Long-term memory in mental retardation: Evidence for a specific impairment in subjects with Down's syndrome

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Pergamon

PII] S9917Ð2821"85#99944Ð2

Neuropsycholo`ia\ Vol[ 24\ No[ 0\ pp[ 60Ð68\ 0886 Copyright Þ 0885 Elsevier Science Ltd[ All rights reserved Printed in Great Britain 9917Ð2821:86 ,06[99¦9[99

Long!term memory in mental retardation] Evidence for a speci_c impairment in subjects with Down|s syndrome GIOVANNI A[ CARLESIMO\% LUIGI MAROTTA$ and STEFANO VICARI$% Clinica Neurologica\ Universita di Roma\ Tor Vergata\ Italy^ $IRCCS Ospedale Pediatrico Bambino Gesu\ Santa Marinella\ Rome\ Italy^ %IRCCS S[ Lucia\ Rome\ Italy "Received 04 January 0885^ accepted 8 May 0885#

Abstract*This study aimed at investigating long!term memory functioning in Down|s syndrome subjects "DS# as compared to individuals with mental retardation of di}erent etiology "MR# and mental!age matched normal children "MA#[ For this purpose\ tests of verbal and visuo!perceptual explicit memory and a verbal repetition priming task were administered to 04 DS\ 04 MR and 29 MA subjects[ Our results document comparable verbal priming in the three groups[ As for explicit memory\ normal children performed better than MR individuals\ and these\ in turn\ better than DS subjects[ Compared to MR subjects\ DS subjects were particularly de_cient in organizing verbal material according to its categorical structure and in actively retrieving stored information[ These results support a view positing heterogeneity of neuropsychological de_cits across distinct etiology MR groups[ Copyright Þ 0885 Elsevier Science Ltd[ Key Words] long!term memory^ mental retardation^ Down|s syndrome[

list recall ð32\ 34Ł and word!pair learning tasks ð07Ł\ other studies have found reduced primacy e}ect in word!list recall ð35Ł\ de_cient learning of new associations ð00\ 17Ł and poor retrieval of visuo!spatial information ð7Ł in MR individuals[ Parallel to uncertainties regarding the overall level of memory performance\ studies concerned with the qualitative aspects of memory impairment in MR subjects have also provided discrepant results[ Thus\ while Rossi ð39Ł described a reduced level of semantic clustering in a task of free recall of related word lists in MR subjects\ subsequent studies reported comparable clustering in MR and MA groups ð34\ 47Ł[ Moreover\ in a study based on multiple recall trials following the single presentation of related and unrelated word lists\ Winters and Semchuk ð47Ł demonstrated comparable improve! ment passing from recall of uncategorized to categorized lists in MR and MA groups but signi_cantly greater forgetfulness in MR than in normal children passing from the third to the fourth recall trial "intertrial delay] 2 days#[ Among the possible explanations for discrepant results obtained by various authors "e[g[ methodological di}er! ences in testing instruments used\ dissimilar levels of men! tal retardation#\ a relevant one is the heterogeneity of etiological groups included in the di}erent MR samples[ In e}ect\ despite the large amount of experimental work

Introduction Long!term memory "LTM# functioning in individuals with mental retardation "MR# has been extensively inves! tigated[ Studies in which MR patients have been com! pared with chronological age!matched subjects "CA# have consistently documented impaired memory per! formance in the MR group ð08\ 49Ł[ However\ the relative contribution of encoding\ storage and retrieval de_cits to the LTM dysfunction of MR subjects is still a matter of debate[ Thus\ while reduced elaborative encoding of incoming information has been most frequently emphas! ized as the critical de_cit of MR people ð34\ 44Ł\ de_cient long!term consolidation of the memory trace "ð20Ł^ but see ð24Ł#\ as well as di.culty in the active retrieval of stored information ð47Ł have also been described[ Overall\ studies comparing memory performances of MR individuals with those of mental age!matched "MA# normal children have produced far less consistent results[ While some authors have documented comparable per! formances of MR and MA normal individuals on word!  Address for correspondence] Giovanni A[ Carlesimo\ IRCCS S[ Lucia\ V[ Ardeatina\ 295\ 99068 Rome\ Italy^ tel[] 90028 5 404900^ fax] 90028 5 4921986[

