Neuropsycholo`ia\ Vol[ 25\ No[ 7\ pp[ 606Ð618\ 0887Þ 0887 Elsevier Science Ltd[ All rights reserved\ Pergamon Printed in Great Britain

9917Ð2821:87 ,08[99¦9[99PII] S9917Ð2821"87#99996Ð3

The in~uence of semantic and perceptual encodingon recognition memory in Alzheimer|s disease

MARIE!CLAIRE GOLDBLUM\�& CLAUDIA!MARIA GOMEZ\�GIANFRANCO DALLA BARBA\� FRANCž OIS BOLLER\� BERNARD DEWEER\$

VALEłRIE HAHN$ and BRUNO DUBOIS%

� U[213 INSERM\ Centre Paul Broca\ Paris\ France^ $ U[178 INSERM\ Ho¼pital de la salpe¼trie�re\ Paris\ France^% De�partement de Neurologie\ Ho¼pital Henri Mondor\ Cre�teil\ France

"Received 12 May 0886^ accepted 29 December 0886#

Abstract*Previous results from a population of patients with Alzheimer|s disease "Dalla Barba and Goldblum\ 0885# demonstratedthat the ability of patients to make a semantic association between two items was signi_cantly and positively correlated to theirperformance on a yes:no recognition task for the same items and that patients who were impaired on the semantic task didsigni_cantly worse on the recognition task than patients who were unimpaired on the semantic task[ These _ndings gave support toa hierarchical model of organization of human memory in which episodic memory depends on the integrity of semantic memory[The present study further investigates the relationship between semantic memory de_cits and episodic recognition memory in 04patients with Alzheimer|s disease and 04 controls\ as a function of their semantic and perceptual encoding abilities and of theircognitive impairment in other domains[ The results con_rmed the previous _ndings and showed that\ although patients heavily reliedon perceptual analysis\ this type of encoding did not enhance their recognition memory[ Correlations analyses showed thatsome patients who were not impaired in the semantic association\ but with particularly low scores on a verbal ~uency task presentedwith a pattern\ in recognition memory tasks\ that suggests a possible early involvement of frontal lobes in this subgroup of patients[Þ 0887 Elsevier Science Ltd[ All rights reserved[

Key Words] Alzheimer|s disease^ semantic memory^ episodic memory^ semantic encoding^ perceptual encoding[

Introduction

There is a general agreement that the prevailing classi!cal view of human long term memory "LTM# as a simpleunitary system cannot easily be maintained[ Much of therelevant information favoring the view that LTM shouldbe fractionated into functionally di}erent systems or sub!systems comes from the study of brain!damaged patientswith selective memory impairment ð23Ł[ There is lessagreement\ however\ as to how the organisation of LTMshould be conceptualized[ For instance\ the neurologicalreality "beyond its heuristic value# of the frequently useddistinction between semantic and episodic memory sys!tems has been questioned ð0\ 1Ł[

Neuropsychological evidence for the selective impair!ment of semantic or episodic memory would validate the

& To whom all correspondence should be addressed] Marie!Claire Goldblum[\ U[213 INSERM\ 1 ter rue d|Ale�sia\ 64903Paris\ France[ Fax] 22 0 34 78 57 37^ E!mail] goldblumÝbroca[inserm[fr

606

view that these two memory systems are independent\ atleast in functional terms if not necessarily in terms ofdistinct cerebral structures[ It has been argued that epi!sodic and semantic memory systems are organized in ahierarchical way ð27\ 28Ł[ According to this hypothesisepisodic memory is a speci_c subsystem of semantic mem!ory\ implying therefore that episodic memory depends onthe integrity of semantic memory[ Such a model _ts wellwith selective impairment of episodic memory\ but notwith a condition in which semantic memory would becompromised in the context of an intact episodicmemory[ Alternative hypothesis ð26Ł hold that episodicmemory and semantic memory are organized in parallel\i[e[ that they are two speci_c and independent subsystemsof long!term memory[ According to this view\ selectivede_cits of each of the two systems can be observed\ sincethe operations of one system do not depend on the integ!rity of the other system[

Episodic memory de_cits in the absence of comparabledisturbances in the semantic domain have been regularlydescribed ð6\ 7\ 10\ 31\ 32Ł and this pattern is the most

M[!C[ Goldblum et al[:Recognition memory in Alzheimer|s disease607

prominent in classic amnesia\ although this view has notachieved consensus[ Some authors consider that this viewis possibly confounded by di}erences in time periodsbecause spared abilities\ which correspond mainly to gen!eral semantic knowledge\ would also correspond to old\overlearned memories\ while impaired abilities wouldcorrespond to the acquisition of new information\whether or not their nature is semantic or episodic\ ð0\24\ 26Ł[ However\ studies of memory!loss associated withnormal aging also show\ as a general _nding\ that mem!ory for speci_c events declines with age whereas age!related decrement in semantic memory organization andfunctioning are minimal if not absent ð5Ł[

Relatively pure semantic memory impairment has alsobeen reported in several cases\ yet\ information relatedto episodic memory was never precisely described in thesecases\ being either not tested ð20\ 22 39Ł or reported to benormal\ anecdotally ð00Ł\ or on the basis of informalclinical assessment ð06\ 07Ł[

Semantic memory disorders have also been well docu!mented\ particularly in the context of Alzheimer|s diseaseð4\ 11Ł[ Indeed\ besides a severe and progressive deterio!ration of episodic memory\ semantic memory disordersare the rule\ as shown by the poor performance of patientsin category ~uency tasks\ naming and semantic matchingof words and pictures\ although they seem to appear laterin the course of the disease[ Desgrange et al[ ð02Ł studieda group of patients with Alzheimer|s disease "AD# andisolated two cases with semantic memory disorders in thecontext of an intact episodic memory[ Notwithstandingthe fact that an intact episodic memory cast doubt on thediagnosis of AD in these cases\ the semantic memoryimpairment of the two patients was deduced from per!formance on only semantic and formal verbal ~uencytasks[ Consequently\ case è1 was also presented as apotential candidate for another dissociation betweenimpairment in executive functions\ which were also mea!sured partly by the verbal ~uency tasks and intact epi!sodic memory[ The fact that executive functions andsemantic memory were assessed by performances onoverlapping tests clearly does not allow to make anyconclusion in terms of semantic memory disorders per se[Actually\ data relevant to a clear double dissociation\ i[e[semantic memory impairment without episodic memoryimpairment\ are not conclusive[

It should be noted\ however\ that double dissociationmay not be the only way to look at the independence\or interdepence\ between hypothesized memory systems[Even a condition like AD\ in which disorders in the twomemory systems are present to various degrees\ may givesome clue to the relationship they may entertain[

