics ð03Ł\ have been taken as evidence of anattentional disorder being the cause of the symptom[ Ithas also been shown that extinction patients\ althoughnot aware of the identity of the extinguished stimulus\are able to make high level judgement when indirectmeasures of processing are used ð10\ 1Ł[ This phenomenonhas been interpreted as a high!order awareness de_cit\which implies intact low!level perceptual processes[

Visual extinction has usually been studied using simpleand brie~y presented visual events[ Therefore\ it has beenmainly characterized as a 1D phenomenon\ a}ectingeither meaningless visual event ð02Ł\ letters ð3Ł\ brie~ypresented line!drawings of meaningful objects ð10Ł orreproduction "photographs# of real objects ð1Ł[ It is stilluncertain whether extinction can a}ect awareness ofhigher and more complex object representations\ such asthose derived from processing of real 2D meaningfulobjects or\ on the contrary\ whether extinguished infor!mation can enter awareness once 2D object rep!resentation is triggered[ Mattingley\ Davis\ and Driverð03Ł have recently shown that\ when bilateral stimuli for!med a common surface "like in Kanizsa _gures#\ or whenthe task required completion of a partially occluded_gure\ within a 2D illusory framework\ extinction sig!ni_cantly diminishes[ In other words\ if a coherent objectis present in the _eld or if a 2D representation is activatedthrough a perceptual illusion\ this would be su.cient forvisual information to bypass the extinction problem andto reach awareness[ As Mattingley et al[ ð03Ł haveobserved\ pre!attentive processes must be carried out nor!mally for the patient to give a correct answer when anobject is present and to show extinction when only mean!ingless stimuli are present[ But\ if extinction takes placeafter pre!attentive processes are completed and a}ectsnon!object construct\ does this mean that extinctionalways spares 2D objects recognition< In other words\ is

it intrinsic to the nature of extinction not to involveperception of real 2D objects< The Mattingley et al[|s ð03Ł_ndings showed that extinction can be overcome in aparticular condition in which pre!attentive grouping pro!cesses derive\ from multiple bilateral meaningless visualevents\ the presence of a single object[ However\ it is stillunknown whether extinction can a}ect real tri!dimensional objects when objects are presented as twoseparate sensory events[

Very recently\ Maravita ð01Ł described\ in the som!atosensory domain\ extinction for the dimension and rec!ognition of 2D geometric shapes[ A patient with lighttouch extinction was unable to say which of two di}erentspheres placed simultaneously in the two hands was thebigger[ Sometimes he was not even able to say that theleft hand object was a sphere[ To our knowledge\ nostudy has so far reported a thorough investigation ofsomatosensory extinction for real 2D man!made objects[The _rst aim of this paper is\ therefore\ to investigateextinction of 2D meaningful objects in the somatosensorymodality\ where the identi_cation of meaningful objectsstrictly depends on the reconstruction of their 2D shape[

Another point of interest is whether extinction is codedin terms of retinotopic:somatotopic or spatiotopic framesof reference[ In the visual domain\ there is evidence thatseems to suggest that extinction is not coded reti!notopically[ For instance\ visual extinction can beobserved even when two visual stimuli are presented inthe right ipsilesional visual _eld\ e[g[\ ð3Ł[ In this case\ theextinguished stimulus is always the {more contralesional|of the two\ which is not only presented in the neuro!logically intact visual _eld\ but also\ in retinotopic terms\nearer to the fovea than the normally detected stimulus[This phenomenon cannot be explained within a reti!notopic frame of reference\ because the brain damage"ipsilesional to the tested _eld# does not a}ect the part ofthe retina responsible for the perception of the sector ofvisual _eld in which the extinguished stimulus ispresented[ It seems\ instead\ that visual extinction isdetermined within a spatiotopic frame of reference[ Inthe somatosensory domain\ Smania and Aglioti ð06Ł haveshown that\ in right brain damage patients a}ected bysomatosensory extinction\ light touch stimuli deliveredto the contralesional hand in a condition of double!sim!ultaneous stimulation\ were detected with lower accuracywhen the hand was in the anatomic position\ i[e[\ in itshomonymous hemispace\ than when the hand wascrossed in the heteronomous hemispace[ Because pro!cessing of information in primary somatosensory areasshould not be in~uenced by the spatial position of thehand\ these results have been interpreted as suggesting ahemispatial component in determining extinction[ Theopposite result\ i[e[\ lower accuracy of the contralateralhand in detecting light touch stimuli\ both when the handwas in the homonymous hemispace and when it was inthe heteronomous hemispace\ would have been inter!