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on LTM functioning in mental retardation\ only sporadic attempts have been made to look for possible qualitative di}erences in the memory pro_le of distinct MR eti! ological groups ð7Ł[ This lack of interest likely re~ects a general skepticism about the possibility of showing behavioral di}erences characterizing various MR eti! ological groups ð07\ 19Ł[ However\ recent evidence sug! gests that\ when appropriately investigated\ qualitative di}erences between cognitive performances of di}erent MR groups are likely to emerge[ Presumably due to the high incidence of the genetic syndrome\ the MR eti! ological group most extensively investigated in order to show possible qualitative peculiarities in memory pro_le is represented by Down|s syndrome "DS# subjects[ In particular\ a number of studies concerned with short! term memory abilities have documented that DS subjects could be di}erentiated from other MR etiology groups for reduced verbal span ð5\ 23Ł\ a lack of modality and phonological similarity e}ects in verbal span ð23\ 40Ł and for particularly impaired performances when the task calls for a backward recall of verbal and spatial sequences ð42Ł[ The main aim of the present study was to compare LTM performances of samples of DS and di}erent eti! ology MR subjects with those of a group of MA normal children in order to reveal possible qualitative pec! uliarities characterizing the memory pro_le of DS pati! ents[ Since\ to the best of our knowledge\ this is the _rst neuropsychological approach for investigating LTM in DS subjects\ the present research was conceived as a pilot study\ and no particular prediction has been advanced about possible di}erences in the memory pro_le of DS compared to other etiology MR groups[

Neuropsychological battery According to current conceptualizations distinguishing di}erent components in the LTM structure ð31\ 36Ł\ the battery included tests for the assessment of implicit memory "stem com! pletion#\ episodic memory for verbal material "free recall and yes:no recognition for lists of related and unrelated words\ prose recall# and episodic memory for visuo!perceptual material "reproduction of Rey|s Figure Form B#[

Stem completion Forty words\ each of four to 00 letters in length\ were selected[ The frequency of occurrence of these words in Italian primary school textbooks ranged from one to 00 with a mean of 1[5 per million ð3Ł[ The stem "i[e[ the _rst three letters# of each word was unique among the 39 words and constituted the beginning of at least 09 entries in Zingarelli|s Dictionary ð59Ł[ The 39 words were divided into two lists to create two di}erent test forms[ The two 19!word sets were comparable for the frequency of occurrence and word length[ A 19!word list was presented to each patient in an initial study phase and in the subsequent stem completion "targets#\ and the other list was presented only in the stem completion task "foils#[ The 19!word sets were counterbalanced across patients so that each set appeared as often as a target or foil list[ All stimuli were printed individually on index cards[ During the study phase\ patients were told that they would see a series of words presented one at a time on the index cards and that they were to rate each word according to how much they liked or disliked it[ Each word was presented for 4 sec[ If the subject had problems in reading\ the examiner read the words for him[ During the test phase\ which immediately fol! lowed the study phase\ 39 three!letter word stems were pre! sented one at a time on the index cards[ Since the aim of this test is to evaluate the in~uence of prior exposure to a word list on a subsequent completion test in the absence of explicit recollection of the previous study phase\ patients were asked to complete each stem with the _rst word that came to mind[ Once again\ if the subject was not able to read\ the examiner read the stems for him[

Material and methods Word!list learning Subjects Fifteen persons with Down|s syndrome "eight males\ seven females# and 04 persons with non!Down|s syndrome mental retardation without speci_c etiologies "six males\ nine females#\ with a mean chronological age of 05[6 "S[D[ 2[9# and 06[0 "S[D[ 1[4#\ respectively and a mean mental age of 8[0 "S[D[ 1[4# and 8[6 "S[D[ 1[0# years respectively\ were included in our study[ Mental age was determined by Wechsler intelligence scales "WISC!R or WAIS depending on the chronological age#[ All subjects with DS had a karyotype with a free trisomy 10[ To exclude cases with focal brain lesions or psychiatric pathologies\ both DS and MR subjects were selected from a larger sample on the basis of the following criteria] normal birth record\ no history of seizures\ no neurosensorial de_cits "visual or acous! tic#\ no evidence of focal neurological signs\ or endocrine patho! logies and no psychosis or behavioral abnormalities at the time of the study[ All subjects lived with their own families and\ at the time of the study\ they were not attending any speci_c rehabilitative program[ Thirty normally developing children "06 males\ 02 females#\ matched with MR and DS subjects on the basis of their MA\ were selected to form the control group[

