A Critical Review of Memory Stimulation Programs in Alzheimer´s Disease

8/13/2019 A Critical Review of Memory Stimulation Programs in Alzheimers Disease

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J Neuropsychiatry Clin Neurosci 15:2, Spring 2003 133

GRANDMAISON et al.

ads for signicant events, active memory recall andrecognition exercises, interpersonal problem-solving sit-uations, and targeted conversation exercises.

Visual ImageryThe use of visual imagery techniques is based on the

concept that visual associations improve the encoding,consolidation, and recall capacities of verbal material because the memory system does not rely on the verbalsemantic mode alone. According to Breuil et al., 44 evenwhen several cognitive functions are compromised inAD, patients are still able to elaborate some cognitivestrategies. Recall failures would occur because the re-trieval strategies are not well applied. Thus, mental im-agery is used to simultaneously stimulate visual andverbal semantic modes to facilitate the encoding, con-solidation, and retrieval capacities in the everyday en-vironment. Since many systems (mainly the visual andverbal semantic systems) are stimulated with visual im-agery, generalization of learning from one environmentto another or from one type of information to anotherhas been hypothesized to occur. 44 Examples of visualimagery include asking a subject to pay attention to spe-cic visual details of the information being learned (fo-cus on facial features, for example) or to form a mentalimage of an object presented in the verbal modality.

Encoding Specicity With Support at RetrievalThese strategies were developed to provide supportiveconditions at both encoding and retrieval phases of ep-isodic learning. The encoding specicity paradigm ne-cessitates the use of similar cues for acquisition (or en-coding) and retrieval, 27,4547 since this paradigm holdsthat the amount of informational overlap between a cuepresented at retrieval and the memory representationestablished at encoding is critical to episodic memoryprociency. 48 In other words, the more congruent a cueis with the context prevailing during encoding or withthe cognitive operations carried at encoding, the moreeffective it will be at retrieval. Early studies have showna modest, almost nonsignicant improvement of recallin subjects with mild and moderate AD when the samesemantic cues were provided by the experimenter at en-coding and retrieval. 45,49,50 The lack of efcacy of the

experimenter-provided semantic cues in subjects withdementia has been attributed to a semantic encodingspecicity decit early in the AD process. 46,47,50 On theother hand, the self-generated cues with encoding-retrieval compatibility have been hypothesized to opti-mize episodic recall in AD because an elaborative activ-ity is taking place at encoding. 51 Self-generated cueingstrategies were then developed to be used similarly atencoding and retrieval: self-generated and semantic

cues, that is, choice of category or description of the itemto be remembered by the subject; 27,52 self-generated andmotor cues, that is, pantomime of the movements as-sociated with the use of the object to be remembered; 26,27

or combinations of these cues. 27 In this paper we reviewonly the articles using self-generated cues.

The Errorless Learning ApproachThe errorless learning approach favors the eliminationor reduction of incorrect or inappropriate responsesduring memory training. 10,53 In other words, using thisparadigm, subjects are not allowed to commit errorswhen they are receiving memory training. This tech-nique was rst designed to facilitate the acquisition of new information in individuals with learning disabili-ties, and it was successfully adapted to memory trainingin subjects who had suffered brain injuries. 10,30,5456

Clare et al. 10 have adapted this method for patients withAD. With errors kept to a minimum during the training,it is hypothesized that interferences in the memorystores will be avoided, which will facilitate the encodingprocess of new information. Learning, retention, and re-trieval should thus be easier. 30 Baddeley and Wilson 30

have shown that errorless learning improves the learn-ing process in subjects withamnesia. The errorless learn-ing training program is often conducted in conjunctionwith the spaced retrieval technique or the vanishingcues technique. In the errorless learning programs, subjects are instructed to say that they do not know an an-swer instead of giving a wrong answer; they are en-couraged not to guess.

The Vanishing Cues TechniqueThe vanishing cues technique consists of several at-tempts to recall information, using prompts that aregradually decreased until recall is successfullyachieved.This method is mainly based on two well-establishedand related principles: the backward chaining proce-dure of behavioral modication 56,57 and some preser-vation of implicit memory in subjects with amnesia. 37

Some authors view the vanishing cues technique as acomplementary method to achieve an errorless learningtraining. 58 An example of the vanishing cues techniqueis to rst present complete words to the subject and then

ask him to say the word when the last letter or last fewletters are missing. Wilson 56 provides the following ex-ample: PEGGY is rst presented, then PEGG_, thenPEG_ _, and so on.

The Spaced Retrieval TechniqueThe spaced retrieval technique or the expanded retrievalpractice involves testing for the repeated recall of newlyacquired information at increasingly longer inter-


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134 J Neuropsychiatry Clin Neurosci 15:2, Spring 2003

MEMORY STIMULATION PROGRAMS IN ALZHEIMERS DISEASE

vals 32,33,59 or with an increasing number of interveningitems. 60,61 This technique is based on experimental evi-dence suggesting that the longer the distracting interval between the rst and the second successful recall, thegreater the likelihood of recall at a third recall attempt. 62

The expanded retrieval practice also potentially contains

a practice effect and therefore implies some preservationof implicit/procedural memory, since the subjects repeatthe same items over different trials. In this method, thesubject is asked to recall the information with increasingnumbers of intervening items (for example, zero, three,. . . nine, and so on interpolated items between recalls of the learned item) or at increasing intervals of time (forexample, 5 seconds, 10 seconds, . . . 60 seconds, and soon after presentation of the item to learn, or 2, 4, . . . 20days after the last test). In terms of the time interval between recalls, the subject has either to reach a prede-termined goal (for example, 60 seconds or 20 days) orto increase the time interval until he or she can no longerrecall the information.