A[ Berti et al[:Neuropsycholo`ia 26 "0888# 222Ð232 224

preted by Smania and Aglioti as evidence of a som!atotopic component in the extinction de_cit[ Whethersomatosensory extinction may manifest itself in a spa!tiotopic frame of reference or in a somatotopic frameof reference when 2D objects are to be perceived andrecognized\ has never been previously investigated[

In this paper we describe a patient who\ after a righthemispheric stroke\ developed left hemispatial neglectand left light touch extinction on double!simultaneousstimulation[ In order to investigate "0# whether extinctionmay a}ect 2D object representation and "1# the nature ofthe frame of reference in which extinction manifests itselfin the somatosensory domain\ we designed an experimentin which the patient had to make di}erent kinds of judge!ments on bilaterally presented 2D meaningful objects[The objects had to be manipulated with the hands placedin either the anatomical:homonymous hemi!space or inthe crossed:heteronomous hemi!space[ Our experimentaldesign allowed us to study in detail the characteristics ofthe patient|s somatosensory extinction phenomenon[ Wealso studied\ with the same design\ two neurologicallyintact subjects in order to clarify some aspects of thepatient|s performance[

1[ Experiment 0

1[0[ Materials and methods

1[0[0[ Case historyENM was a 58 year!old right handed man who\ after

an episode of vertigo and decreasing of visus\ was admit!ted to the hospital[ On examination\ he was found tohave high blood pressure\ to be alert and cooperativewith no signi_cant neurological alterations[ On the dayafter the admission his conditions worsened\ he becameconfused and disoriented in time and space and\ onneurological examination\ a mild left hemiparesis wasobserved[ No mention of objective visual impairmentcould be found in the hospital notes[ A CT scan showeda hypodense lesion in the right occipito!parietal lobeswith mass e}ect of the omolateral ventricle and somelacunar lesion due to small ischemic damage in thesemioval center[0

Two months later he was admitted to Don GnocchiRehabilitation Center in Parma where he was tested[ Hisneurological status was then improved[ He was coop!erative and oriented in space and time[ The left upperlimb motor capacity was back to normal\ while a mildmotor disorder was still a}ecting the lower limb[ Visual_eld was di.cult to assess clinically because of the pres!

0 The localization of the brain damage is based on the radiologyreport found in the patient|s notes[ Unfortunately\ we did not havedirect access to the CT scan _lms and\ therefore\ we could not recon!struct the patient|s lesion[

ence of a severe left visual neglect "see below#[ He had nomajor sensory disorder\ but light touch extinction wasobserved on each session[

1[0[1[ Materials and designWe used 45 objects belonging to 35 categories of man!

made common objects "by {category| we mean the nameof a group of objects sharing similar functional charac!teristics\ e[g[\ the category of pens^ within a categoryobject share the name but not necessarily the physicalshape#[ Stimuli were real objects whose dimensions weresuch that they could be easily manipulated by thesubjects[ Considering the major axis of each object\ thesmallest object was a bottle cap and its major axis mea!sured 1 cm\ whereas the biggest object was a knife!_leand its major axis measured 14 cm[

In a single session of the experiment\ two di}erentkinds of trial were employed] single!stimulation trials anddouble!stimulation trials[ There were 05 single stimu!lation trials "7 for the right and 7 for the left hand# inwhich 05 of the 35 categories of objects were used "seebelow#[

The other 29 categories of objects were presented on39 double!stimulation trials\ in which two objects wereplaced simultaneously one into the right and one into theleft hand[ For 09 of these 29 categories\ we used twoobjects di}erent in shape\ but with the same name[ There!fore\ a total of 39 objects were used in the double!stimu!lation trials[ An object presented in a trial could also bepresented in another trial with the constraint that it couldnot be presented more than twice\ either to the same orto di}erent hands[ Most objects\ however\ were presentedonly once[ Therefore\ the possibility of overlearning wasvery remote[ Double!stimulation trials were of two kinds]the two objects presented to the hands could have thesame name "Same Condition trials# or could have di}er!ent name "Di}erent Condition trials#[ There were 19Same Condition trials and 19 Di}erent Condition trials[On half of the Same Condition trials "09 trials# the twoobjects placed into the left and the right hand were exactlythe same "i[e[\ they had both the same name and thesame shape#[ This condition was named SameÐIdenticalcondition "SI Condition#[ In the other half of the SameCondition trials "09 trials# the two simultaneously pre!sented objects still shared the name of the category butwere di}erent in shape[ This condition was named SameÐDi}erent condition "SD Condition# "see Fig[ 0#[

Turning to the Di}erent Condition trials\ on half ofthese trials "09 trials# the two objects\ although belongingto di}erent name categories\ had very similar shapes[This condition was named Di}erentÐSimilar condition"DS Condition#[ In the other half of the Di}erent Con!dition trials "09 trials# the objects not only had di}erentnames\ but were also completely di}erent in shape"Di}erentÐDissimilar Condition\ DD#[


Fig[ 0[ Experimental condition] 0a � Same Identical "SI# condition^0b � Same Di}erent "SD# condition^ 0c � Di}erent Similar "DS# con!dition^ 0d � Di}erent Dissimilar "DD# condition[

1[0[2[ ProcedurePatient ENM was tested on four di}erent days in a

week[ On each day\ he performed one session[ The _rstsession and the last session began with the Albert ð0Ł test[After the Albert test\ light touch sensation and visualrecognition of objects "see below# were assessed[ Lighttouch sensation was tested using a randomized sequenceof stimulation\ in which 7 double!simultaneous stimuli\and 05 single stimuli "7 to the right and 7 to the left# weredelivered to the patient|s hands[