To study the relationship between these hypotheticalcognitive functions "episodic vs semantic memory#\ DallaBarba et al[ ð8Ł devised an experimental design\ in whichaphasic patients were asked to encode the same type ofnon!verbal material either perceptually or by making asemantic association[ Their assumption was that\ if thehierarchical hypothesis is correct\ it should be expected]

"0# that patients with impaired semantic memory havealso impaired episodic memory and "1# that a positivecorrelation should be expected between patients abilityto make a semantic association at encoding and theirability to recognize the same items in a Yes:No rec!ognition memory test[ They found that in aphasics withunimpaired semantic memory\ recognition performanceimproved following semantic encoding\ whereas in thosewith semantic memory de_cit the recognition per!formance was not in~uenced by the type of encoding[

In a further study\ Dalla Barba and Goldblum ð09Łstudied recognition memory for semantically!relateditems in a population of patients with Alzheimer|s disease"AD# and a group of normal controls "NC#[ The abilityof AD patients to make a semantic association betweentwo items was signi_cantly and positively correlated totheir performance on the recognition task[ Moreover\those patients who were impaired on the semantic associ!ation task did signi_cantly worse on the recognition taskthan patients who were unimpaired on the semanticassociation task[

Both studies suggest that episodic memory may dependon the integrity of semantic memory and give support tothe hierarchical model of organization of humanmemory[ However\ to warrant that results in the ADpopulation were not due to attentional mechanism ratherthan semantic processing per se\ a control of encodingconditions\ semantic vs perceptual was in order[

The aim of the present study was to replicate _ndingsof the previous study ð09Ł and by means of two newexperimental conditions\ to compare] "0# the e}ects ofperceptual and semantic encoding on recognition mem!ory performance\ "1# the e}ect of the presence vs absenceof possible semantic associations between the to be recog!nized items and "2#\ to contrast the patients encoding andrecognition memory capacities with their performancesin other neuropsychological domains[

Method

Subjects

Fifteen patients with AD "00 women and 3 men\ mean age63 "SD � 7#\ mean years of education 00 "SD � 2# meanMMSE score 19[6 "SD � 2## entered the study[ They wererecruited at the {{Clinique de Me�moire du Centre de Neuro!psychologie de l|Ho¼pital de la Salpe¼trie�re||[ The diagnosis ofprobable AD was made according to the NINCDS!ADRDAcriteria ð14Ł[ MRI or CT scanning\ together with blood analysisshowed no evidence for another etiology[ Patients with a historyof head injury\ alcoholism\ or serious psychiatric illness wereexcluded from this group[ Patients with a score of 3 or higheron the Hachinski scale ð05Ł were excluded to reduce the possi!bility of including multi!infarct dementia[ Patients with a scoreunder 04 on the Mini!Mental Status Examination "MMSE^ð03Ł# were also excluded from the study[

Fifteen normal subjects "8 women and 5 men\ mean age 61"SD � 7#\ mean years of education 03 "SD � 5# mean MMSEscore 18[6 "SD � 0## constituted a control group "NC#[ Theywere either spouses of patients or other individuals who vol!

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unteered to participate in the research projects of our labora!tory[ Informed consent was obtained from all subjectsparticipating to the study[

No signi_cant di}erence emerged in sex distribution betweenthe groups "x1 � 9[5\ P × 9[69 n[s[#[

Factorial analyses of variance "ANOVAS# conducted onthese variables showed no signi_cant e}ect of sex on eitherage\ years of education\ or MMSE scores[ The group factorsigni_cantly a}ected MMSE scores "F"0\15# � 62[4^P ³ 9[9990# and years of education "F"0\15# � 7[05^ P ³ 9[998#[Group comparisons indicated that\ as expected\ AD patientshad MMSE scores signi_cantly lower than NC "t � 8[6^P ³ 9[9990# and that AD patients had also a lower level ofeducation than controls "t � 2[0^ P ³ 9[994#[

Neuropsychological evaluation

The AD patients and controls were submitted to a set oftasks assessing their cognitive abilities in various domains]

Memory] Wechsler Memory Scale ð30Ł[Lan`ua`e] Sentence Comprehension "Part VI of the Token Test\

ð01ŁVerbal semantics] Verbal Fluency "subjects were given 59 s to

generate as many exemplars as possible from the semanticcategory of animals#\ Confrontation Naming of 37 pic!tures "from the set of Snodgrass and Vanderwart 0879ð25Ł#\ Word to Picture Matching "the words depicting the37 pictures used in the naming task had to be matchedto the corresponding picture among a choice of threeitems#[

Non Verbal Semantics] A Picture Classi_cation task ð17Ł\ inwhich subjects had to sort pictures of living and non!living things at two category levels "subordinate level for5 categories of living things\ such as mammals\ and 5categories of non!living things\ such as vehicles^ attributelevel for 3 categories of living things\ such as _erce vsnon!_erce animals and 3 categories of non!living things\such as fast vs slow vehicles#[

Visuo!Constructive abilities] Immediate Copy of Rey|s complex_gure ð29Ł and Benton|s Line Orientation test ð2Ł[

Intellectual abilities] Raven|s Colored Progressive Matrices!PM36 ð21Ł[

Scores obtained by the 1 groups of subjects are shown inTable 0[ As expected\ AD patients obtain lower scores than NC

Table 0[ Neuropsychological evaluation

Intellectual Non!verbal Visuo!constructiveGroup abilities Language Verbal semantics semantics abilities Memory

Benton|sWordÐpicture Picture Rey|s line

Raven|s Token test Naming Verbal matching classi_cation _gure orientationPM!36 "max � 02#� "max � 37# ~uency "max � 37# A|�� copy test WMS

AD 07[1 8[6 25[8 8[7 35[8 9[83 07[1 08[5 71[3"SD# "4[8# "1[1# "6[1# "2[7# "0[2# "9[90# "4[8# "5[6# "8[5#NC 29[4 01[1 35[2 12[6 36[4 9[87 20[7 14[9 011[2"SD# "1[9# "9[6# "1[0# "3[0# "9[5# "9[91# "1[1# "2[3# "7[0#

Student t � 6[5 t � 3[1 t � 3[7 t � 8[5 t � 0[3 t � 5[5 t � 3[9 t � 1[7 t � 00[8t!test P ³ 9[9990 P ³ 9[9990 P ³ 9[9990 P ³ 9[9990 n[s[ P ³ 9[9990 P ³ 9[9990 P ³ 9[91 P ³ 9[9990

� Subjects| comprehension was assessed only on part VI "02 commands# of the Token Test[�� Statistical comparisons were carried by means of comparisons of the discrimination index A| proposed non!parametric SignalDetection Theory which takes into account rates of hits and false alarms ð04Ł[

on every test[ Group comparisons "see last row# show that\ withthe exception of Word to Picture Matching\ these di}erencesare highly signi_cant[