Two lists of words "semantically related and unrelated# were selected[ The _rst list was composed of 01 unrelated nouns of concrete objects[ The frequency of occurrence of these words in italian primary school textbooks ranged from _ve to 67 with a mean of 29[6 per million ð3Ł[ The second list was composed of 01 words\ four for each of three semantic categories "animals\ fruits\ body parts#[ The frequency of occurrence in this case ranged from one to 45 with a mean of 05[4 per million ð3Ł and was similar across categories[ For each list\ the test consisted of _ve consecutive immediate free!recall trials\ followed by a 04!min delayed recall trial[ On the _rst immediate trial\ the 01 words were presented orally by the examiner at a rate of one per second[ Immediately following presentation\ subjects were asked to recall as many words as possible[ The same word list was used in the additional four learning trials[ Fifteen minutes after the _fth immediate recall trial\ subjects were again asked to recall as many words on the list as possible "delayed recall#[ A yes:no reco`nition test was given only for the unrelated word list\ 04 min later[ This test explores the subject|s ability to discriminate 01 previously studied words from 01 unstudied words on a 13!word list read by the examiner[

G[ A[ Carlesimo et al[:LTM in Down|s syndrome Half of the subjects were administered the unrelated list _rst and then the related one^ word!lists were administered in the reverse order to the remaining subjects[

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signi_cant ðF9[5 with 1\46 d[f[Ł\ in this way\ docu! menting comparable priming in the three groups of pat! ients "¦2[1\ ¦3[4 and ¦3[9 in the DS\ MR and MA controls\ respectively#[

Prose recall A short story ð33Ł was read by the examiner[ The subject was asked to recall the story immediately after presentation "immediate recall# and after a 04!min interval "delayed recall#[ Performance scores were given according to the number of informative units reported "max7#[

Word!list learning Several memory indexes can be derived from the word! list memory tasks adopted in the present study[ They are analyzed separately in the following subsections[

Rey|s Figure Form B reproduction

Overall performance level The test ð27Ł consisted of a free!hand copy\ followed by an immediate and a delayed "04!min later# memory reproduction without representation[

Results

The mean number of words recalled by the three groups in the _ve consecutive immediate recall trials of the related and unrelated word lists "Fig[ 1# were analyzed by means of a three!way mixed ANOVA with group as a between factor and type of list "related and unrelated#

Stem completion For each subject\ the number of stems completed with words from the experimental list was computed as a func! tion of the study condition[ These data "Fig[ 0# were submitted to a two!way mixed ANOVA with group "DS\ MR\ and MA children# as between!factor and study con! dition "unstudied and studied words# as within!factor[ Results revealed a nonsigni_cant group e}ect ðF0[5 with 1\46 d[f[Ł\ because a similar number of stems was completed with words from the experimental list "both studied and unstudied# in the DS "7[0#\ MR "8[8#\ and control "8[7# groups[ However\ the main e}ect of the study condition was highly signi_cant ðF73[9^ P³9[990 with 0\46 d[f[Ł\ thus revealing a robust priming e}ect[ Finally\ the group×study condition interaction was not

Fig[ 1[ Word!list learning] immediate and delayed recall of related and unrelated lists by DS\ MR and MA subjects[

Fig[ 0[ Stem completion task] completion of stems with words of the experimental list as a function of the study condition "studied vs unstudied word# by DS\ MR and MA subjects[