The other sessions began with the visual presentationof the 39 objects\ which were to be used in the double!stimulation trials[ The patient was seated upright at atable[ Each object was placed on the table immediatelyto the right of the patient|s trunk midline\ at approxi!mately 49 cm from the patient|s eyes[ The patient wasasked to look at the objects\ but not to touch them\ andto name the objects[ He was allowed 19 s for inspectionand naming[ If he could not name or recognize an object\the experimenter would tell him the name of the object[These trials were designed to assess the patient|s fam!iliarity with the objects and his naming capability[ Afterthis visual recognition test\ 05 single!stimulation tactiletrials\ 7 with the object presented to the right hand and 7with the object presented to the left hand\ in a randomizedsequence\ followed[ The patient\ again seated upright atthe table\ was blindfolded\ the hands were placed on thetable with the palm upright\ each hand being on its natu!ral side "uncrossed position#[ He was asked to name theobject and was allowed to manipulate it for a maximumof 19 s or until he could give the name of the object[There was no repetition of objects within these trials andthe objects used for the single stimulation trials were notused in the subsequent conditions[

Single stimulation trials were followed by 3 blocks ofdouble!stimulation trials\ in the uncrossed position[ Ineach block 4 SameÐCondition and 4 Di}erentÐConditiontrials were run in a randomized order\ for a total of09 double!stimulation trials[ In each block the SameÐCondition and the Di}erent Condition trials all belongedto the same type\ so that we had one block with SI trialsintermingled with DD trials\ one block with SD trialsand DD trials\ one block with SI and DS trials\ and oneblock with SD and DS trials[ As already mentioned\a single session comprised 39 double!stimulation trials[Again the patient\ blindfolded\ was asked to judgewhether the two objects had the Same or Di}erent name"Same:Di}erent judgement# and then to name bothobjects[ Before giving the answer\ the patient was allowedto manipulate the objects for a maximum of 19 s[ Muchstress was put on the fact that\ on double!stimulationtrials\ the manipulation of the objects had to be madesimultaneously with both hands to avoid that a double!stimulation trial could turn into a single!stimulation trial[ENM was not given any feedback on his performance[

Finally\ 05 single!stimulation trials and 3 blocks of


double!stimulation trials\ identical to the ones justdescribed\ were run with crossed hands\ so that the righthand manipulated the object to the left of the patient|strunk midline and the left hand manipulated the objectto the right[ In the crossed condition\ we swapped theposition of the objects so that the objects that in theuncrossed conditions were presented to the left hand werenow presented to the right hand and vice versa[ Thecrossed condition was run twice[

In summary\ patient ENM performed altogether on 53single!stimulation trials and 059 double!stimulation trialsin the uncrossed condition and on 21 single!stimulationtrials and 79 double!stimulation trials in the crossed con!dition[

1[0[3[ PredictionsPatient ENM showed light touch extinction "see

below#[If the presence of light touch extinction compromises

high level somatosensory processing\ we would expect to_nd a recognition problem for a single object placed inthe hand contralateral to the brain damage\ that is thehand a}ected by the extinction de_cit[

If\ however\ tactile extinction compromises highersomatosensory processing only when the system is over!loaded\ we would expect to _nd recognition problemsonly with simultaneous presentation of two objects\ onein the right and one in the left hand[ According to Smaniaand Aglioti ð06Ł\ the possibility that the recognition de_citis related to low level sensory processes\ and thereforecoded in somatotopic coordinates\ would be supportedif the de_cit always a}ected the contralesional hand[ Thatis to say\ in either the crossed or uncrossed condition theextinguishing hand should always be the left[ On thecontrary\ if extinction is related to the space where themanipulation is performed\ i[e[\ coded in spatiotopiccoordinates\ then both hands should manifest the extinc!tion phenomenon when placed in the space\ left to thetrunk midline\ contralateral to the brain damage[ That isto say\ the extinguishing hand should be the left in theuncrossed condition and the right in the crossedcondition[

If the patient showing extinction for recognition ofmeaningful objects was nevertheless able to make accu!rate same!di}erent judgements on the objects sim!ultaneously presented to both hands\ the level at whichthe judgement is made can be inferred as follows[ If thejudgement is based on a relatively low level object shaperepresentation\ correct Same judgements should be foundonly in the SI Condition[ Similarly\ accurate Di}erentjudgements should be found only in the DD Condition[If\ on the other hand\ accurate Same!Di}erent judge!ments are based on a categorical level of representation\correct Same judgements should be found also in the SDCondition and correct Di}erent judgements should befound also in the DS Condition "Also see ð1Ł#[

1[1[ Results

ENM showed a severe neglect in the Albert ð0Ł test "onevery occasion he was tested he crossed only the right!most lines# and a clear!cut tactile extinction[ Indeed\ henever reported the left light touch stimulus when it wassimultaneously presented with another one on the righthand\ although being able to detect single stimuli deliv!ered to the right and left hand[