Experimental procedure

Each item of the four lists used in the experimental protocolwas adapted from the Pyramids and Palm!Trees test ð19Ł[ Theyconsisted of a 29×19 cm card representing three di}erent pic!tures placed at each angle of a virtual triangle "Fig[ 0#[

For each of the 3 lists\ 13 items were constructed[ The 13cards were divided randomly into 1 sets of 01 cards for use astarget items and lure items[ Consequently\ each target item orlure item consisted of a card representing three di}erentpictures[ Within each group of subjects\ target items for halfthe subjects were lure items for the other half[

As a consequence of varying encoding conditions "list 1 vslist 2#\ explicit demands to realize such an encoding "lists 1 and2 vs list 0 and 3# and the presence vs absence of semanticrelationship between the 2 pictures within items "list 0\ 1 and 2vs list 3#\ only items in list 1 strictly corresponded to the originaltest ð19Ł which requires subjects to match a target picture "e[g[an Egyptian pyramid#\ to one "e[g[ palm!tree# entertaining asemantic relationship with the target\ among two choice pic!tures "e[g[ palm!treeÐ_r tree#[

List 0[ Semantic relationship present between pictures\ no explicitencoding required "Fig[ 0a#[ The 01 items were presented oneafter the other for approximately 2 s each and subjects weregiven no further instruction than to closely inspect the items[

List 1[ Semantic relationship present between pictures\ explicitsemantic encoding required "Fig[ 0b#[ The 01 items were pre!sented one after the other for approximately 2 s each[ For eachitem subjects were instructed to choose the picture "e[g[ themarine# they considered most closely related to the target "e[g[the buoy#[

List 2[ Semantic relationship present between pictures\ explicitperceptual encoding required "Fig[ 0c#[ As for lists 0 and 1\pictures in the same card had a semantic relationship\ but aperceptual dimension was introduced[ For that purpose\ one ofthe two choice pictures had a similar "2 items#\ di}erent "2items#\ smaller "2 items#\ or larger "2 items#\ size than the target[To minimize the possible processing of items through semantic

M[!C[ Goldblum et al[:Recognition memory in Alzheimer|s disease619

Fig[ 0[

knowledge\ the real relative sizes of pictured objects wererespected[ The 01 items were presented one after the other forapproximately 2 s each[ For each item subjects were instructedto choose the item they considered most closely related in size"similar\ di}erent\ smaller\ or larger# to the target "see Fig[0c\ for an example of {{larger*the cow*than the target*thefawn|| relationship#[

List 3[ Semantic relationship absent between pictures\ no explicitencoding required "Fig[ 0d#[ In contrast to the other lists\ thepictures used in these items did not entertain any particular"evident# semantic or physical relationship[ The 01 items werepresented one after the other for approximately 2 s each[ As forlist 0\ subjects were given no further instruction than to closelyinspect the items[

The four lists were presented in a _xed order "0!1!2!3# to thesubjects who were not informed that their memory of the itemswould be tested[ Although covert naming of the stimuli couldnot be prevented\ subjects were explicitly asked not to name thepresented pictures[ The presentation of the 01 experimentalitems in list 1 and 2 was preceded by an item for which theexaminer explained the encoding task to the subject[ Followingthe presentation of the 3 series of 01 items\ subjects were givena Yes:No recognition test consisting of the 37 studied itemstogether with 37 lure items[ For each experiment the lures weredesignated in advance[ The items of the recognition test werepresented in the same order for each subgroup of subjects[

Results

The mean scores obtained by the 1 groups in the enco!ding and recognition tests are shown in Table 1[

Because our patients had a signi_cantly lower levelof education than NC\ the subjects performance on thedependent variables "1 association and 3 recognitionmemory tasks# was examined by means of an ANCOVA\with education "years of schooling# as a covariate[ Theresults showed no signi_cant main e}ect of education oneither the semantic or perceptive association"F"0\15#�9[908\ n[s[^ and F"0\15#�9[044\ n[s[\ respec!tively# or the recognition scores "List 0] F"0\15#�1[15\n[s[^ List 1] F"0\15#�9[462\ n[s[^ List 2] F"0\15#�9[462\n[s[ and List 3] F"0\15#�9[702\ n[s[#[ Moreover no inter!action emerged between education and the group factoron the dependent variables[ Consequently education hasbeen eliminated from further analyses and individualscores were submitted to repeated measures analyses ofvariance "ANOVAS# with group "AD and NC# as theintersubject factor and encoding "semantic or perceptual#and recognition memory scores "type of list] 0!1!2!3# asintrasubject factors[

M[!C[ Goldblum et al[:Recognition memory in Alzheimer|s disease 610

Table 1[ Mean encoding ") correct# and recognition "A|� scores#

Group Encoding Recognition

Semantic Perceptual List 0 List 1 List 2 List 3

AD 76[1 81[7 9[61 9[74 9[68 9[61"SD# "09[8# "7[14# "9[02# "9[97# "9[97# "9[03#NC 86[1 87[8 9[85 9[86 9[85 9[83"SD# "4[0# "1[8# "9[91# "9[91# "9[93# "9[92#

� Scores were computed according to the discrimination index A| proposed in non!parametric Signal Detection Theory which takesinto account rates of hits and false alarms ð04Ł[

Encoding

The results showed that subjects encoding scores weresigni_cantly a}ected by the group factor "F"0\17#�02[12^ P³ 9[991#[ Group comparisons showed that ADpatients obtained signi_cantly lower scores than NCwhatever the type of encoding "semantic] t�2[1\P³ 9[993^ perceptual] t�1[6\ P³ 9[90#[ The type ofencoding also signi_cantly a}ected the subjects encodingscores "F"0\17#�4[2^ P³ 9[92#[ Both AD and NC sub!jects obtained higher scores on the perceptual comparedto the semantic encoding task\ although the di}erencedid not reach statistical signi_cance in either group[

Recognition memory

Recognition memory scores were signi_cantly a}ectedby the group "F"0\17#�80[48^ P³ 9[9990# as well as thetype of list factors "F"2\73#�7[4^ P³ 9[9990#[ Like forencoding\ AD patients obtained signi_cantly lower scoresthan NC whatever the type of list[ However\ there was

Fig[ 1[

a signi_cant interaction between the type of list to berecognized and the group factor "F"2\73#�3[38^P³ 9[995#[ As illustrated in Fig[ 1\ the source of thisinteraction was mainly due to the performance of the 1groups on recognition memory for items in list 0[

