JOURNAL OF CLINICAL AND EXPERIMENTAL NEUROPSYCHOLOGY2008, 30 (7), 828–835NCENExploring different routes of recovery frommemory in Alzheimer’s disease: Evidencefor preserved long-term primingLong-Term Priming in Alzheimer’s DiseaseXavier Mil<strong>le</strong>t, 1 Mélanie Le Goff, 1 Sophie Auriacombe, 2 Co<strong>le</strong>tte Fabrigou<strong>le</strong>, 1Jean-François Dartigues, 1,2 and Hélène Amieva 11 Inserm U593, Université Victor Sega<strong>le</strong>n, Bordeaux, France2 Memory Clinic, University Hospital of Bordeaux, Bordeaux, FranceDownloaded By: [EBSCOHost EJS Content Distribution] At: 13:32 29 September 2008Studies investigating implicit memory in Alzheimer’s disease suggest that priming abilities disappear over time.This study investigates long-term priming in Alzheimer’s disease. A total of 20 patients with Alzheimer’s diseaseand 20 controls underwent the Free and Cued Se<strong>le</strong>ctive Reminding test. After a 30-minute delay, participantswere submitted to a word identification task comprising the studied words and new words. The patients exhibiteda long-term priming effect similar to that presented by the comparison group. Therefore, whereas explicit retrievalis definitely impaired in Alzheimer’s disease, implicit processes allowing the retrieval of that same informationoperate relatively normally, including after a long delay.Keywords: Implicit memory; Delayed retrieval; Dementia.INTRODUCTIONEpisodic memory decline is considered to be themain neuropsychological marker of Alzheimer’sdisease (AD). To evidence such a deficit, variousverbal memory tasks are availab<strong>le</strong>. Among thesetasks, the Free and Cued Se<strong>le</strong>ctive Reminding(FCSR) test combining free and cued recall trialshas been shown to have good sensitivity to distinguishdementia from normal aging and to predictfuture dementia diagnosis (Grober & Buschke,1987; Grober, Lipton, Hall, & Crystal, 2000). Itsprocedure relies on two conditions known to maximize<strong>le</strong>arning processes—that is, depth of processingand encoding specificity. Depth of processing(Craik & Lockart, 1972) refers to the ability toencode words semantically and generate organizationalstrategies, whi<strong>le</strong> encoding specificity (Tulving& Pearlstone, 1966) is defined by the similaritybetween encoding and recol<strong>le</strong>ction strategies. TheFCSR test involves the semantic categoricalprocessing of the to-be-remembered words duringthe encoding phase. Further, the same semanticcategories as those used during the encoding phaseare provided during retrieval to facilitate recall.The ability to benefit from cues to retrieve the targetwords has been shown to distinguish AD fromage-associated memory deficits (Grober &Buschke, 1987; Grober, Buschke, Crystal, Bang, &Dresner, 1988) and from other dementia syndromes(Pillon, Deweer, Agid, & Dubois, 1993; Pasquier,Grymonprez, Lebert, & Van der Linden, 2001).Because patients suffering Parkinson, Huntington,and frontotemporal dementias improve their performancewith cuing, they are typically diagnosedwith impaired retrieval processes. In contrast,patients with AD not only exhibit strong difficultiesin free recall (Bäckman, Small & Fratiglioni,2001; Grober & Kawas, 1997; Grober et al., 2000;Jones, Livner, & Bäckman, 2006) but also fail toshow much improvement in performances whencues are provided (Buschke, Sliwinski, Kuslansky,The authors thank M. Paccalin, I. Migeon-Dubal<strong>le</strong>t, M.D. Lussier, and V. Cressot for referring patients with Alzheimer’s disease.Address correspondence to Hélène Amieva, Inserm U593, Université Victor Sega<strong>le</strong>n Bordeaux 2, 146, rue Léo Saignat, 33076Bordeaux Cedex, France (E-mail: He<strong>le</strong>ne.Amieva@isped.u-bordeaux2.fr).© 2008 Psychology Press, an imprint of the Taylor & Francis Group, an Informa businesshttp://www.psypress.com/jcen DOI: 10.1080/13803390701819028
Downloaded By: [EBSCOHost EJS Content Distribution] At: 13:32 29 September 2008& Lipton, 1997; Petersen, Smith, Ivnik, Kokmen,& Tangalos, 1994; Tounsi et al., 1999; Traykovet al., 2005). This pattern of performance in ADhas been interpreted as the consequence of encodingprocesses deficiency (Pasquier et al., 2001;Pillon et al., 1993), in accordance with resultsobtained with other memory tests (e.g., Greene,Badde<strong>le</strong>y, & Hodges, 1996).Neverthe<strong>le</strong>ss, considering implicit and explicitfeatures of retrieval may be important to investigatethe nature of memory decline in AD. Whereasexplicit recall refers to conscious and deliberaterecovery of past experiences, implicit recall is characterizedby spontaneous and nonconscious waysto access stored information (Graf & Schacter,1985). In particular, priming phenomena ref<strong>le</strong>ctthe impact of prior experience in the form of processingfacilitation without conscious rememberingof this experience. Among the various priming paradigms,perceptual priming consists in the repetitionof physically identical items and is modalityspecific (Car<strong>le</strong>simo et al., 