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and trial "from 0 to 4# as within factors[ The main e}ect of group was signi_cant ðF04[5^ P³9[990 with 1\46 d[f[Ł[ Planned comparisons revealed that the average recall in each trial for DS subjects "4[3# was less than for MR subjects "6[9# ðF7[5^ P³9[90 with 0\46 d[f[Ł who\ in turn\ recalled less than MA controls "7[0# ðF3[7^ P³9[94 with 0\46 d[f[Ł[ The Type of list e}ect was also signi_cant ðF03[1^ P³9[990 with 0\46 d[f[Ł\ due to the better average recall from the related "6[1# than from the unrelated "5[4# list[ The signi_cant trial e}ect ðF041[6^ P³9[990 with 3\117 d[f[Ł was an expression of the learn! ing curve passing from the _rst to the _fth recall trial[ The group×type of list interaction approached signi_cance ðF1[7^ P9[96 with 1\46 d[f[Ł[ In e}ect\ while MR sub! jects recalled signi_cantly more words from the related "6[6# than from the unrelated "5[3# list on the average in each trial ðF02[1^ P³9[99 0 with 0\46 d[f[Ł\ the same was not true for DS "4[6 vs 4[0# and MA normal children "7[1 vs 6[8# ðF1[4 and 0[0\ respectivelyŁ[ The remaining group×trial ðF9[8Ł\ type of list×trial ðF0[1Ł and group×type of list×trial ðF9[7Ł interactions were not signi_cant[ The for`ettin` rate passing from immediate to delayed recall of both the related and unrelated lists "Fig[ 1# was investigated by another three!way group×type of list×trial "_fth immediate and 04? delayed# mixed ANOVA[ In this analysis\ only the group ðF00[6^ P³9[990 with 1\45 d[f[Ł and the trial ðF17[2^ P³9[990 with 0\45 d[f[Ł e}ects were signi_cant\ thus documenting di}erent levels of overall recall in the three groups "plan! ned comparisons^ MA×MR×DS subjects^ P³9[94 in all comparisons# and a signi_cant memory decay passing from the last immediate to the delayed recall trial[ However\ no interaction between main factors was sig! ni_cant ðF consistently ³0[7Ł\ in this way demonstrating comparable forgetting rates in the three groups[ In the yes:no reco`nition task for the unrelated list\ the MA control group obtained signi_cantly more hit!rates "00[4# and less false alarms "9[0# than the MR "09[2 and 0[6# and DS "09[1 and 1[7# groups ðF consistently ×3[9Ł[ Performance levels of the MR and DS groups\ instead\ did not di}er reliably ðF9[0 and 0[6 for the hit rates and false alarms\ respectivelyŁ[

recall level\ the number of categories that the subject recalls and the distribution of the total items recalled across categories[ In the ARC score\ chance clustering is set at 9 and perfect clustering at 0[ The computational formula for the ARC score is] ARC 

R−E"R# \ max R−E"R#

where R is the total number of clusters "i[e[ the number of times a category item follows an item from the same category#\ E"R# is the expected "chance# clustering based on the number of words recalled and max R "computed as the di}erence between the number of items recalled and the number of categories represented in the recall protocol# is a measure of perfect clustering behavior "i[e[ the maximum possible number of clusters for the number of words recalled#[ As shown in Fig[ 2\ MR subjects clustered items during the _ve immediate recall trials consistently better than MA controls[ However\ in neither group was there a clear progression of the ARC score in successive recall trials[ The clustering behavior of DS subjects was less regular\ with the ARC score alternating negative and positive peaks[ A group×trial two!way mixed ANOVA revealed a di}erence between groups that was close to signi_cance ðF1[4^ P9[98 with 1\46 d[f[Ł[ Planned comparisons showed a signi_cantly higher ARC score in the MR "¦9[02# than in the MA "−9[90# group ðF3[8^ P³9[94 with 0\46 d[f[Ł but no di}erence between DS "¦9[92# and the MA and MR subjects ðF9[1 and 1[2\ respectivelyŁ[ Finally\ neither the trial e}ect ðF0[5 with 3\117 d[f[Ł nor the group×trial interaction ðF0[9 with 7\117 d[f[Ł approached signi_cance[

Serial position curve in the immediate recall of the unrelated list The serial position curve in the free recall of unrelated supraspan word lists is a largely documented phenom! enon in the experimental study of memory[ Typically\

Semantic clustering in the immediate recall of the related list Besides the gain in overall recall passing from the unre! lated to the related word list\ another way of evaluating the ability to take advantage of the semantic relatedness between words on the list to improve recall is to analyze the clustering behavior for the categorized list[ We adopted the adjusted ratio of clustering "ARC# score developed by Roenker et al[ ð28Ł as a measure for the estimation of semantic clustering[ The ARC is preferable to other clustering measures ð4\ 6Ł because it provides an estimate of clustering that is independent of the overall

Fig[ 2[ Adjusted ratio of clustering in the immediate recall trials of the related word!list by DS\ MR and MA subjects[