ENM|s naming performance in the visual modalitywas fairly good[ He misnamed only _ve objects out of39[ The name of these objects were\ then\ given to thesubject and he was also asked to repeat them aloud beforethe execution of the tactile experiment[

In the tactile condition of the experiment "see Table 0#\he again performed pretty well in the naming per!formance of single!stimulation trials\ both in theuncrossed and crossed condition\ where there was nosigni_cant di}erence between the naming performance ofthe right and left hand ð67 vs 70)\ uncrossed "P�9[49by Fischer|s exact test# and 70 vs 76) crossed "P�9[49by Fischer|s exact test#Ł[

Table 1 shows the results of double!stimulation trials[It is worth noting that naming performance should beassessed in the Di}erent Condition ð10\ 1Ł\ because\ aftera Same judgement\ it followed that both objects had thesame name "the patient typically said {same [ [ [ watch|#[Di}erent Conditions were\ therefore\ the most signi_cantto establish the presence of tactile extinction for object

Table 0ENM|s naming in single stimulation trial

Trials LH RH")# ")#

Uncrossed 14:21 15:21"67# "70#

Crossed 02:05 03:05"70# "76#

LH � left hand^ RH � right hand[

Table 1ENM|s accuracy for same:di}erent judgements overall and for namingin di}erent trials on double!stimulation

Trials S:D LH RH")# ")# ")#

Uncrossed 015:059 13:79 63:79"68# "29# "82#

Crossed 47:79 04:39 16:39"62# "27# "56#

S:D � Same:Di}erent judgements^ LH � left hand^ RH � right hand[


naming "the patient typically said {di}erent [ [ [ pen on theright\ knife on the left| in the correct response or {pen onthe right [ [ [ left I do not know| in the wrong response#[ENM|s naming performance on the Di}erent trials of theuncrossed conditions was fairly good when we considerthe right hand "82) correct#\ but was impaired for theleft hand "29)# and the di}erence between the two handswas signi_cant ðChi ð0Ł�69[30\ P³ 9[990Ł[ Errors werealways omissions[ In other words he always said {left [ [ [ Ido not know what it is|[ He was not even able to describethe general shape of the object and when asked to saywhat the object was for he could not give any answer[ Thesame was true when we consider naming in the crossedcondition[ As already mentioned\ there was no di}erencein the naming performance of the right and left hand onsingle!stimulation trials[ However\ left naming per!formance was signi_cantly worse "27)# than right nam!ing performance "56)# on double!stimulation trials ðChið0Ł�6[10\ P³ 9[90Ł[ Based on these data\ we might con!clude that ENM showed extinction for naming of objectsplaced in his left hand1\ whatever position in the extra!personal space "right or left of the trunk midline# wasoccupied by the left hand[ In fact\ although the left handwas always the worst\ the right hand performance wors!ened in the crossed condition compared to the uncrossedcondition "56 correct vs 82) correct^ Chi ð0Ł�01[40\P³ 9[90#[

These data also show that ENM performed themanipulation correctly on the double stimulation trials\i[e[\ simultaneously with both hands\ otherwise we wouldnot have observed the di}erence in performance betweenthe two hands[

Despite the patient|s poor naming performance in theDi}erent Condition\ his Same:Di}erent judgements wereabove chance on both uncrossed ð68) correct\ Chið0Ł�17[7\ P³ 9[9990Ł and crossed trials ð62) correct\Chi ð0Ł�7[4\ P³ 9[994Ł[ In addition\ Same:Di}erentjudgements were above chance also if we consider eachcondition separately\ on the uncrossed trials "SI P³ 9[90\SD P³ 9[94\ DD P³ 9[990\ DS P³ 9[94\ see Table 2#[On the crossed trials\ only SD condition did not di}erfrom chance[ In all other conditions\ ENM gave Same!Di}erent judgements above chance level "P³ 9[94 ineach condition#[

1 We did not compare the performance for the left!hand object alonewith identi_cation of the same object on the left in bilateral trialsbecause the objects in the single trials and in the double stimulationtrials were di}erent[ This is because we wanted to avoid the possibilityof over!learning[ However\ although the categories of the stimuli weredi}erent in the single and double stimulation trials\ the type of stimuluswas the same "real man!made objects# and this is what is generally usedin these kind of extinction studies "see ð1\ 10Ł#[ If some other factors\ notrelated to the extinction phenomena\ but related to the characteristics ofthe stimuli\ had in~uenced naming performance in double stimulationtrials\ we should also have found an increase of naming errors for theright!hand objects[

Table 2ENM|s accuracy for same:di}erent judgements in the various con!ditions

Trials SI SD DD DS")# ")# ")# ")#

Uncrossed 21:39 17:39 27:39 29:39"79# "69# "84# "64#

Crossed 04:19 00:19 06:19 04:19"64# "44# "74# "64#

SI � same identical^ SD � same di}erent^ DD � di}erent dissimilar^DS � di}erent similar[