External Memory AidsIt may be difcult for subjects with amnesia to maintainthe use of internal memory strategies, and therefore thepotential of external memory aids might become moreimportant. Indeed, external memory aids have beenwidely used with populations with traumatic brain injury or stroke. 3740,63 Some individuals in the early stagesof AD report an increase in the spontaneous use of sim-ple external memory aids, such as notes they write tothemselves or a calendar they use to remember appoint-ments or to remind them of important dates. Most pa-tients with AD increase their reliance on their caregiversas a form of external memory aid. 64 Using external aidsnevertheless involves memory, especially metamemoryand prospective memory, as well as some executivefunctioning, since the subjects must be aware of theirmemory problems and remember to record informationas well as how and when to access this information. Toovercome these difculties, Hersh and Treadgold 65 de-vised a radio paging system that involves an arrange-ment of microcomputers linked to a conventional com-puter memory and, by modem, to a paging company.Reminders for each individual using the system are en-

tered into the computer and, at the appropriate date andtime, transmitted to an individual alphanumeric pager.An audio or vibration alarm alerts the wearer that thepager contains a reminder of a task to be carried out.The pager is clipped on a waistband or carried in apocket. Until recently, the efcacy of the NeuroPage hadprincipally been studied in subjects with traumaticbraininjury or stroke, 39,63 although one study has reported onuse of technology with AD patients. 10

The Dyadic ApproachIn the dyadic approach, the patients caregiver becomesinstrumental in carrying out different memory and cog-nitive improvement strategies. These strategies are usedfor several purposes: to facilitate the recall of signicantlife events; to improve memory functioning through vi-

sual and verbal mnemonic strategies designed to facili-tate recall and recognition; to improve executive func-tioning through problem-solving exercises usingplanning, conceptualization, and classication withinthe context of interpersonal skills; and to increase socialinteraction by improving communication skills with tar-geted conversation exercises of word uency and verbalexchange. 9 In the reviewed literature, some specicmemory training procedures can be used within the dy-adic approach, but the training and theoretical focus aremore on the patient-caregiver dyad than on the memorysystems.

REVIEW OF THE EVIDENCE ON EFFICACY

We identied 17 articles that pertained to memory im-provement programs used with AD patients. Table 1presents the results obtained with the different memoryremediation programs. One article 10 contained resultson two methods; they are reported separately in the table. Thus Table 1 provides results for 18 different stud-ies. The severity of dementia varied from mild to mod-erate in 17 reviewed studies, 10,26,27,31,4244,51,53,59,6672 withMMSE scores ranging from 9 to 29. Two studies alsoincluded subjects with severe dementia. 26,27 In all stud-ies memory assessments were performed at baseline, be-fore the training took place, both in order to make thediagnosis of dementia and to specically dene thememory problems. However, in most of the studies,these extensive evaluations were not carried out againat the end of the training programs or, if they were, theresults were not provided. Only six studies provideddata on a long-term follow-up extensive memory as-sessment. 10,42,43,53,59,67 None of the patients were re-ported to be on cognition-enhancing drugs in thesestudies.

Visual ImageryThree studies used visual imagerybased mnemonictechniques as memory stimulation programs in demen-tia. 31,44,66 The study by Zarit et al. 31 involved 14 patientswith AD in a didactic visual-imagery training group,11 patients with AD in a problem-solving group, and 10patients with AD in a waiting-list control group. Thepatients were randomly assigned to the treatment andwaiting-list control groups. The training was carried out


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in dyads, in seven 90-minute sessions. The visual im-agery tasks consisted of forming mental images of words that subjects had to remember. The problem-solving tasks consisted of learning how to take practicalsteps to manage day-to-day problems caused by thememory loss. Recall and recognition tasks of 15 items

were used to assess memory at baseline and at the endof the training sessions, along with the Memory and Be-havior Problems Checklist, to assess the impact of thetraining on everyday functioning capacity. The subjectsin the didactic visual-imagery condition signicantlyimproved their recall performance during the trainingsessions, but most of the gains had been lost by the timeof the posttraining assessment. On the recall trials, thesubjects in this group retained a mean of 2.4 of 15 itemsat baseline, a mean of 6.6 items at midtraining, and amean of 2.4 items at posttraining evaluations. On therecognition trials, these subjects retained a mean of 4.7of 15 items at baseline, a mean of 5.7 items at midtrain-ing, and a mean of 5.3 items at posttraining evaluations.Overall, the memory results were mediocre, and the im-pact on everyday functioning capacity was not encour-aging. Using the same measures, no positive effects werenoted in the other two groups. There was no longitu-dinal follow-up to measure long-term retention of theitems.

Backman et al. 66 included eight subjects with AD intheir imagery-based mnemonic training of face-nameassociations. There was no control group. The patientswere given 6 minutes to study pictures of faces pre-sented on cards, and they had to identify a distinctivefacial feature on each card in order to create a visualassociation with the name of the individual shown inthe picture. There was no time limit for the duration of the training. The authors did not provide the total number of pictures presented to each patient. The goal of thestudy was to increase the time that a face-name associ-ation could be held in memory. The authors found thatthe retention time of face-name associations increased inonly one of the eight subjects (from 3 minutes and 30seconds at baseline to 21 minutes and 30 seconds aftertraining). Thus, the outcome of the training was not atall encouraging. No other subjects beneted from thetraining. There was no generalization of the training to

other memory functions as measured by the BostonNaming Test, a word uency task, and the BentonVisualRetention Test, Form A.