G[ A[ Carlesimo et al[:LTM in Down|s syndrome

when the number of items correctly recalled are plotted as a function of their positions on the list\ a U!shaped curve is obtained with the _rst and last items of the list best recalled ð11\ 12Ł[ It is generally agreed that the elevation of the early part of the curve "primacy effect# is due to the fact that initial items on a list bene_t from more extensive rehearsal than subsequent items and\ as a consequence\ have a higher probability of being stored in LTM ð30Ł[ The mid!list items form the asymptotic part of the curve and are generally considered a reliable index of the ability to store new items in LTM ð46Ł[ The interpret! ation of the enhanced recall of terminal items "recency effect# is more controversial "for reviews\ see ð0\ 01\ 11\ 16\ 44Ł#[ According to many authors ð11\ 12\ 21\ 44Ð 46Ł\ the recency e}ect represents the output of a limited capacity\ transitory\ short!term memory store[ According to others ð13Ð15Ł\ the recency e}ect actually arises from the adoption of a positional retrieval strategy "favoring _nal list items# applied to items stored in LTM[ The serial position curves for DS\ MR and MA control subjects "Fig[ 3# were constructed by computing the sum of words recalled from each serial position of the word lists across the _ve immediate recall trials[ An exam! ination of the serial position curve of the whole group revealed that the U!shaped curve reached and maintained its asymptote at positions 3Ð6[ Accordingly\ we collapsed positions 0Ð2\ 3Ð6 and 7Ð01 to form the primacy\ the mid!list and the recency tracts of the curve\ respectively[ For statistical purposes\ primacy\ mid!list and recency scores were calculated as the average of recall scores from the respective serial positions[ These data were submitted to a two!way mixed ANOVA with group as the between factor and serial position "primacy\ mid!list and recency tracts# as the within factor[ The main group e}ect was signi_cant ðF04[2^ P³9[990 with 1\46 d[f[Ł[ Planned comparisons revealed better average recall in the MA controls "2[2# than in the DS "1[0# and MR "1[6# groups ðF17[0 and 09[5^ P³9[90 in both cases with 0\46 d[f[Ł[ Comparison between DS and MR groups approached signi_cance ðF2[0^ P9[97 with 0\46 d[f[Ł[ The serial position e}ect was also signi_cant ðF13[5^ P³9[990 with 1\003 d[f[Ł[ Planned comparisons revealed better recall from primacy "2[9# and recency "2[9# than from

Fig[ 3[ Serial position curves in the immediate recall trials of the unrelated word!list by DS\ MR and MA subjects[

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mid!list "1[0# serial positions ðF26[5 and 25[1 respec! tively^ P³9[990 in both cases with 0\46 d[f[# but no di}erence in average recall from primacy and recency tracts ðF9[0 with 0\46 d[f[Ł[ Finally\ the group×serial position interaction was signi_cant ðF1[6^ P³9[94 with 3\003 d[f[Ł[ Planned comparisons made to qualify this interaction revealed a lower recall in DS than in the MA control group irrespective of the tract considered of the serial position curve "P³9[90 in all comparisons#[ MR subjects scored lower than MA controls in the primacy ðF7[0^ P³9[90 with 0\46 d[f[Ł and mid!list tracts ðF01[6^ P³9[990 with 0\46 d[f[Ł but at a level com! parable to that of normal children in the recency tract ðF9[2Ł[ Finally\ MR and DS children were indis! tinguishable for primacy and mid!list tract recall ðF9[0 in both comparisonsŁ\ but MRs recalled signi_cantly bet! ter than DS subjects from the recency tract ðF02[7^ P³9[990 with 0\46 d[f[Ł[

Prose recall Performance scores of the three groups of subjects on the immediate and delayed recall of the short story were analyzed by means of a two!way Group×Trial "immedi! ate and delayed# mixed ANOVA[ The Group e}ect was signi_cant ðF17[6^ P³9[990 with 1\46 d[f[#[ Planned comparisons revealed better overall recall in MA "4[1# than in MR "2[3# subjects ðF7[1^ P³9[9 0 with 1\46 d[f[#[ The latter\ however\ recalled better than the DS subjects "9[5# ðF05[5^ P³9[990 with 1\46 d[f[#[ Neither the Trial e}ect nor the Group×Trial interaction were signi_cant ðF0[8 and 9[7 respectively#\ thus revealing the lack of reliable forgetting passing from immediate "2[1# to delayed recall "1[8# in the whole sample and in the single patients| group[ However\ it should be noted that in the DS sample possible signi_cant forgetting might have been obscured by a ~oor e}ect in the immedi! ate recall performance[