1[2[ Discussion

From these results we can conclude that in the tactiledomain "as in the visual domain#\ accurate Same:Di}erent judgements can be achieved even when the pati!ent does not always know what object he is manipulatingwith the left hand[ A possible interpretation of the resultsis that\ although the patient is not able to recognize theleft hand stimulus\ extinguished objects are\ nonetheless\processed at a high level[ Volpe et al[ ð10Ł and Berti et al[ð1Ł argued that extinguished stimuli were not lost by thevisual system\ but they were processed\ unconsciously\up to a high level[

A criticism to such conclusions was advanced byFarah\ Monheit and Marcie ð5Ł[ They proposed thatextinguished stimuli are\ in fact\ poorly processed[According to them\ even poor perception can be su.cientto account for a dissociation between Same:Di}erenttasks and identi_cation tasks\ because the Same:Di}erentcomparison would be less demanding than object identi!_cation[ The crucial experiment carried out by Farah etal[ ð5Ł to support their claim was performed on normalsubjects[ Subjects were asked to perform both a Same!:Di}erent task and an identi_cation task\ in a conditionof double!simultaneous visual stimulation[ Left visual_eld stimuli were perceptually degraded[ The resultsshowed that normal subjects identi_ed correctly 86) ofright stimuli\ but only 44) of left stimuli "note that inthis case 44) is not chance level\ because the namingtask implied the choice between many di}erent visualstimuli#[ Nonetheless\ in the Same:Di}erent task theyperformed correctly on 79) of trials[ Therefore\ theauthors| conclusion was that they had replicated theVolpe et al[|s ð1Ł results\ simply by degrading the leftstimulus[

There are two points that deserve a comment[ First\most extinction patients have a more severe recognitionproblem than that caused by the degradation used byFarah et al[ ð5Ł[ For instance\ two patients in Volpe etal[|s ð10Ł study had an identi_cation rate of 9)\ and inthe Berti et al[|s ð1Ł study\ when stimulus presentation


was very short "09Ð04 m#\ patient ENM identi_ed only18) of left stimuli\ but still had a Same:Di}erent per!formance at 67) correct[ This means that not only witha recognition rate of 44) "as in the Farah et al[ study\ð5Ł#\ but even with very low recognition rate\ extinctionpatients can still give correct answers in the Same!:Di}erent task[ Second\ sometimes Same:Di}erentjudgements are not easier than naming "for instance whenthe judgement is required on two objects very similarin shape\ but with di}erent names#[ In this case\ evenrecognition can be a}ected "see below#[ Therefore\ inorder to replicate in normal subjects the _ndingsdescribed in extinction patients\ we should degrade theleft stimulus so much as to obtain the same recognitionrate as that observed in the patients[ If\ by so doing\ thedissociation persisted\ then the hypothesis that the twotasks simply di}er for the amount of information necess!ary to perform them\ would be more convincing[ On thecontrary\ if normal subjects with a left hand recognitionrate of 18) performed at chance in the Same:Di}erenttask\ this would show that\ below a certain level of degra!dation\ information is not enough even for the Same!:Di}erent judgement[ Thus\ the dissociation we _nd inpatients can be reasonably ascribed to intact\ or quasi!intact\ unconscious:pre!attentive processes[

2[ Experiment 1

In order to disentangle these two possibilities\ we car!ried out the same experiment performed by ENM in twonormal subjects "GVB and GB#\ matched for sex\ age\and educational level with the patient[

2[0[ Materials and methods

2[0[0[ ProcedureMethod and procedure were the same as reported

above for the double!simultaneous stimulation trials ofExperiment 0[ The crucial di}erence was that\ in orderto create a recognition problem in the tactile domain\ weasked the subjects to wear on the left hand a ski glovethat decreased the perceptual performance of the lefthand[ The ski glove was a leather _ve!_ngers glove\approximately 9[7 cm thick\ that allowed active explo!ration of the object\ although limiting it compared to themanipulation with the hand without the glove[ Sensoryperception was also grossly impaired by the use of theglove because both subjects could not detect any singlelight touch stimulus delivered to the hand wearing theglove[

2[0[1[ PredictionsOur prediction was that\ with the glove\ normal sub!

jects should show impaired perception in the left hand[Therefore they should "0# have a low level of object rec!ognition with the {a}ected| hand\ and "1# have a lower

level of Same:Di}erent correct judgement rate thanENM[ This is because our hypotheses is that ENM hasintact or quasi!intact pre!attentive sensory processes\whereas normal subjects with the glove do not[

2[1[ Results

In Table 3 the results of the two subjects on double!stimulation trials are reported[ The only condition inwhich we were able to obtain the same level of recognitionperformance as in ENM was the DS condition "see Table3#[ For subject GVB naming performance was good forobjects in the right hand "79) correct#[ However\ whenwe consider the left hand\ whose perceptual capabilitywas degraded with the glove\ naming performance wassigni_cantly worse "29) correct# than naming with theright hand "P³ 9[94 by Fischer|s exact test#[ In this con!dition\ Same:Di}erent judgement did not di}er sig!ni_cantly from chance "59) correct^ P�9[49 byFischer|s exact test#[