The study of Breuil et al. 44 involved 29 subjects withAD in a stimulation group and 27 subjects with AD ina non-stimulation group. The stimulation training wascarried out in 10 sessions each lasting 60 minutes. Theauthors described their method as a global stimulationprogram that relies strongly on mental imagery. Various

perceptual modalities were stimulated through visualimagery and semantic priming. The subjects had to rstconnect dots to form an umbrella and were then askedto draw an upside-down, closed umbrella, to evoke as-sociated words, to talk about rainy months, and to talkabout regions of the country associated with rainfall.

The subjects were also asked to mention and visualizecharacteristic aspects of the geographic region, such asthe main cities, foods, and cultural events. Subjects werealso asked to name objects presented on pictures, to clas-sify them into categories (e.g., fruits, vegetables, and thelike), to name all the objects belonging to a specic se-mantic category, and to provide names of fruits fromother countries. The nonstimulation group received nocognitive stimulation. Breuil et al. reported an improve-ment of the total MMSE scores in the stimulated groupafter the training (the scores were not provided, how-ever) and immediate positive effects on the Word ListMemory Test ( P 0.09). No other improvements werenoted in the other areas measured, which were verbaluency and activities of daily living.

In summary, the three studies using visual imagerytechniques registered mediocre results, despite the factthat the authors of two of the studies reported somekind of improvement.

Encoding Specicity With Support at RetrievalWe reviewed three studies that used the encoding spec-icity strategies with cognitive support at retrieval inpatients with AD. 26,27,51 The severity of dementia variedfrom mild 26,27,51 to moderate 26,27 and severe. 26,27 Thethree studies specically targeted episodic and semanticmemory, since the subjects had to learn lists of words orobjects. All the studies examined the effects of differentencoding conditions on performance at retrieval withthe free and cued recall paradigms as well as the encod-ing-retrieval compatibility paradigm.

The study by Karlsson et al. 26 included subjects withmild ( n 12), moderate ( n 17), and severe ( n 14)AD as well as 36 healthy older adults. Each subject re-ceived one training session and was asked to remembertasks performed using a given object (subject performedtask, or SPT; for example, lift the cup) or to rememberverbal material. The authors referred to these methods

as, respectively, motor coding and verbal coding. Half of the subjects in each group received the SPT instruc-tions, and the other half received the verbal task. Eachsubject in the SPT group was presented with 25 objects(belonging to ve semantic categories), one at a time,which they had to manipulate according to the verbalinstructions given by the experimenter. After the pre-sentation of the last item, the subjects had 5 minutes forfree recall of as many items as possible. A cued recall


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trial with semantic category cues was then adminis-tered. The results showed a signicant effect of the task(SPT versus verbal task) in the three groups with ADand in the control group. The groups with mild, mod-erate, and severe AD as well as the control group per-formed signicantly better on the SPTs than on the ver-

bal tasks ( P 0.05) and signicantly better on these tasksin the cued recall than in the free recall condition(P 0.05). The authors concluded that motor coding, butnot verbal coding, improves free recall and cued recallin normal older adults as well as in patients with AD,thus supporting the idea that in order to demonstratememory enhancement in AD, it is necessary to providea substantial amount of environmental support as aguidance process for remembering. It may be that motorcoding counteracts some of the severe attentional andsemantic memory decits associated with AD. 26 Therewas no longitudinal follow-up of this learning training.

The study by Herlitz et al. 27 included subjects withmild ( n 10; mean MMSE score, 24.5), moderate ( n10; mean MMSE score, 16.6), and severe AD ( n 10;mean MMSE score, 6.6) as well as healthy control subjects (n 10; mean MMSE score, 29.7). All subjects ex-perienced, in a single learning training session, ve dif-ferent encoding conditions: in the verbal encodingcondition, the subject listened to a list of nouns read bythe experimenter and read the corresponding words oncards, one at a time; in the object encoding condition,the subject was presented with the actual objects andhad to name them; in the semantic encoding condition,the subject was presented with the objects and wasasked to answer questions about their functional use; inthe semantic/motoric condition, the subject was pre-sented with the objects and asked to motorically dem-onstrate how to use them; and in the motoric condition,the subject had to use presented objects according to theexperimenter-provided instructions. The goal of thestudy was to assess which encoding condition providedthe best retention and recall performance, using the freeand cued recall paradigms. After each condition, subj-ects were asked to free-recall all items they could re-member during a 2-minute period. A cued recall wasthen immediately carried out whereby the semanticcategory names were provided as cues. Using the free

recall paradigm, the patients with mild, moderate, andsevere AD recalled, respectively, from 35% to 40% (bestperformance in the object condition), from 15% to 30%(best performance in the verbal condition), and from 0%to 5% of the items (best performance in the verbal con-dition). Using the cued recall paradigm, the patientswith mild, moderate, and severe AD recalled, respec-tively, from 40% to 60%, from 20% to 35%, and from 2%to 20% of the items (best performance in the motoric

condition). Although the recall performance of subjectswith AD signicantly beneted ( P 0.001) from the cuedrecall paradigm, there was no signicant effect of theencoding conditions in subjects with mild and moderatedementia. Only the patients with severe AD signi-cantly improved their cued recall performance in the

motoric condition ( P 0.01). In comparison, the controlsubjects recalled 60% to 80% of the items using the freerecall paradigm and 70% to 90% of the items using thecued recall paradigm. The controls signicantly im-proved their performance in the semantic and seman-tic/motoric conditions as compared with the verbal con-dition ( P 0.01). The authors concluded that patientswith mild AD are able to utilize cues to increase retrievalperformance after poor (i.e., verbal) as well as rich (i.e.,semantic) encoding conditions; that patients with mod-erate AD are able to benet from cues after all forms of encoding, with the exception of pure verbal encoding;and that patients with severe AD are able to utilize cuesonly after motoric encoding. There was no longitudinalfollow-up of the learning training.