Rey|s Figure Form B reproduction In the copy condition of Rey|s Figure reproduction test\ MA control subjects "15[7# outscored MR subjects "08[5# ðF10[9^ P³9[990 with 0\46 d[f[Ł and the latter\ in turn\ performed better than DS subjects "03[9# ðF8[3^ P³9[90 with 0\46 d[f[Ł[ In order to correct memory per! formances for the constructive abilities of single subjects\ performance scores in the immediate and delayed mem! ory condition were expressed as a percentage of the copy condition[ When these data were analyzed by means of a two!way group×trial "immediate and delayed# mixed ANOVA\ a signi_cant di}erence emerged between groups ðF2[8^ P³9[94 with 1\46 d[f[#[ Planned com! parisons demonstrated that the signi_cance of the group e}ect was actually sustained by a signi_cant di}erence

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between overall performance score of MA "9[71# and DS "9[52# subjects ðF6[2^ P³9[90 with 0\46 d[f[Ł[ The performance of MR subjects "9[61#\ instead\ did not di}er signi_cantly from the other two groups[ The trial e}ect approached signi_cance ðF2[9^ P9[98 with 0\46Ł due to an overall performance decrement passing from the immediate "9[63# to the delayed memory task "9[60#[ Finally\ the group×trial interaction was not sig! ni_cant ðF1[0Ł thus demonstrating a comparable for! getting rate in the three groups of patients[

Discussion The _rst main result of the present study is the de_cient overall level of explicit memory performances in MR individuals as compared to normal children and impaired explicit memory in DS compared to di}erent etiology MR subjects[ This pattern of results "MA×MR×DS# was consistent across modality conditions "verbal and visuo!perceptual# and delay of assessment "immediate and delayed tests#[ The _nding of de_cient episodic mem! ory in MR individuals is consistent with previous results ð7\ 17\ 35Ł\ but is in contrast with other experimental data ð32\ 34Ł[ As noted above\ the discrepancy in the literature likely re~ects the heterogeneity of memory tasks employed in the di}erent studies and the variable etiology of mental retardation a}ecting subjects included in the di}erent experimental samples[ What is new in our study is the particularly de_cient memory performances exhi! bited by DS subjects[ Previous reports had already described a reduced extension of verbal span in DS indi! viduals compared to both MA and di}erent etiology MR individuals ð5\ 23\ 40\ 42Ł[ Our _nding of a de_cient recency e}ect in the recall of supraspan word lists in the DS group con_rms the hypothesis of poor verbal STM in DS individuals[ However\ to the best of our knowledge\ this is the _rst demonstration that de_cient memory in DS extends also to the long!term domain[ A more analytical view of our results provides details about basic mechanisms presumably underlying de_cient memory in MR and DS individuals[ Encoding was inves! tigated by comparing learning of related and unrelated word lists[ In normal adult individuals\ organizational strategies based on the semantic categorization of words to be remembered generally produce better memory for related than for unrelated word lists[ Moreover\ the organizational activity during retrieval of the cat! egorizable list can be objecti_ed by measuring the sem! antic clustering e}ect "by which words belonging to the same category tend to be grouped during free recall# ð26Ł[ Our group of normal children did not show any sem! antic category e}ect[ Not only did they remember as many unrelated as related words\ but their ARC scores on immediate recall trials were consistently below those of the MR group[ Instead\ a semantic e}ect emerged in the performance of the MR group[ These subjects recalled the related list signi_cantly better than the unrelated one