Turning to subject GB\ a similar pattern of resultsemerges "see Table 3#[ Right hand naming was fairly good"89) correct#\ whereas left hand naming was signi_cantlyworse "29) correct^ P³ 9[90 by Fischer|s exact test#[Same:Di}erent judgements were at chance "49) correct#[Considering the two subjects together\ the overall resultscon_rmed this pattern] right hand naming 74)^ left handnaming 29) "the di}erence was signi_cant\ P³ 9[990 byFischer|s exact test#^ Same:Di}erent judgement atchance\ 44) "P�9[49 by Fischer|s exact test#[

If we inspect the overall performance of GVB and GB"Table 4#\ it clearly emerges that\ although the di}erencebetween right hand and left hand performance still per!sisted "72 vs 32)^ P³ 9[990 by Fischer|s exact test#\ lefthand overall performance is better than in the conditionDS only[ With such performance\ the overall Same:Di}erent score is 64) correct ðthe score is signi_cantlyabove chance\ Chi "df�08#�09[5\ P³ 9[90Ł[ Thissomehow con_rms the Farah et al[|s ð5Ł idea that Same:

Table 3GVB and GB|s accuracy for same:di}erent judgements and for namingin DS condition on double!stimulation

Subjects S:D LH RH")# ")# ")#

GVB 5:09 2:09 7:09"59# "29# "79#

GB 4:09 2:09 8:09"49# "29# "89#

TOTAL 00:19 5:19 06:19"44# "29# "74#



Table 4GVB and GB|s accuracy for same:di}erent judgements overall and fornaming in di}erent trials on double!stimulation

Subjects S:D LH RH")# ")# ")#

GVB 29:39 7:19 06:19"64# "39# "74#

GB 29:39 8:19 05:19"64# "34# "79#

TOTAL 59:79 06:39 22:39"64# "32# "72#


Table 5GVB and GB|s accuracy for same:di}erent judgements in the variousconditions

Subjects SI SD DD DS")# ")# ")# ")#

GVB 8:09 5:09 8:09 5:09"89# "59# "89# "59#

GB 8:09 5:09 09:09 4:09"89# "59# "099# "49#

TOTAL 07:19 01:19 08:19 00:19"89# "59# "84# "44#

SI � same identical^ SD � same di}erent^ DD � di}erent dissimilar^DS � di}erent similar[

Di}erent judgement tasks are simpler than recognitiontasks[ However\ inspection of Table 5 clearly shows thatthis might be true for the easy conditions of the experi!ment\ e[g[\ when the two objects are either identical "SIcondition\ overall performance 89) correct# or com!pletely di}erent "DD condition\ overall performance84) correct#[ In these conditions it is even obvious thatone can make a correct Same:Di}erent judgement evenif he or she has no idea of what is being held in the lefthand[ However\ in the two di.cult conditions "SD andDS#\ where physical similarity did not correspond to cat!egorical similarity\ normal subjects with low level lefthand recognition performance were not able to makecorrect Same:Di}erent judgements[ Indeed\ in either con!ditions their scores were at chance "59)\ P�9[26 byFischer|s exact test\ and 44)\ P�9[49 by Fischer|s exacttest#[

2[2[ Discussion

The results of the second experiment showed thatwhen\ in normal subjects\ in double stimulation trials\ we

decrease the tactile:haptic perception of one hand\ to adegree similar to that observed in extinction patients\Same:Di}erent judgements were at chance\ whereas pati!ent ENM\ in the same di.cult conditions "SD and DS#and with a similar pattern of left hand recognition rate\obtained a Same:Di}erent score of 69 and 64) correct2[Therefore\ based on our reasoning\ the di}erence in theSame:Di}erent judgement performance between patientENM and the two controls must be due to the fact thatpatient ENM did have access to the category of objects hewas not able to name\ whereas normals\ with a peripheralsensory de_cit caused by the glove\ did not[ Moreover\in our experiment Same:Di}erent judgements were notachieved simply by relying on the texture or the weightsof the objects to be compared[ Indeed\ such a strategywould have caused a great amount of errors in the SDtrials[ In these trials objects\ although sharing the samename had di}erent shape\ di}erent texture and di}erentweights[ If ENM had relied on weight and texture hewould have answered {di}erent| instead of {same|\ per!forming even worse than chance[ On the contrary heperformed well above chance in the SD condition of theexperiment "69) correct#[

We partially agree with Farah et al[|s ð5Ł intuition thatthe Same:Di}erent judgement is a task that\ in certainconditions\ can be easier than the recognition:namingtask[ We would like to point out\ however\ that not allSame:Di}erent tasks are the same[ When we use physi!cally similar objects\ belonging to di}erent naming cat!egories\ Same:Di}erent judgements are much moredi.cult and the amount of information needed for anexplicit judgement of similarity seems to be the same asthe amount of information required by recognition[

3[ General discussion

We summarize our _ndings as follows]

"0# Patient ENM with extrapersonal visual neglect anda right occipito!parietal lesion showed extinction onthe hand contralateral to the brain damage whentested with light touch stimuli[ Although able to reco!gnize\ both visually and tactually\ meaningful man!made objects if presented one at a time to the left orto the right hand\ he was not able to recognize tac!