The study by Lipinska et al. 51 included 15 subjectswith mild AD and 15 older healthy control subjects.During a single session, subjects were shown 20 pho-tographs, representing common objects, for 30 secondseach. To realize the process of self-generated semanticencoding specicity, the subjects were asked to name therst 10 pictures (the naming condition) and for the re-maining 10 pictures were instructed to name the objectsand to select, from two possible alternatives, the seman-tic category to which they belonged (the naming cate-gory decision condition). At the retrieval phase, the subjects were rst asked to freely recall as many objectnames as possible from the list. They then had a cuedrecall trial in which they were provided with semanticcategory cues similar to those used at the encodingphase (encoding-retrieval compatibility). Finally, subj-ects had a four-alternative multiple-choice recognitiontrial in which each target item was presented in a book-let along with three distracting items. In the poorest en-coding-retrieval conditionthe naming conditionus-ing the free recall paradigm, patients with ADremembered 6.7% of the information, whereas the con-trol subjects recalled 11.3%. Comparatively, in the

richest encoding-retrieval conditionthe naming

category decision conditionusing the recognition par-adigm, patients with AD recognized 68% of the infor-mation, whereas the control subjects recognized 67.3%of the information. The authors did not mentionwhether there was any signicant difference betweengroups. Only the performance of subjects with AD sig-nicantly ( P 0.05) beneted from the richest encodingsituation (naming category decision condition) in


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cued recall and recognition trials. In this study, patientswith AD, as opposed to the normal older subjects,showed an effect of the encoding manipulation. For thenormal older subjects, the requirement of naming ap-peared to be sufcient to optimize performance. Theseresults suggest that patients with AD need more cog-

nitive support at encoding than normal older adults tomake effective use of cues at retrieval. The overall lownumbers recorded in recall trials could have been theresult of the relatively short presentation of the stimulusduring learning. There was no longitudinal follow-up of this learning session.

In summary, the three studies using the encodingspecicity strategies with cognitive support at retrievalfound that subjects with mild to moderate AD best ben-eted from the richest encoding and retrieval condi-tions, that is, with semantic and motor encoding accom-panied by a cued recall or recognition paradigm. Themotor encoding was especially efcient in patients withsevere AD.

The Errorless Learning Approach Combined With theSpaced Retrieval TechniqueFive studies using errorless learning and spaced re-trieval techniques together are reported in the literature:the studies of Arkin, 53 Clare et al., 10,71,72 and Kixmiller. 59

The information to be learned consisted of autobio-graphical information; 10,53 various information such asnames of people 71,72 and how to use a calendar; 10 andfuture appointments. 59 Thus, the focus of the rst fourstudies 10,53,71,72 was on episodic memory, and the targetof the third 59 was prospective memory.

The study by Clare et al. 10 included six experimentalsubjects in a multiple single-case study with an experi-mental design. Internal memory training was used withfour subjects, and external memory aids training wasusedwith the other two (results are presentedseparatelyin Table 1). For the subjects undergoinginternal memorytraining, the information to be learned consisted of names of participants of social clubs, names of partici-pants of a support group, names of famous people, andvarious personal information (episodic memory). Onetraining session was provided for every item to belearned, and the length of the sessions varied according

to the information presented. A recall test trial consist-ing of all items was administered at the end of eachtraining session. Follow-up assessments were scheduled1, 3, and 6 months after completion of the intervention.The results were based on the mean proportion (%) of correct responses. The four patients were able to signi-cantly increase the amount of information to be learned,from approximately 20% to 60% of the information. Theresults were maintained at the 6-month follow-up eval-

uation. The subjects neuropsychological scores werenot reported, but the authors mentioned that no signi-cant changes occurred in the global cognitive prole of three of the subjects when compared with baseline data.A deterioration of the global cognitive prole was re-corded for one patient.

Clare et al.71

used an errorless learning and spacedretrieval approach in a case study to help a 72-year-oldpatient with mild AD learn the names of the 14 peoplein his social club. At a baseline presentation of the pic-tures, the subject knew the names of three members.These three pictures were retained for practice purposesduring training. The remaining 11 faces were learnedover 21 sessions. Sessions took place twice weekly; onenew picture was added every week, and one sessionperweek was used for practice. The length of the sessionvaried depending on the time the subject required tolearn the name. The subject was asked to give an answeronly if he was sure; prompts in the form of vanishingcues were provided in the case he was uncertain. Recallwas then asked, without prompts, using the expandedrehearsal method. The authors described the initial in-tervals as short but gradually increasing until a 10-min-ute interval was reached. Home practice was encour-aged. Follow-up sessions were conducted at 1, 3, 6, and9 months after the end of the training sessions. The subj-ect recalled 20% of the information at baseline (three of 14 pictures). He was able to learn and retain all 14 names by the end of training (session 21), and he remembered98% of the names over the posttests 1, 3, 6, and 9 monthslater. A follow-up study 72 found that the patient wasable to retain 70% of the names over a 2-year period.The 1999 report by Clare et al. 71 was the rst to showgains with the AD population using errorless learningand spaced retrieval techniques combined, and the 2001follow-up report 72 was the rst to show that these gainscan be maintained over 2 years. These data suggest thaterrorless learning and spaced retrieval can be usefulmethods for stimulating new and relatively durablelearning in patients with AD despite the degenerativenature of the illness.