In the NC group\ recognition scores of items for whichsemantic or perceptual encoding were required\ "list 1 andlist 2 respectively# did not signi_cantly di}er "t�9[47\P× 9[4# but\ more importantly\ no di}erence emergedbetween recognition scores on list 1 and list 0\ in whichsemantic encoding was possible but not explicitlyrequired "t�0[4\ P× 9[0#[ Moreover\ both list 1 and list0 yielded signi_cantly higher recognition scores than list3\ for which no speci_c encoding was required and nosemantic link was present between pictures in the sameitems "t�3[07\ P³ 9[990 and t�2[4^ P³ 9[993\ respec!tively#[

By contrast\ in the AD group\ recognition of items inlist 1 "for which semantic encoding was explicitlyrequired# was signi_cantly higher than recognition ofitems in every other list "list 3] t�2[4\ P³ 9[993\ List 2]t�1[8\ P³ 9[91 and list 0] t�3[90\ P³ 9[991#[ No

M[!C[ Goldblum et al[:Recognition memory in Alzheimer|s disease611

di}erence emerged between recognition scores for itemsin lists 0 and 3 for which no encoding instruction wasgiven[ List 2\ for which explicit perceptual encoding wasrequired\ yielded signi_cantly better performance"t�1[2\ P³ 9[93# only over list 3 for which no explicitencoding was required and no semantic relationshipexisted between pictures in the same item[

Correlation analyses between encoding conditions andrecognition memory performances

To further explore the relationships between semanticand perceptual encoding abilities of subjects and their inrecognition memory performance\ correlation analyseswere conducted on individual subjects scores[

No signi_cant correlation emerged in the NC group\either between perceptual and semantic encoding scores\recognition memory scores of the 3 lists\ or encoding andrecognition memory scores[

In the AD patients group "Table 2#\ only a trend for acorrelation between perceptual and semantic encodingemerged "P³ 9[0#[ Recognition memory scores on list 1items appeared to be signi_cantly correlated to scores onlist 2 items "P³9[93# as were scores on items of list 2 andlist 3 "P³ 9[94#[ Semantic encoding scores were sig!ni_cantly correlated to recognition of items of list 1"P³ 9[991#\ and scores on perceptual encoding were cor!related to recognition of items of list 2 "P³ 9[995# butalso to recognition of items of list 1 "P³ 9[94#[

Correlation analyses between recognition memory anddemographic data

In the NC group\ no signi_cant correlation emergedbetween either age\ educational level or MMSE scoresand either "semantic or perceptual# encoding abilities\ orrecognition memory performances[ In the AD patientsgroup only one signi_cant correlation emerged betweensemantic encoding and MMSE scores "r�9[406\P³ 9[94#[

Table 2[ Correlations between encoding and recognition scores]AD patients

Encoding

Encoding Semantic PerceptualPerceptual 9[336

Recogntion RecognitionList 0 9[212 9[911 List 0List 1 9[610 9[406 9[239 List 1List 2 9[274 5[50 9[052 9[448 List 2List 3 9[250 9[258 9[954 9[104 9[401

Correlation analyses between encoding conditions\recognition memory and neuropsychological evaluationperformance

Since two cognitive domains "verbal semantics andvisuo!constructive abilities# were evaluated using mul!tiple tests\ individual scores have been transformed into{{z scores|| in order to obtain single composite scores[

The semantic or perceptual encoding abilities of NCsubjects were not signi_cantly correlated with their neu!ropsychological scores[ As regard recognition memory\only recognition of items in list 2 "perceptual encoding#showed a signi_cant correlation with their compositescore on verbal semantics "r�9[428\ P³ 9[93#[

For AD patients "Table 3#\ semantic encoding abilitieswere signi_cantly correlated with their language com!prehension "r�9[475\ P³ 9[91# and non!verbal sem!antic "picture categorization# scores "r�9[438\P³ 9[93#[ Perceptual encoding abilities were signi_cantlycorrelated with their composite visuo!constructive scores"r�9[578\ P³ 9[993#[ Recognition memory of list 1 wassigni_cantly correlated with their scores on the WechslerMemory Scale "r�9[456\ P³ 9[94# and recognition ofitems in list 0 with language comprehension "r�578\P³ 9[993#[ As expected\ the patients recognition of itemsin list 2 showed a signi_cant correlation with their com!posite scores on visuo!constructive abilities "r�9[524\P³ 9[90#[

The absence of correlation between semantic encodingabilities of AD patients and their score on verbal sem!antics was somehow unexpected[ One possible expla!nation might be that the composite score included theperformance on the Word to Picture Matching test whichhad revealed not to be a sensitive measure of AD patientssemantic disturbances\ since no signi_cant di}erenceemerged between patients and NC on this test "Table 1#[When scores on Word to Picture Matching were removedthere was actually a trend for a correlation between thesemantic encoding abilities of AD patients and their scoreon verbal semantics "r�9[492\ P³ 9[95#[

In order to examine more closely the correlationsreported above\ a correlation analysis has been conductedtaking into account each score entering the compositemeasures "visuo!constructive and verbal semantics abili!ties#[

Visual Confrontation Naming performance of the NCsubjects was the main source for the correlation betweentheir verbal semantics composite score and their rec!ognition of items in list 2 "r�9[506\ P³ 9[91#[ Thisanalysis also demonstrated that their recognition of itemsin list 1 was signi_cantly correlated with their score onthe Word to Picture Matching test "r�9[591\ P³ 9[91#[

In the AD group\ the signi_cant correlation betweensemantic encoding scores and composite verbal semanticscore was mainly due to visual confrontation namingscores and a signi_cant correlation emerged between ver!bal ~uency scores and recognition of items in list 0"r�9[434\ P³ 9[93#[ Scores on the copy of Rey|s _gure

M[!C[ Goldblum et al[:Recognition memory in Alzheimer|s disease 612

Table 3[ AD patients] Correlations between encoding\ recognition and neuropsychological abilities

Verbalsemantics

Intellectual Language Verbal "without wordÐ Non!verbal Visuo!constructiveabilities token test semantics picture matching# semantics abilities Memory

EncodingSemantic 9[291 9[475 9[238 9[492 9[438 9[317 9[360Perceptual 9[103 9[154 9[958 9[030 −9[924 9[578 9[066

RecogntionList 0 −9[128 9[578 9[243 9[364 9[169 −9[060 9[398List 1 9[132 9[367 9[056 9[225 9[177 9[331 9[456List 2 9[005 9[031 9[130 9[393 [032 9[524 9[020List 3 −9[946 9[021 −9[099 9[978 9[187 9[204 9[290

was the main source for the signi_cant correlationbetween their composite visuo!constructive score andtheir perceptual encoding "r�9[587\ P³ 9[992# as wellas their recognition memory scores of list 2 "r�9[587\P³ 9[992#[ Moreover\ a signi_cant correlation emergedbetween patients scores on the Rey|s _gure copy and boththeir scores on semantic encoding "r�9[431\ P³ 9[93#and recognition of items in list 1 "r�9[598\ P³ 9[91#[