2 Note that we did not think it useful to also test the patient with theglove because\ if the glove deteriorates the performance in normalsubject\ causing an arti_cial sensory de_cit\ the e}ect would have beeneven more severe in a patient with a cerebral damage and with\ already\some perceptual:attentional problems[ In ENM\ the use of the glovewould have resulted in an even more severe naming problem caused\this time\ by a peripheral sensory de_cit[ As such\ the de_cit couldnot be bypassed by any sort of implicit processing[ The only possibleprediction is that also ENM would have presented with a chance levelperformance in the Same:Di}erent task\ like normals[


tually the same objects with the left hand\ when ano!ther object was held by the right hand[ That is\ heshowed extinction for naming and recognition ð1\ 00Łof real man!made objects[

"1# Extinction of the left hand object persisted when thenaming task was performed with the arm crossed\i[e[\ when the right hand was manipulating the objectto the left of the trunk midline and the left hand wasmanipulating the object to the right of the trunkmidline[ In the crossed condition also the per!formance of the right hand worsened[

"2# Although patient ENM was very often unable toname the left hand object\ he performed well abovechance in a Same:Di}erent task[

"3# Experiment 1 showed that ENM|s good performancein the Same:Di}erent task cannot be completelyascribed to a di}erence in the di.culty between thetwo tasks\ because normal people with only per!ipheral sensory de_cits\ and the same recognition rateas patient ENM\ were not able to perform the Same:Di}erent judgements that patient ENM could carryout with a signi_cant degree of accuracy[ On thecontrary\ we may conclude that patient ENM showeda covert\ nonconscious processing of left hand stim!uli[

These _ndings have many theoretical implications] _rstwe showed that extinction for naming:recognition canalso involve real 2D meaningful objects[ The few clinicalstudies that took into account extinction in the som!atosensory modality were mainly concerned with pat!ients| ability to report light touch stimuli delivered toeither hand and did not study extinction of complexstructured con_gurations[ Some of these studies con!sidered the qualitative aspects of extinction[ Schwartz\Marchok\ and Flynn ð05Ł studied brain damaged patientssimultaneously brushing the _ngers of the two hands withstimuli either identical or di}erent in tactile quality[ Thepatients had to name the materials of which the stimuliwere made[ If patients had {quality extinction| they cor!rectly reported the material of the stimuli when only onestimulus at a time was presented either to the right or tothe left _ngers[ In contrast\ they reported only the qualityof the stimuli presented to the _ngers of the ipsilesionalhand and not the one presented to the _ngers of thecontralesional hand\ in the condition of double!sim!ultaneous stimulation[ A somehow similar test was usedalso by Ito\ Tanabe\ Ikejiri\ Ohuda\ Sawada\ and Shi!raishi ð00Ł\ who showed that extinction could manifestitself at two di}erent levels] the level that they calledperception "i[e[\ when patients not only had qualityextinction but also failed to detect simple stimuli on lighttouch stimulation# and the level of recognition "i[e[\ whenpatients could detect simple light touch stimuli\ but werenot able to recognise the material in the quality extinctiontest#[ Our data\ in keeping with Maravita|s ð01Ł _nding

of extinction of 2D geometric shapes\ show that som!atosensory:haptic extinction is not con_ned to passivetactile stimulation but also a}ects the haptic explorationof more complex and salient percepts[ The mechanismsunderlying somatosensory:haptic extinction are likely tobe similar to that proposed for visual extinction[Although some authors have pointed out that visualextinction can have a sensory component ð1\ 19Ł\ severalobservations suggested that it is a disorder of selectiveattention ð3\ 07Ł[ The disorder manifests itself as an atten!tional bias "e[g[\ ð3Ł# that gives rise to extinction {whentwo events must compete for attention| ð03Ł and the resultis that {stimuli on the ispilesional side have a competitiveadvantage|[ This mechanism has been suggested also fortactile extinction ð00Ł and seems to be at work also inpatient ENM[

The study of ENM|s extinction also discloses someaspects of the functioning of normal perceptual processes[In patient ENM the attentional bias\ in the hapticdomain\ caused by the brain damage\ becomes evidentwhen two simultaneous stimuli compete for attention[Theories of normal perception have suggested that atten!tion acts on stimuli whose basic characteristics have beenalready processed ð08Ł[ Much evidence exists that colour\shape and motion are usually coded in parallel and pre!attentively[ Recently it has been shown that stimulusprocessing is parallel not only for target de_ned by singlefeature "e[g[\ colour# but even when the detection of targetrequires the conjunction of two stimulus characteristics"e[g[\ colour and form\ ð09Ł or movement and form\ ð04Ł#[In other words studies on normal perception show thatmany di}erent stimulus features can be derived pre!attentively[ In addition\ a number of recent neu!ropsychological observations demonstrated that atten!tion is not a pre!requisite even to have access to categoryrepresentation of 1D objects[ Indeed visual extinctionpatients can extract\ from 1D stimuli that are not attent!ively processed\ enough information to decide whetheror not an extinguished object shares the same categoryname with another object presented in the good visual_eld ð19\ 1Ł[ Maravita ð01Ł showed that also 2D rep!resentations of meaningless objects can be derived with!out attention[ Indeed\ the patient he described presenteda normal illusory after e}ect\ which could only beobtained if normal processing of the left!hand 2D extin!guished stimulus was carried out[