The study by Arkin 53 included seven subjects in thememory training group and four in the control group.The control subjects met with the experimenter but re-

ceived no specic memory training. A random assign-ment procedure provided homogeneous groups with allof the lower-functioning individuals in the same group.The author then assigned the subjects to the experimen-tal and control groups in order to obtain heterogeneousgroups. A single-case experimental design was used be-cause the patients had to relearn 32 autobiographicalfacts (episodic and autobiographical memory) recordedon tapes for each subject. This information was obtained


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from the patient and his or her caregiver. The informa-tion was learned using an errorless approach and thespaced retrieval technique. For the spaced retrieval tech-nique, the authors did not provide information aboutthe time intervals between recall trials or the longesttime interval to be achieved. A research student admin-

istered the tape-recorded exercise once a week for tenconsecutive weeks; the exercise took approximately 20minutes. The number of facts learned by the end of the10-week training program was recorded. At baseline,the experimenters made sure that each subject knew atleast 16 of the 32 (50%) autobiographical facts; the subj-ects had to learn the remaining 16 facts. Of the 16 factsleft to be learned, the seven subjects in the memorytraining group learned from seven to 13 facts. These re-sults were signicant when compared with the controlgroup. (The mean scores of the control subjects re-mained unchanged after 10 weeks.) For most subjects inthe training group, memory functioning improved most between the third and the fourth session, or 3 to 4 weeksafter baseline.

Kixmiller 59 included ve patients with mild AD in theexperimental group and two patients with mild AD inthe control group of errorless learning and spaced re-trieval training program. Six training sessions, each last-ing from 30 to 120 minutes, were conducted over twoweeks in the patients homes. The length of the trainingsession depended on the length of time the subjectneeded to complete the task without making errors. In both the experimental and control groups, subjects hadto learn how to write down appointments, take medi-cation, and remember future important dates (prospec-tive memory). The experimental training included ob-servation, modeling, verbal prompt, self-instruction,independent trials with feedback, drilling with self-instructions, and trials in which subjects carried outtasks independently. Patients were prevented from mak-ing errors during training. The control group receivedinstructions in general memory strategies, memoryquestionnaires, and verbal descriptions of the tasks tolearn, and they independently completed the tasks. Aspaced retrieval technique was also used for posttests.Recall trials were attempted immediately after trainingand then 3, 4, and 7 weeks after the completion of the

training. Only the experimental training group im-proved performance on specic, prospective memorytasks. By the end of training, the participants who re-ceived memory training completed 79% of the requiredtasks, whereas the control group completed 14% of thetasks. The effects were maintained up to 7 weeks afterthe treatment in the ve experimental subjects.

In summary, the 17 subjects trained with the errorlesslearning approach combined with the spaced retrieval

technique all showed signicant improvement in thepercentage of information recalled after the training ses-sions. Of these subjects, 29%reportedly maintained theirlearning over a 7-week period, 17.6% over a 6-monthperiod, and 0.06% over a 2-year period.

The Spaced Retrieval TechniqueOne study, that of McKitrick et al., 68 used only thespaced retrieval technique to stimulate memory in ADpatients. This study included only four experimentalsubjects. The researchers goal was to stimulate pro-spective memory by asking subjects to remember a taskrequired for the following week. Three different tasks (adifferent task every week) had to be learned. The du-ration of the training varied with the participants, be-cause the training was carried out until the subject couldretain and recall the information for at least 60 seconds.The intervals were then increased by 30 seconds aftereach successful recall. The experimental subjects wereable to learn 100% of the tasks. This achievement can beconsidered a success. However, the long-term effects of the memory training were not measured.

The Spaced Retrieval Technique With Visual ImageryOne study, that of Davis et al., 67 used the spaced re-trieval technique in combination with visual imagery tostimulate memory in AD patients. This was the rst ran-domized placebo-controlled crossover trial that mea-sured the efcacy of a cognitive stimulation program inpatients with AD. The study involved 37 subjects withmild to moderate AD (mean MMSE score, 22.4) ran-domly assigned to an experimental ( n 19) or a placebogroup ( n 18). After an extensive baseline neuropsy-chological examination, both groups were started on a5-week memory training program. All subjects rst hadto recall autobiographical information (seven facts).About half of the patients (19 of 37) did not know theseseven autobiographical facts and participated in aspaced retrieval technique training to learn them. Everyexperimental subject (including those receiving thespaced retrieval training) participated in a peg taskrequiring them to learn three pairs of rhyming numbersand objects (e.g., 1-bun, 2-shoe, 3-tree). The subjectswere then instructed to use the numbers as pegs (re-

minders) to help them recall the words. Once they com-pleted this task, the subjects were asked to learn thenames of three staff members using pegs (e.g., kneefor Naomi), to visualize the peg, and to associate thisvisualization with the persons face. The placebo groupwas asked to complete exercises such as repeating thealphabet (mock training) during 5 weeks. Every patientwas reassessed at the end of the 5-week trial by exam-iners blind to the experimental conditions. The placebo


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group then crossed over to receive the 5-week interven-tion program; only this group was retested a third time by the examiners, who were no longer blind to the ex-perimental conditions.