Subgroup analysis

The results presented above showed that AD patientsability to match items on a semantic basis was correlatedto their subsequent ability to recognize these items andthat this encoding condition induced signi_cantly betterrecognition memory scores than any other condition[

In order to substantiate these results we looked atindividual data dividing patients according to their abilityto make a semantic association[ In one group "SM¦#were included all patients with a score on the semanticassociation task within two standard deviations "SD#compared to the mean score obtained by NC\ and in asecond group "SM−# all patients whose score on thesemantic association task was below two SD|s comparedto the mean score obtained by NC[ Subsequent to thisnew division\ the SM¦ group consisted of 7 patients "1men and 5 women# with the following "mean# charac!teristics] age 65 years\ 00 years of education and MMSEscore of 10\4[ The SM− group consisted of 6 patients "1men and 4 women# with the following "mean# charac!teristics] age 60 years\ 00 years of education and MMSEscore of 08[6[

Results of the neuropsychological assessment of pat!ients entering the subgroups are shown in Table 4[Although the SM− group of patients generally obtainedlower scores than the SM¦ group of patients on theneuropsychological tests\ a signi_cant advantage for theSM¦ group emerged only on the Token Test[

Individual scores were submitted to repeated measuresanalyses of variance "ANOVAs# with group "SM¦ and

SM−# as an intersubject factor and encoding "semanticor perceptual# and recognition memory scores "type oflist] 0!1!2!3# as intrasubject factors[

The results "Fig[ 2# showed that encoding scores ofpatients were a}ected signi_cantly by the group factor"F"0\02#�03[97^ P³ 9[992#[ As expected\ SM¦ patientsobtained signi_cantly higher scores than SM− on thesemantic task "t�3[27\ P³ 9[9996#[ The type of enco!ding also signi_cantly a}ected the subjects encodingscores "F"0\02#�4[8^ P³ 9[93#[ However\ the inter!action between the group and encoding factors was onlymarginally signi_cant "F"0\02# 3[90^ P³ 9[96#[

Recognition memory scores were signi_cantly a}ectedby the group factor "F"0\02#�7[01^ P³ 9[91# as well asthe type of list factors "F"2\28#�5[14^ P³ 9[991#[ Thepro_les of the two groups on recognition memory testswere similar "Fig[ 2# and no signi_cant interactionemerged between the type of list to be recognized and thegroup factor[

Between!group comparisons showed\ however\ thatAD patients with SM¦ obtained signi_cantly higherscores than SM− patients only on list 0 and list 1"t�1[10\ P³ 9[94 and t�2[1\ P³ 9[997 respectively#[

Within!group comparisons indicated that\ althoughrecognition performance scores were highest on list 1for both SM¦ and SM− patients\ only SM¦ patients!showed a signi_cantly better recognition performance onlist 1 compared to recognition of either list 0 "t�1[37\P³ 9[94#\ list 2 "t�1[72\ P³ 9[92#\ or list 3 "t�1[73\P³ 9[92#[ In the SM− group of patients the same com!parisons showed that both list 1 and 2\ for which anexplicit encoding strategy was required\ yielded a sig!ni_cantly better recognition performance only over list 0"t�2[16\ P³ 9[91 and t�1[35\ P³ 9[94 respectively#[

Correlations analysis had shown a signi_cant cor!relation between the verbal ~uency scores of the totalgroup of AD patients and their recognition memory oflist 0 for which there was a possible semantic processingof items although no explicit encoding was required[ Wedecided to look at this result more precisely\ taking intoaccount both the ability of the subjects to make a correct

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Table 4[ Neuropsychological evaluation of the SM¦ and SM− subgroups of AD patients

Intellectual Non!verbal Visuo!constructiveGroup abilities Language Verbal semantics semantics abilities Memory

Benton|sWordÐpicture Picture Rey|s line

Raven|s Token test Naming Verbal matching classi_cation _gure orientationPM!36 "max � 02#� "max � 37# ~uency "max � 37# A|�� copy test WMS

SM¦ 08[3 0[0 27[0 09[0 35[6 9[84 11[8 10[3 76[2"SD# "5[4# "0[7# "6[9# "3[8# "0[4# "9[91# "00[2# "4[5# "7[5#SM− 05[8 7[2 24[5 8[3 36[2 9[82 02[8 06[8 67[2"SD# "4[3# "0[6# "6[6# "1[1# "9[84# "9[91# "02[9# "6[5# "7[8#

Student t � 9[70 t � 2[90 t � 9[561 t � 9[232 t � 9[886 t � 9[705 t � 0[34 t � 0 t � 0[74t!test n[s[ P � 9[90 n[s[ n[s[ ns n[s[ n[s[ n[s[ n[s[

� Subjects| comprehension was assessed only on part VI "02 commands# of the Token test[�� Statistical comparisons were carried by means of comparisons of the discrimination index A| proposed in non!parametric SignalDetection Theory which takes into account rates of hits and false alarms ð04Ł[

semantic association and their score on the verbal ~uencytask[ In the group of SM¦ patients\ 2 subjects wereconsidered to have a {{high|| verbal ~uency "mean pro!duction of 05 words^ r�04Ð06# whereas 4 other subjectshad a mean production of 6 words "r�3Ð09# and wereconsidered to have a {{low|| verbal ~uency[ In the SM−group of patients no such distinction could be made sinceall patients had low verbal ~uency scores with a meanproduction of 8 words "r�5Ð01#[ The pro_les of thesethree groups of patients and of the controls on the twoencoding tasks and the four recognition lists are pre!sented in Fig[ 3[

The observed patterns suggest that patients with SM¦do not constitute an homogeneous group[ Whatever theirscore on the verbal ~uency task\ SM¦ patients do notdi}er on their mean recognition score for items in list 1"which is in keeping with their preserved ability to makea correct semantic encoding of these items#[ However\SM¦ patients with low verbal ~uency obtained scoresthat were closer to those of patients with SM− in everyother recognition memory condition\ for which either noencoding instruction was given "list 0 and 3# or with aperceptual encoding instruction[ This suggest that verbal~uency de_cits may constitute a cause of memory de_citsin AD patients relatively independent from semantic andepisodic memory disorders[

Discussion

The purpose of the present study was to investigatethe relationship between semantic memory de_cits andepisodic recognition memory performance in patientswith AD as a function of di}erent encoding situationsand of the type of their cognitive impairment[