In the present study patient ENM had access to cat!egory names of extinguished left hand objects\ such as togive above chance SameÐDi}erent judgements also in themost demanding condition of our experiment "Di}erentÐSimilar condition#[ Because object category could beaccessed only through the tactile manipulation of theobjects\ and therefore\ through a 2D reconstruction oftheir shape\ it can be argued that 2D tactile processingwas carried out normally and\ because of the presence ofextinction\ without attention[ Therefore the present data


seem to suggest that even 2D representation of mean!ingful objects can be derived pre!attentively\ when theattentional bias towards the ipsilesional side was asstrong as to prevent the explicit recognition of the object[Contrary to Mattingley et al[|s study ð03Ł\ the presence ofcoherent objects did not give rise*neither in the presentstudy\ nor in Maravita|s ð01Ł*to awareness of the stim!uli[ This is only apparently contradictory[ Indeed\ in Mat!tingley et al[|s study ð03Ł awareness emerged when twophysically separate visual stimuli originated the illusionof one single surface or object[ In our study\ instead\perception of real objects was always related to two sim!ultaneous\ but clearly separate\ sensory events[ Thisobservation once more con_rms that the nature of extinc!tion is deeply related to the presence of two separateevents\ which compete for attention\ even when they arecomplex and structured as in the experiments justdescribed[

Another interesting _nding of the present study is thatthe attentional impairment shown by ENM in the som!atosensory domain was not related "or not completelyrelated# to his defective coding of extrapersonal space[Indeed\ left hand performance was always worse thanright hand performance independently of the spatial pos!ition of the hand[ Prima facie these data seem to suggestthat ENM|s somatosensory extinction was strictly relatedto the sensory _eld a}ected by the brain damage and\therefore\ according to Smania and Aglioti ð06Ł\ coded insomatotopic coordinates[ This conclusion would implythat ENM|s extinction is more a sensory problem thanan attentional de_cit[ However\ leaving aside the evidencethat shows that the nature of extinction is attentional ð3\07Ł\ the presence of a primary sensory impairment is atodds with ENM|s intact pre!attentive processing[ As weshowed in Experiment 1\ the presence of sensory de_citsprevents any further processing of the stimulus[

How can we\ then\ account for the presence of anattentional de_cit that seems to be coded in somatotopiccoordinates< An explanation might be found in Graziano\Yap and Gross|s ð7Ł investigation on monkeys "also seeð8Ł#[ They described neurons in the premotor cortex ofprimates that respond to visual stimuli in the space adjac!ent to the hand or the arm[ The receptive _elds werefound to move when the arm\ but not the eyes\ changedposition[ In other words\ they are arm!centred neuronsthat can provide the basis for a body centred rep!resentation of space\ which would be useful\ for instance\for the control of reaching movements[ These neuronswere found to also have tactile receptive _elds "also seeð6Ł# on those parts of the body "e[g[\ the arm skin# closeto the visual receptive _elds[ Thus they are the best can!didates for a body centred attentional system[

It has recently been shown ð4Ł that a visuo!tactile per!ipersonal space exists also in humans and that it moveswith the part of the body to which it is anchored[ DiPellegrino\ La�davas and Farne ð4Ł described a patient

in which visual stimuli delivered in the space near theispilesional hand extinguished tactile stimuli on the con!tralesional hand[ Extinction was observed both when thehands were in the anatomical position and when theywere crossed[ It is\ therefore\ reasonable to conclude\ thatin the present study\ the persistence of extinction of theleft hand object when the left hand moved into the rightperipersonal space was more related to the coding ofperipersonal space in a coordinate system centred onbody parts\ than to a somatotopic distribution of extinc!tion[

Another reason for rejecting a sensory interpretationof ENM|s extinction is that\ although in this patientextinction was mainly a left hand phenomenon\ when therecognition had to be performed by the right hand inthe left space\ a signi_cant worsening of the right handperformance was observed[ This _nding is in keepingwith extinction being coded in spatiotopic coordinates[We may advance the hypothesis that patient ENM\ notonly had extinction related to a body!centred coordinatesystem\ which gave rise to extinction of left hand objects\irrespective of the space where the left hand was man!ipulating the object\ but was also a}ected by an atten!tional de_cit related to an extrapersonal space coordinatesystem "ENM showed extrapersonal neglect#\ whicha}ected object recognition when the una}ected handoperated in the a}ected space[

Acknowledgements

This study was supported by a grant from the Eur!opean Science Foundation\ ENP European ResearchGrant No[ 129[ We thank Giuseppe di Pellegrino for hissuggestions and comments\ and also Fabio Benfenati\Paolo Neyroz and Diego Varotto for the execution of thephotographs[

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Somatosensory extinction for meaningful objects in a patient with right hemispheric stroke

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