and\ although a clear progression of the ARC was not observed on successive recall trials\ they clustered the related items signi_cantly better than normal MA chil! dren[ Finally\ DS children did not reveal a sure semantic relatedness e}ect[ Their better recall of the related than the unrelated list did not reach statistical signi_cance\ and the irregular pro_le of their ARC curve suggested poor organizational activity in the recall of the cat! egorizable list[ The lack of organizational strategies for word!list recall in 8!year!old normally developing chil! dren is not unexpected[ Spitz ð34Ł has already documented that a clear clustering e}ect in word!list recall does not emerge before 09 years of age[ What was unexpected in our results was the signi_cant e}ect of semantic organ! ization in word!list recall exhibited by the group of MR individuals[ In our opinion\ the better encoding abilities demonstrated in the word!list recall task by retarded ado! lescents compared to normal children underlines the limit of mental age as a unique criterion for matching normal and MR individuals in neuropsychological and behavioral investigations[ Due to the considerable dis! crepancy in their chronological ages\ MR and normal MA matches are in fact strikingly di}erent for years of schooling\ level of personal autonomy and life experi! ences[ This is particularly true in Italy\ where MR chil! dren attend normal schools on the basis of their chronological age[ In our opinion\ the more prolonged exposure to linguistic and academic experiences by retarded adolescents may well account for the more e.cient utilization of semantic strategies in the word!list learning task by the MR than by the MA group[ On the other side\ the fact that DS subjects did not show any signi_cant organizational activity in the word!list recall\ despite being comparable to the unknown etiology MR individuals for mental and chronological ages\ docu! ments a particular di.culty of this etiology group in the use of semantic strategies for improving episodic memory and suggests that reduced semantic elaboration may be at the base of their poor LTM performances[ Consolidation of recently stored memory traces was investigated by analysing the memory decay passing from immediate to delayed recall of the word lists\ the short story and Rey|s _gure[ In all cases\ the forgetting rate was comparable in the three groups of patients\ thus not supporting the hypothesis of an accelerated decay of the memory trace as a possible cause of the memory impair! ment showed by the mentally retarded individuals[ A _nal hypothesis explored in the present study is that MR and DS subjects fail to remember because of a di.culty in deliberately accessing previously stored mem! ory traces[ If this is the case\ then the memory de_cit disclosed by these subjects should be particularly relevant when the memory task requires active recovery of acquired information "as in free recall procedures# but should no longer be observed when retrieval operations are facilitated by the presentation of target and distractor stimuli by the examiner\ and the task is to discriminate previously encountered material from new material "as in

G[ A[ Carlesimo et al[:LTM in Down|s syndrome

recognition procedures#[ Overall\ our data do not support this hypothesis for MR individuals[ Their performance was de_cient compared to MA normal children in both the delayed recall and the recognition conditions of the unrelated word!list test[ DS subjects\ instead\ improved their performance passing from recall to recognition[ In fact\ in the delayed recall test\ they remembered sig! ni_cantly less words than MR subjects\ but in the rec! ognition task\ their performance did not di}er from that of the MR group[ These data seem to suggest that poor memory in DS is due\ at least in part\ to a de_cit in the deliberate retrieval of previously stored memory traces[ A second main result of the present study is the com! parable priming e}ect shown by normal children\ MR and DS individuals in the stem completion task[ These data con_rm and extend to mentally retarded individuals previous _ndings demonstrating the resistance of rep! etition priming to cerebral damage and its substantial independence from explicit memory performances[ In e}ect\ both developmental ð22\ 25Ł and neuro! psychological ð03Ł studies reveal a substantial pres! ervation of the priming e}ect in physiological "childhood and normal aging# and pathological "amnesic syndromes# conditions characterized by de_cient explicit memory[ To summarize\ MR individuals reveal an implicit mem! ory\ as assessed by repetition priming\ adequate to their mental age[ However\ their explicit LTM is de_cient com! pared to MA normal children[ Unfortunately\ our data contribute little toward clarifying the basic mechanisms of their memory impairment[ The forgetting rate passing from immediate to delayed recall as well as the rate of facilitation passing from recall to recognition retrieval procedures were\ in fact\ similar in the two groups[ More! over\ MR individuals took more advantage\ than normal children\ of the opportunity to organize incoming material according to its categorical structure for improv! ing word!list recall[ The only suggestion from our data\ that might contribute to an interpretation of the memory de_cit in MR individuals\ regards the poor primacy e}ect shown by these subjects in the free recall of unrelated word lists "for similar results\ see ð35Ł#[ According to Rundus ð30Ł\ the elevation of the early tract of the serial position curve is actually an expression of the active rehearsal of incoming words while the list is read by the examiner[ Accordingly\ a de_cient active rehearsal of incoming material by MR subjects could facilitate the precocious decay of memorandum from STM rep! resentation\ thus reducing its chances of being transferred to the LTM store[ DS subjects performed explicit memory tasks at a sig! ni_cantly lower level than di}erent etiology MR indi! viduals[ Our data provide some clues about basic mechanisms presumably underlying the memory de_cit in DS individuals[ First\ long!term consolidation of the acquired information does not seem less e}ective in DS than in MR and MA individuals[ Their forgetting rate passing from immediate to delayed recall was\ in fact\ comparable to that of the other two groups[ With respect