As expected\ besides Language comprehension\ Visuo!Constructive abilities\ Memory and Reasoning capacity\AD patients had signi_cantly lower scores than NC sub!

jects in every task of semantic memory\ except the Wordto Picture Matching\ for which no di}erence appearedbetween the two groups[ This is in agreement with pre!vious literature showing that de_cits of semantic memoryare present even at an early stage of the disease and thatWord to Picture Matching is frequently preserved ð08Ł[

In line with their decreased semantic abilities\ AD pat!ients were impaired in the semantic encoding task "Pyra!mids and Palm trees#[ Interestingly\ their performancewas correlated to their general cognitive state measuredby the MMSE\ to other measures of verbal and non!verbal semantic memory and more surprisingly\ to theirvisuo!constructive abilities[

Performance of AD patients on the perceptual enco!ding although higher than on the semantic condition wassigni_cantly lower than that of controls[ Their per!formance was related to global scores on visuo!con!structive abilities and particularly with the copy of Rey|s_gure\ but not with their general cognitive state "MMSE#[

Various possible\ non exclusive\ explanations can beforwarded for this fact[ First\ the MMSE evaluates lessvisuo!constructive abilities than general knowledge andword meaning[ Second\ the perceptual encoding taskmight be considered as being easier than the semanticencoding task since the scores of both patients and con!trols were higher in this condition[ Finally\ progressionof the disease together with its heterogeneity ð12\ 13Łmight also contribute to the observed independencebetween MMSE scores and visuo!constructive de_cits[It has been shown that within the general pattern ofneuropsychological disease progression of AD\ visuoÐspatial abilities are usually impaired in later stages of thedisease at the di}erence of memory or lexico!semanticabilities ð18Ł[ The discrepancies between semantic andperceptual encoding correlations with MMSE scores maybe due to relatively early stage of the disease[ The lack ofsigni_cant correlation between semantic and perceptualencoding scores could also re~ect asymmetries of right

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and left hemisphere impairment[ The observed cor!relation between semantic encoding performance andscores on a visuo!constructive task such as the copy ofthe Rey _gure in the AD group is not in contradictionwith this hypothesis[ Patients may have recourse to theirbetter preserved visuo!constructive abilities to alleviatetheir semantic impairment[

In regards to this apparently surprising correlationbetween semantic encoding scores of patients and theirvisuo!constructive abilities\ in particular with the copy ofRey|s _gure\ results obtained on a picture categorizationtask in a group of AD patients ð17Ł are relevant[ Patientscategorized signi_cantly better living items\ which possessa high degree of intra!category visual similarity\ at asubordinate level[ By contrast\ when classi_cation hadto be carried out at an attribute level\ for which visualsimilarity was not relevant\ the performance of patientswas poor and showed no advantage for classi_cation ofliving items over non!living ones[ Such an over!relianceon perceptual analysis which leads to relatively goodperformance in classi_cation of living things at a sub!ordinate level and poor performance in classi_cation ofliving things at a subordinate level is in agreement withresults by Chan et al[ ð3Ł[ These authors underlined thefact that in categorizing names of animals\ AD patientsfocused rather on concrete perceptual "size# informationthan on abstract conceptual knowledge about dom!esticity like NC subjects and the more so as a function ofthe severity of dementia[

Thus\ the general pattern of correlations within thepatient group showed some consistency\ whereas the gen!eral lack of correlations in NC may re~ect the high "ifnot ceiling# level of performances of this group[

As expected\ AD patients were impaired relative to NCin recognition memory task whatever the presence "list 1and 2# or absence "list 0 and 3# of encoding cues\ and thetype of encoding "semantic] list 1 or perceptual] list 2#[

In the two groups\ recognition of list 1 for whichexplicit instruction to semantic encoding was providedentailed the highest scores\ whereas list 3 in which therewas no semantic or physical relationship and no explicitencoding instruction entailed the lowest scores[ This pat!tern indicates that both the ability to e}ect semanticprocessing and the presence of explicit instruction toencode the to be recognized items are important deter!minants of recognition memory[ The pattern of per!formance of AD patients resembles the one of aphasicpatients ð8Ł but shows important di}erences relative toNC subjects[

For NC subjects\ the lack of di}erence between rec!ognition of items in list 0 or 1 and the superior recognitionof these 1 lists compared to list 3 indicates that they madeuse of the semantic relationship to encode stimuli[ Scoresof items recognition in list 2 and 3 actually did not di}ersigni_cantly\ suggesting that encoding based on per!ceptual cues is less e.cient than encoding based on sem!antic cues[ However\ the lack of signi_cant di}erencebetween recognition of stimuli from either list 0 or 1 and

stimuli of list 2\ also suggests that NC subjects bene_tedto the same extent of perceptual and semantic encoding[Another explanation is however possible\ namely\ thatNC probably resorted to abstract conceptual knowledge\stored within semantic memory\ to make the requiredphysical comparisons of size between pictures[

The results obtained in AD patients show that\ at earlystages of the disease\ they can make use of what is pre!served of their semantic knowledge to encode picturedstimuli\ inducing higher recognition memory scores inthe semantic encoding condition\ in agreement withresults from Dalla Barba and Goldblum ð09Ł[ The superi!ority of recognition of semantically encoded items overperceptually encoded items replicates results from DallaBarba et al[ ð8Ł in aphasic patients and provides somefurther evidence that it is the deeper semantic processing\rather than a general attentional mechanism\ which isresponsible for a higher performance in the recognitionmemory task\ since in both conditions AD patients wereexplicitly asked to pay attention and focus on relation!ships between to be recognized items[

Moreover\ as found in previous studies ð8\ 09Ł onlypatients with relatively good abilities at semantic enco!ding "SM¦# obtained a signi_cantly higher recognitionmemory for list 1[

These results\ together with the correlation betweenrecognition of items in List 1 and the Wechsler Memoryscore of the patients\ are in agreement with the as!sumption that episodic memory depends largely onthe integrity of semantic memory[ Findings by Pattersonand Hodges ð20Ł\ although obtained on a short termmemory task\ are also compatible with this assumption[They tested three patients with impaired semantic mem!ory on a repetition task of lists of words chosen indi!vidually for each case on the basis of their beingsemantically preserved "{{known|| words# or impaired"{{unknown|| words#[ As a consequence of this {{criticalmanipulation|| ð20Ł\ these patients who had largely intactsingle word repetition and digit span\ showed a dramaticdissociation in repetition of {{known|| words that wasrelatively good\ and {{unknown|| words which gave riseto very poor performance[