The performance of the subjects after the training wascompared with their performance at baseline on a va-

riety of cognitive tests (MMSE, WMS-R Logical Memoryand Visual Reproduction, WAIS-R Digit Span, Verbal Se-ries Attention Test, Controlled Word Association Test,Category Fluency, Finger Tapping Test, and GeriatricDepression Scale). The initial experimental group (IEG)and the placebo group (PG) both improved on ve neu-ropsychological measures, although these improve-ments did not reach statistical signicance, possibly be-cause of the small numbers of patients in each group.The two groups improved on short-term and long-termvisual recall, although the improvement of the PG wassometimes greater than that of the IEG. The IEG regis-tered a mean positive change of 2.72 points whereas thePG had a mean positive change of 4.36 points on im-mediate recall of the visual reproduction subtest. TheIEG had a mean positive change of 3.72 points whereasthe PG had a change of 2.4 points on delayed recall of the visual reproduction subtest. Only the IEG improvedon a measure of verbal attention (from 218.7 to 197.5seconds on the Verbal Series Attention Test). The im-provement in both groups was less impressive on mea-sures of long-term verbal recall and of semantic uency.The IEG registered a mean change of 1.15 items, and thePG had a change of 1.65 items, on the delayed recall of logical memory subtest. The subjects of the IEG in-creased their verbal production by a mean of 1.16 wordson the Category Fluency task, whereas the subjects of the PG improved by only 0.83 words. The 19 patientswho did not know the seven personal facts at baselinewere able to learn a mean of 55% of the items after 5weeks of training, and this nding was signicant(P 0.01).

The authors concluded that the spaced retrieval tech-nique showed some efcacy in helping the patients re-learn autobiographical information. The authors sug-gested that practice effects on the tests might explain theimprovement of both the experimental and controlgroups on the other measures. Although this is certainly

possible, it does not seem likely that practice effectsalone would explain all of the improvement, given thedegenerative nature of the memory decits in AD andthe interval of 5 weeks between pre- and posttests. Thusthe improvement may have been due in part to somegeneralization effect of the spaced retrieval techniquethat was used by the subjects in both the IEG and thePG who needed to learn the autobiographical informa-tion. Another possible explanation lies in the simple fact

that meeting with an experimenter might improve ormaintain functioning independently of cognitive stimu-lation. There was no longitudinal follow-up to measurethe long-term effects of the training.

External Memory Aids

The study by Clare et al.10

included two subjects withAD who used external memory aids. The errorless learn-ing approach, involving regular practice with prompt-ing provided by the caregiver, was used to teach twopatients how to use an external memory aid in order todecrease the repetition of questions the patients ad-dressed to their caregivers. One subject had to learn howto use a calendar, and the other had to learn how to usea diary with a NeuroPage. The authors did not reportthe length and frequency of the training. Assessmentstook place at baseline, at the end of the training, and 3and 6 months after the completion of training. The number of questions asked daily by the patients was re-corded and used as a measure of efcacy. Only the pa-tient trained with the calendar signicantly improvedhis functioning: he asked a mean of 2.6 questions a dayat baseline, 0.75 questions a day at the end of the train-ing, 0.4 questions a day at the 3-month follow-up, and0.5 questions a day at the 6-month follow-up. The pa-tient trained with the diary and the NeuroPage initiallyimproved his functioning and then registered a declineat the 6-month evaluation: he asked a mean of 1.6 ques-tions a day at baseline, 0.75 questions a day at the endof the training, 0.5 questions a day at the 3-month fol-low-up, and 2 questions a day at the 6-month follow-up. However, since the number of questions asked bythe two patients was relatively low at baseline, one canargue that there was not much room for improvement.

Dyadic TrainingFour studies on dyadic training in AD were found. Thestudy by Kesslak et al. 69 included 11 subjects with ADand 11 healthy controls. They used dyadic training aswell as some principles of errorless learning to teacheach patient some episodic information (such as namesand interests) about the other participants in the group.The training was thus carried out in a group format, butthe patients learned the information through each pa-

tient-caregiver dyad. The patients met together the rstweek, and the following week each patient had to pro-vide information about some other participants of thetraining program, as shown on individual pictures. Thepatients were encouraged to practice at home using thepatient-caregiver dyad. The investigators did not use apure errorless approach, since they allowed the patientsto make errors but they immediately corrected them.The overall training lasted four weeks; the authors did


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not provide information about the duration of the in-dividual sessions. The patients improved their perfor-mance on name recall during the training: they wereable to recall a mean of six names at the second sessionand seven names at the fourth session, whereas the con-trols performance remained the same (they remem-

bered approximately eight names at the second sessionand at the end of the training). There was a signicantimprovement by session 2 but no further signicantimprovements thereafter. There was no longitudinalfollow-up.

Quayhagen et al. 42,43 mostly used dyadic training asa means of generally improving the cognitive and socialfunctioning of the patients and their caregivers, andtherefore they did not target any specic training strat-egies or memory systems. In an initial pilot study, 42 theauthors included ten dyads in the experimental groupand six dyads in the control group. The subjects weretrained with the techniques of conversation, memory-provoking exercises (the authors provided no explana-tions or details), and problem solving. The authorsfound that memory improved in theexperimental group(a mean of 5.1 items [out of 25] retained on posttesting4 months after training and 5.3 items retained 8 monthsafter training, compared with 3.7 items retained at base-line). No such improvement was recorded for the con-trol group (respectively, 2.5 items retained at baseline,2.7 items 4 months after training, and 2.3 items 8 monthsafter training).