1999; Verfaellie, Keane,& Johnson, 2000). Numerous studies consistentlyfound a preservation of perceptual repetition primingin AD patients following short delays, particularlyin word identification tasks (F<strong>le</strong>ischman &Gabrieli, 1998; F<strong>le</strong>ischman et al., 1995, 2005;Keane, Gabrieli, Fennema, Growdon, & Corkin,1991; Keane, Gabrieli, Growdon, & Corkin, 1994;Koivisto, Portin, & Rinne, 1996; Russo &Spinn<strong>le</strong>r, 1994).Whi<strong>le</strong> numerous studies addressed short-termpriming in AD, whether such priming effectremains following long-lasting intervals has received<strong>le</strong>ss attention. A few studies using different paradigmscontributed to the suggestion that primingmagnitude in AD patients diminishes over time ata faster rate than in normal elderly adults. The tasksused included homophone spelling (Fennema-Notestine, Butters, Heindel, & Salmon, 1994), nonverbalstimuli discrimination (Heindel, Salmon,Fennema-Notestine, & Chan, 1998), picture naming(Mitchell & Schmitt, 2006), word fragmentcomp<strong>le</strong>tion (Heindel, Cahn, & Salmon, 1997), and<strong>le</strong>xical decision (Schnyer, Al<strong>le</strong>n, Kaszniak, &Forster, 1999) procedures. The delay used also variedsubstantially across the studies. In the metaanalysison implicit memory in AD by Meiran andJelicic (1995), among the 17 studies using wordbasedperceptual priming, only 3 used a study–testdelay longer than 10 minutes. Thus, the authorsconsidered a delay of 10 minutes or more as a longtermdelay. This study–test delay proved to be usefulin evidencing differences between AD and controls,since AD patients’ performances in word-basedperceptual priming only differed from that ofLONG-TERM PRIMING IN ALZHEIMER’S DISEASE 829controls after a 10-minute delay. Nonethe<strong>le</strong>ss,Ostergaard (1994) used a noteworthy long-termpriming procedure in two word identificationtasks. Experimental conditions varied according tothe number of initial exposures with stimuli (onevs. multip<strong>le</strong> exposures) and according to the recalldelay. Whereas repetition priming in AD was compromisedafter a 10-minute delay in the conditioninvolving a sing<strong>le</strong> presentation of the target stimuli,a significant priming effect could be evidencedin the condition involving multip<strong>le</strong> presentations.Thus, repeated exposures with the material duringthe encoding phase appeared to strengthen memorytrace and facilitate incidental retrieval in ADpatients.Therefore, the status of long-term priming abilitiesin AD remains unc<strong>le</strong>ar. In this study, we comparedthe delayed recall performances of mild tomoderate AD patients and elderly controls accordingto different procedures of retrieval. We firstadministered the FCSR test involving three freeand cued recall trials, a recognition task, and adelayed recall. Finally, after an additional 30-minute delay, participants were submitted to acomputerized word identification task that consistedof identifying as quickly as possib<strong>le</strong> a seriesof words comprising the words presented duringthe FCSR test and new words. A 30-minute delaywas used in order to decrease the likelihood ofexplicit contamination in normal controls (e.g.,Toth, Reingold, & Jacoby, 1994). The evidence ofsignificant priming performances in AD patientswould suggest the persistence of a memory traceafter a long-lasting delay.ParticipantsMETHODWe included 20 patients (ages ranged from 60 to84 years) meeting NINCDS-ADRDA (NationalInstitute of Neurological and Communicative Disordersand Stroke–Alzheimer’s Disease andRelated Disorders Association) criteria (McKahnet al., 1984) for probab<strong>le</strong> AD. Characteristics ofthe participants are shown in Tab<strong>le</strong> 1. Patientswith a history of severe head injury (loss of consciousnessfor more than 48 hours), alcoholism,and depressive symptomatology were excluded.All the patients scored 20 or higher in the Mini-Mental State Examination (MMSE; Folstein,Folstein, & McHugh, 1975). We also included 20elderly controls (ages ranged from 60 to 84 years)matched with the AD group for age, sex, and <strong>le</strong>velof education. None of them manifested any sign of
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5. Conclusion généraleCompte tenu
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BIBLIOGRAPHIE102
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York: Cambridge University Press.Ba
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Multidimensional measures of person
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Fox, N.C., Warrington, E.K., Freebo
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Procedural memory in patients with
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625-632). London: Academic Press.La
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Patterson, K., Graham, N., & Hodges
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test: role of aging and divided att
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Epreuve de titresCe travail de thè