However\ two _ndings from the present study needfurther consideration[ First\ the correlation between theRey _gure copy scores\ the perceptual encoding and rec!ognition of items encoded this way "list 2# but alsothrough semantic association "list 1#\ corroborates "withrespect to the correlation between the Rey _gure copyand the semantic association scores#\ that AD subjectsmay be over!relying on perceptual attribute processing\even though they can make use of their semantic knowl!edge to encode pictured stimuli\ as discussed above[Second\ the recognition of items from list 2\ after per!ceptual encoding\ was signi_cantly superior to items fromlist 3 and marginally signi_cant to items from list 0\whereas no di}erence emerged from recognition of itemsfrom both lists for which no cue to encoding was provided"lists 0 and 3#[

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The pro_le on the recognition memory task of thesubgroups de_ned according to their preserved semanticabilities during the encoding phase\ together with thepositive correlation between Verbal Fluency scores andrecognition of items from list 0 suggest explanations forthese facts[ However\ because of the small sample size ofthe subgroups\ these explanations can only be tentative[

As illustrated in Fig[ 3 our group with relatively pre!served semantic abilities does not appear homogeneous[Like NC subjects\ some AD patients with relatively intactSemantic memory "SM¦# may consult conceptual sem!antic knowledge while making association along per!ceptual attributes of items in list 2\ and also whenpresented with items from list 0 for which semantic pro!cessing was not explicitly required[ Actually these pat!ients correspond to SM¦ VF¦[ Other AD patients withrelatively intact semantic memory "SM¦ VF−# only usetheir relatively preserved semantic abilities wheninstructed to do so\ and thus\ whereas they obtain com!parable scores to the SM¦ VF¦ patients on the rec!ognition of items from list 1\ they obtain scorescomparable to the SM− group in every other condition[

This raises the crucial question of {{purity|| of mostcognitive tests[ Verbal ~uency is considered as a sensitivetest to detect semantic memory de_cits in early dementiaof Alzheimer type ð11\ 16Ł\ but also as a test sensitive tofrontal lesions ð15Ł[ This latter possibility implicates thatSM¦ VF− patients may represent AD patients that are\because of a larger\ or earlier\ dysfunction of frontallobes\ unable to spontaneously resort to otherwise pre!served semantic knowledge[ The small sample size of thesubgroups in our population and the absence of othermeasures of frontal involvement do not permit to estab!lish the basis of the di}erent pro_les associated with thedegree of verbal ~uency impairment[ Further researchassociating neuropsychological assessment and neuro!imaging data may allow to determine whether verbal~uency impairment is {{only|| a sign of increasing severityof the semantic memory impairment\ or point to a sub!group of AD patients that may include frontal lobeimpairment in the beginning stage of the disease[

Acknowlede`ments*This research was supported by the villad|Epidaure and the AGIRC retirement agency[ The authors aregrateful to Angela Kunhel and Anne Petrov for the revision ofthe English manuscript\ to Dr Agne�s Michon\ Dr Henda Tounsiand Danie�le Parisot for their assistance in patients selection andexamination and to Latchezar Traykov\ Bernard Pillon and totwo anonymous reviewers for their helpful advice andcomments[

References

0[ Baddeley\ A[ D[\ Neuropsychological evidence andthe semantic:episodic distinction[ The Behavioral andBrain Sciences\ 0873\ 6\ 127Ð128[

1[ Baddeley\ A[ D[\ Cognitive Psychology and humanmemory[ Trends in Neuroscience\ 0877\ 00\ 065Ð070[

2[ Benton\ A[ L[\ DesHamsher\ K[ S[\ Varney\ N[ R[and Spreen\ O[\ Visuospatial judgment[ A clinicaltest[ Archives of Neurolo`y\ 0867\ 24\ 253Ð256[

3[ Chan\ A[ S[\ Butters\ N[ and Salmon\ D[ P[\ Thedeterioration of semantic networks in patients withAlzheimer|s disease] A cross sectional study[ Neu!ropsycholo`ia\ 0886\ 24\ 130Ð137[

4[ Chertkow\ H[ and Bub\ D[\ Semantic Memory Lossin Alzheimer!type Dementia[ In Modular De_cits inAlzheimer!type Dementia\ ed M[ F[ Schwartz[ MITPress\ Cambridge\ 0889\ pp[ 196Ð133[

5[ Craik\ F[ I[ M[ and Jennings\ J[ M[\ Human Memory[In The Handbook of A`in` and Co`nition\ eds F[ I[M[ Craik and T[ A[ Salthous[ Lawrence Erlbaum\Hillsdale\ NJ\ 0871\ pp[ 40Ð009[

6[ Dalla Barba\ G[\ Confabulation] knowledge and rec!ollective experience[ Co`nitive Neuropsycholo`y\0882\ 09\ 0Ð19[

7[ Dalla Barba\ G[\ Cipolotti\ L[ and Denes\ G[\ Auto!biographical memory loss and confabulation in Kor!sako}|s syndrome] a case report[ Cortex\ 0889\ 15\414Ð423[

8[ Dalla Barba\ G[\ Frasson\ E[\ Mantovan\ M[ C[\Gallo\ A[ and Denes\ G[\ Semantic and episodicmemory in aphasia[ Neuropsycholo`ia\ 0885\ 23\ 250Ð256[

09[ Dalla Barba\ G[ and Goldblum\ M[!C[\ The in~uenceof semantic encoding on recognition memory inAlzheimer|s disease[ Neuropsycholo`ia\ 0885\ 23\0070Ð0075[

00[ De Renzi\ E[\ Liotti\ M[ and Nichelli\ P[\ Selectivesemantic amnesia with preservation of auto!biographical memory[ Cortex\ 0876\ 12\ 464Ð486[

01[ De Renzi\ E[ and Vignolo\ L[ A[\ The Token Test]a sensitive test to detect receptive disturbances inaphasics[ Brain\ 0851\ 74\ 554Ð567[

02[ Desgranges\ B[\ Eustache\ F[\ Rioux\ P[\ de LaSayette\ V[ and Lechevalier\ B[\ Memory disorders inAlzheimer|s disease and the organization of humanmemory[ Cortex\ 0885\ 21\ 276Ð301[

03[ Folstein\ M[ F[\ Folstein\ S[ E[ and McHugh\ P[R[\ {{Mini!Mental State||] A practical method forgrading the mental state of patients for the clinician[Journal of Psychiatric Research\ 0864\ 01\ 078Ð087[

04[ Grier\ J[ B[\ Non!parametric indexes for sensitivityand bias] Computing formulas[ Psycholo`ical Bull!etin\ 0860\ 64\ 313Ð318[

05[ Hachinski\ V[ C[\ Ili}\ L[ D[\ Zilhka\ E[\ Du Boulay\G[ H[\ McAllister\ V[ L[\ Marshall\ J[\ Russell\ R[ W[R[ and Symon\ L[\ Cerebral blood ~ow in dementia[Archives of Neurolo`y\ 0864\ 21\ 521Ð526[

06[ Hodges\ J[ R[\ Patterson\ K[ and Tyler\ L[ K[\ Lossof semantic memory] implications for the modularityof mind[ Co`nitive Neuropsycholo`y\ 0883\ 00\ 494Ð431[

07[ Hodges\ J[ R[\ Patterson\ K[\ Oxbury\ S[ and Funnell\E[\ Semantic dementia] progressive ~uent aphasiawith temporal lobe atrophy[ Brain\ 0881\ 004\ 0672Ð0795[

08[ Hodges\ J[ R[ and Patterson\ K[ Is semantic memoryconsistently impaired early in the course of Alzh!