In a more recent study, Quayhagen et al. 43 used aspaced retrieval technique to perform the memory train-ing part of their cognitive/social stimulation program.This study included 25 experimental, 25 control, and 28placebo subjects. The placebo subjects observed theircaregivers but did not participate in the training exer-cises (passive approach). The control subjects wereplaced on a waiting list and had no knowledge of anytraining at all. The experimental subjects were traineddaily with 1-hour sessions of active memory recall andrecognition exercises (the authors did not provide anyexplanations), interpersonal problem-solving situations,and targeted conversational exercises. The training wascarried out over 6 days. Results of memory trainingwere measured using the raw scores of the Wechsler

Memory ScaleRevised (WMS-R).73

Subjects were tested before and immediately after training and again 9months later. The experimental subjects improved theirnonverbal memory as assessed on the WMS-R (with amean of 36.7 of 76 items of information retained on thevisual reproduction subtest retained at pretraining test-ing and a mean of 41.4 items retained at the end of train-ing. At the 9-month follow-up evaluation, the perfor-mance of the experimental subjects was compared with

that of the other two subject groups. The effects of thetraining were not maintained (36.8 out of 76 items re-tained in the experimental group versus 32.8 items forthe placebo group and 29.4 items for the control group).

Sandman 70 included 11 dyads of subjects with AD ina study using primarily a dyadic approach. No control

group was used. In this study, an attempt was made tostimulate memory by provoking emotional memories toproduce ashbulb memories. (The author did not pre-cisely dene what are emotional or ashbulb memo-riesthat is, the kind of emotions that should have beentriggered by the memories, and the required degree of emotional intensity). The patients and caregivers had topay attention to specic information presented in lmsor pictures. The pictures contained information aboutthe other subjects in the program. The training was car-ried out over 4 weeks. The author did not provide in-formation about the duration and weekly frequency of the sessions. Memory was formally assessed at baselineor follow-up with a neuropsychological evaluation.Only the amount of information retained was recordedafter the training. This study demonstrated that theemotional memories were best remembered: the pa-tients retained six items in the high arousal condition,compared with approximately two items in the lowarousal condition. There was no follow-up evaluation.

In summary, the four studies using a dyadic approachshowed an immediate slight improvement of question-able statistical and clinical signicance. In theonly studythat made a follow-up evaluation, the effects of thetraining were not maintained 9 months after the train-ing.

DISCUSSION

Memory and cognitive stimulation programs have reg-ularly been mentioned in the literature over the past 15years for the AD population. However, with the excep-tion of a few studies, 26,27,31,43,44,51,67 most of the researchprotocols of the studies we reviewed (61.1%) have in-volved very small groups of subjects ( n 11), whichlack statistical power.

In terms of the assessment of the efcacy of the train-

ing, 61.1% (11 out of 18) of the studies reported changeonly on the specic tests or items for which the subjectshad received training to remember. 10,26,27,51,53,59,6872 Inthe majority of these studies (10 of the 11), the theoretical basis of the training was very well explained and justi-ed, and good, though modest, results were generallyreported. In some of these studies the new learned ma-terial had no real impact on the life of the pa-tients. 26,27,51,70 Nevertheless, the learned or relearned


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material in other studies 10,53,59,68,69,71,72 had some impor-tance in improving the capacity to manage memoryproblems in everyday life (such as the capacity to re-member an appointment or future important dates or tostop asking questions repetitively). Eventually an ame-lioration of these capacities might have a positive effect

on the quality of life of the patients and their caregivers.However, these studies did not measure the possiblegeneralization effect of the memory stimulation trainingto other memory functions or other cognitive functions,and they did not measure the impact of the cognitivetraining on measures of quality of life.

Only three studies reported a generalization of the ef-fects of general cognitive stimulation using exclusivelystandardized cognitive tests, such as memory scalesandthe MMSE. 4244 The theory underlying these studieswasgenerally weaker in terms of cognitive neuropsychologythan the theoretical rationales given in the studies citedin the previous paragraph. In addition, the techniquesused to stimulate memory were often only partially de-scribed and not well justied by the authors. The ob-tained results were barely explained, which made themdifcult to understand for the readers. For example, inone study, 44 the training targeted visual imagery (andthus, to some extent, semantic memory), whereas theposttraining evaluation assessed global cognition asmeasured by the MMSE, episodic memory (word list),and verbal uency. The results of this study were limitedand reportedly had no effect on the patients activitiesof daily living. The biggest challenge in the assessmentof the cognitive stimulation programs using this methodis the incapacity to directly translate the outcome of thetraining into specic applications in the patients life.

Four studies reported the effects of training on boththe specic tests or items for which the subjects weretrained and on other standard measures of memory andcognition. 10,31,66,67 These studies provided measure-ments of change on both the trained material itself andpossible generalization of the training to other areas of memory or cognition. One study demonstrated somestatistically nonsignicant amelioration, 67 and two otherstudies showed no deterioration or change comparedwith baseline on the standard cognitive measures. 10,66

Another study reported the absence of a positive impact

on functioning in everyday life.31

Interestingly, only twoof the studies 10,67 reported an improvement in remembering the specic trained items. These results suggestthat cognitive stimulation of memory may have an im-pact on cognition in general, by slightly improving at-tention and memory functioning 67 or by maintaininggeneral cognitive functions, 10,31,66 even for a 6-month pe-riod. 10 These types of results (slight cognitive improve-ment, maintenance of cognitive function) have been re-

ported in cognition-enhancing drug trials, especially instudies using acetylcholinesterase inhibitors such as do-nepezil. 74