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to the di}erent etiology MR group\ DS subjects showed a reduced e.ciency of organizational strategies "no sig! ni_cant improvement passing from recall of unrelated to related word lists and poor clustering# and a reduced ability to actively recover previously stored memory traces "larger facilitation of retrieval passing from free recall to y:n recognition#[ In short\ our data seem to suggest an interaction between poor encoding and retrieval abilities as a possible reason for a LTM de_cit in DS subjects that is disproportionately more severe than that revealed by an unselected group of MR indi! viduals of a comparable mental age[ Complementary to the cognitive approach\ a di}erent perspective for interpreting poor LTM performances exhibited by DS individuals is represented by the analysis of neuropathological changes produced by trisomy 10 in brain regions known to be critical for memory functions[ Classical studies on the amnesic syndrome in adult indi! viduals point to hippocampal and parahippocampal regions ð37Ł and some diencephalic nuclei "particularly mammillary bodies and the medio!dorsal nucleus of the thalamus# ð43Ł as critical areas where lesions can be responsible for the emergence of severe LTM disorders[ Other cerebral regions\ less frequently involved in ante! rograde amnesia\ are the fornix ð09Ł and the nucleus bas! alis of Meynert ð05Ł[ Moreover\ the role of the frontal lobes in speci_c aspects of memory function "such as memory for temporal order\ source memory and the use of organizational strategies in free recall# has been docu! mented more recently ð10Ł[ In e}ect\ both neuro! pathological ð2\ 04Ł and neuroradiological ð1\ 18\ 29Ł investigations of the gross brain morphology in trisomy 10 have documented that\ in the context of an overall reduction of brain volume\ the cerebral regions most obviously hypoplastic in DS subjects are the frontal lobes\ the limbic regions "including the hippocampal and par! ahippocampal structures# and the cerebellum[ Moreover\ microscopic analysis in these subjects has documented a congenital decrease in the total number of neurons in the hippocampus ð38Ł and the nucleus basalis of Meynert ð02Ł[ Finally\ it is well known that the brain of DS individuals is characterized by the precocious appearance of mor! phological alterations similar to those observable in aged normal subjects[ In particular\ the presence of senile pla! ques and neuro_brillary tangles "characterizing the brain of normal individuals over 59 years of age and\ to a large extent\ the brain of Alzheimer|s demented patients# has been described in the hippocampus and neocortex of DS individuals as young as 19 years of age ð8\ 48Ł[ In sum\ although a strict correlation between morphological changes in the brain and memory impairment in DS is not possible on the basis of the available literature\ the above!mentioned congenital alterations of hippocampi\ frontal lobes and nucleus basalis of Meynert and the superimposed premature appearance of microscopic alterations typical of aging could represent the neuro! pathological substrate of the particularly de_cient LTM functions in young DS individuals[

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G[ A[ Carlesimo et al[:LTM in Down|s syndrome

In conclusion\ the results of the present study dem! onstrate that memory impairment in mentally retarded individuals is not simply a function of the severity of learning disability\ but that it a}ects MR individuals to a degree disproportionate to their rate of cognitive development[ Moreover\ our data document that severity and qualitative characteristics of the memory impairment in mentally retarded individuals vary as a function of the etiology[ In particular\ DS individuals displayed sig! ni_cantly lower LTM performances than a group of MR individuals of di}erent etiology that were comparable for severity of learning disability[ These results provide further support for the conceptual framework positing heterogeneity of qualitative characteristics of mental impairment in di}erent etiology MR individuals ð06\ 41Ł and emphasize the relevance of memory investigation as a particularly fruitful approach for the neuropsychological characterization of mental retardation[

02[

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