M[!C[ Goldblum et al[:Recognition memory in Alzheimer|s disease 618

eimer|s disease< Neuroanatomical and diagnosticimplications[ Neuropsycholo`ia\ 0884\ 22\ 330Ð348[

19[ Howard\ D[ and Patterson\ K[\ Pyramids and PalmTrees] A test of semantic access from pictures andwords[ Thames Valley Publishing Company\ Bury StEdmunds\ 0881[

10[ Kinsbourne\ M[ and Wood\ F[\ Short!term memoryprocesses and the amnesic syndromes[ In Short!termmemory\ eds D[ Deutsch and J[ A[ Deutsch[ Aca!demic Press\ New York\ 0864[

11[ Martin\ A[ and Fedio\ P[\ Word production and com!prehension in Alzheimer|s disease] The breakdownof semantic knowledge[ Brain and Lan`ua`e\ 0872\08\ 013Ð030[

12[ Martin\ A[\ The search for the neuropsychologicalpro_le of a disease state] A mistaken enterprise< Jour!nal of Clinical and Experimental Neuropsycholo`y\0877\ 09\ 11Ð12[

13[ Martin\ A[\ Brouwers\ P[\ Lalonde\ F[\ Cox\ C[ andFedio\ P[\ Alzheimer|s patients subgroups] Quali!tatively distinct patterns of performance and sub!sequent decline[ Centre for Brain Sciences andMetabolism Charitable Trust\ Cambridge\ MA\0876[

14[ McKhann\ G[\ Drachman\ D[\ Folstein\ M[\ Katz!man\ R[\ Price\ D[ and Stadlan\ E[ M[\ Clinical diag!nosis of Alzheimer|s disease] report of the NINCDS!ADRDA Work Group under the auspices of theDepartment of Health and Human Services TaskForce on Alzheimer|s Disease[ Neurolo`y\ 0873\ 23\828Ð833[

15[ Milner B[\ Interhemispheric di}erences in the local!ization of psychological processes in man[ BritishMedical Bulletin\ 0860\ 16\ 161Ð166[

16[ Monsch\ A[ U[\ Bondi\ M[ W[\ Butters\ N[\ Salmon\D[ P[\ Katzman\ R[ and Thal\ L[ J[\ Comparison ofverbal ~uency tasks in the detection of dementia ofthe Alzheimer type[ Archives of Neurolo`y\ 0881\ 38\0142Ð0147[

17[ Montanes\ P[ and Goldblum\ M!C[\ Classi_cationde_cits in Alzheimer|s disease with special referenceto living and nonliving things[ Brain and Lan`ua`e\0885\ 43\ 224Ð247[

18[ Murdoch\ B[ E[\ Chenery\ H[ J[\ Wilks\ V[ andBoyles\ R[ S[\ Language disorders in dementia of theAlzheimer type[ Brain and Lan`ua`e\ 0899\ 20\ 011Ð026[

29[ Osterrieth\ P[\ Le test de copie d|une _gure complexe]contribution a� 0|e�tude de la perception et de lame�moire[ Archives de Psycholo`ie\ 0876\ 29\ 195Ð245[

20[ Patterson\ K[ and Hodges\ J[ R[\ Loss of word mean!ing] implications for reading[ Neuropsycholo`ia\0881\ 29\ 0914Ð0939[

21[ Raven\ J[ Pro`ressive Matrices[ Traduction francžaisede A[ Schutzenberger et D[ Mavre�[ France\ E[ A[ P[0870[

22[ Sheridan\ J[ and Humphreys\ G[ W[\ A verbal!sem!antic category!speci_c recognition impairment[ Co`!nitive Neuropsycholo`y\ 0882\ 09\ 032Ð073[

23[ Sherry\ D[ F[ and Shacter\ D[ L[\ The evolution ofmultiple memory systems[ Psycholo`ical Review\0876\ 83\ 328Ð343[

24[ Shimamura\ A[ P[\ Disorders of memory] the cog!nitive science perspective[ In Handbook of Neu!ropsycholo`y\ Vol[ 2[ eds F[ Boller and J[ Grafman[Memory and its disorders\ ed[ L[ Squire[ Elsevier\New York\ 0878\ pp[ 24Ð62[

25[ Snodgrass\ J[ and Vanderwart\ M[\ A standardisedset of 159 pictures] Norms for name agreement\image agreement\ familiarity\ and visual complexity[Journal of Experimental Psycholo`y] Human Learn!in` and Memory\ 0879\ 5\ 063Ð104[

26[ Squire\ L[\ Memory and brain\ Oxford UniversityPress\ New York\ Oxford\ 0876[

27[ Tulving\ E[\ Elements of episodic memory[ UniversityPress\ Oxford\ 0872[

28[ Tulving\ E[ Pre�cis of elements of episodic memory[The Behavioral and Brain Science\ 0873\ 6\ 112Ð157[

39[ Tyrrel\ P[ J[\ Warrington\ E[ K[\ Frackowiak\ R[ S[J[ and Rossor\ M[ N[\ Heterogeneity in progressiveaphasia due to focal cortical atrophy[ A clinical andPET study[ Brain\ 0889\ 002\ 0210Ð0225[

30[ Wechsler\ D[ Manuel de 0|e�chelle clinique de me�moirede D[ Wechsler[ Les e�ditions du Centre de Psy!chologie Applique�e[ 0858[

31[ Weingartner[ H[\ Grafman\ J[\ Boutelle\ W[\ Kaye\W[ and Martin\ P[ R[\ Forms of memory failure[Science\ 0872\ 110\ 279Ð271[

32[ Wood\ F[\ Ebert\ V[ and Kinsbourne\ M[\ The epi!sodic!semantic distinction in memory and amnesia]clinical and experimental observations[ In HumanMemory and Amnesia\ ed[ L[ S[ Cermak[ LawrenceErlbaum\ Hillsdale\ NJ\ 0871\ pp[ 056Ð082[