In terms of the results reported, six controlled stud-ies,26,27,44,51,59,69 four randomized controlled stud-ies,42,43,53,67 three studies with a multiple single-case ex-

perimental design,10,68,70

and two case studies71,72

havereported positive effects of memory stimulation or re-mediation programs in AD despite the neurodegenera-tive impediment. These positive effects were usuallyregistered during or immediately after the memorytraining 26,27,44,51,53,6770 and were thus limited. At the endof the training, the best results, listed in descending or-der of effectiveness, were obtained with the errorlesslearning approach combined with the spaced retrievaltechnique, 10,53,59,71,72 the spaced retrieval techniquealone, 68 the spaced retrieval technique with visual im-agery, 67 the richest encoding conditions (semantic/mo-tor and motor) with self-generated cues using the en-coding specicity paradigm with cognitive support atretrieval, 26,27,51 dyadic training; 42,43,69,70 and externalaids. 10 Although the program of encoding specicitywith cognitive support at retrieval showed immediatepositive results, the material learned in these studieswas more laboratory-type material and therefore notadapted to the needs of the patients, as it was in theother studies using other strategies principally focusedon prospective and autobiographical memory.

The positive effects of the memory training wererather modest or nonexistent in the studies using onlyvisual imagery. 31,44,66 Visual imagery techniquesareusu-ally cognitively complex and effortful. These techniquesrequire a high level of elaborative processing that mostpatients with brain damage, amnesia, or dementia areunable to achieve spontaneously. 25,32 Furthermore, thecerebral areas typically shown to be involved with vi-sual imagery, that is, the bilateral parietal, 75 temporal,and occipital association areas, 7679 are also the brain re-gions impaired in AD, 80 and, in the early stages of thedisease, particularly the temporal 81,82 and parietal as-sociation areas. 83 Therefore, it might be difcult to useonly these techniques with patients in their everydaylife.

Only four studies using the errorless learning ap-

proach combined with the spaced retrieval tech-nique, 10,59,71,72 two studies using the dyadic ap-proach, 42,43 and one study using external aids 10

provided the results of follow-up assessments. The re-sults of the training were maintained 7 weeks 10 to 24months 71,72 after training using the errorless learningwith the spaced retrieval techniques,3 to 6 months usinga diary with a NeuroPage or a calendar, 10 and 4 to 8months using the dyadic approach. 42 However, theposi-


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tive results of the training were not maintained 9months after the dyadic training in one study 43 and 6months after the training with the diary and theNeuroPage. 10 Only the studies using errorless learningwith spaced retrieval 10,53,59,71,72 provided positive effectsof training that were consistently maintained over time.

An important limitation of the studies of memory re-mediation programs in AD is the lack of informationabout the performance of the subjects on a variety of cognitive measures at the end of the study and, even-tually, at long-term follow-up. These extensive and thor-ough neuropsychological assessments could provide in-formation about a generalization of the effects of thetraining.

CONCLUSION AND RECOMMENDATIONS

The results from the studies we reviewed suggest thatit is possible to stimulate memory in AD. The errorlesslearning, spaced retrieval, and vanishing cues tech-niques, together with the dyadic approach, seem to pres-ent the best memory training methods for patients withAD. Clearly, there is a need for more randomized con-trolled studies with memory stimulation programs tovalidate this treatment approach in the treatment of de-mentia. On the other hand, one of the major advantagesof the client-centered case report approach used in mostof the training procedures reported in this review is atraining specically adapted to the needs of the individ-ual subject in his or her everyday life. Long-term follow-up evaluations of the content of the training, as well asexhaustive neuropsychological evaluations at baseline,at the end of the study, and at follow-up, should be aprerequisite in future study designs, since they wouldserve to assess the long-term effects and the generaliza-tion potential of the training procedures.

The dyadic approach could be used to carry out pro-grams using various training techniques concomitantly,

such as the errorless learning, spaced retrieval, and van-ishing cues techniques. A major advantage of the dyadicapproach is that it may provide the caregiver with someinformation about AD as well as techniques to better dealwith the illness. One of the advantages of the errorlesslearning technique is that patients usually feel good

about themselves, since errors are kept to a minimum.Among other things, this boosts self-esteem and reducesfrustration in patients with cognitive impairments. 6

Although procedural memory is relatively spared inAD,8,1719 only one study was found to specically stim-ulate this memory system. 84 We did not include thestudy in our review, however, because the subjects al-ready knew how to perform the tasks; the goal of thetraining was to improve the time to complete tasks (ac-tivities of daily living, or ADL) rather than to learn newtasks. No study has been found to target proceduralmemory in order to teach patients with AD how to learn,or relearn, ADL tasks. Future research should examinethe efcacy of the combined errorless learning andspaced retrieval techniques in stimulating proceduralmemory in AD.

An ideal memory training should target informationuseful to the everyday functioning of the patients andtheir caregivers, such as activities of daily living, 85 anduse similar training procedures or techniques for everysubject involved in a given program. This approachwould permit the design of standardized memory train-ing programs involving larger numbers of subjects andallow the efcacy of these programs to be tested in ran-domized crossover placebo-controlled trials. Finally, fu-ture research should measure the efcacy and the long-term effects of training in patients who are drug naiveor on placebo compared with patients taking cognition-enhancing drugs such as donepezil, rivastigmine, andgalantamine.

This work was supported by the Jeanne et J.-Louis Levesquedoctoral award to Mr. Grandmaison.

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A Critical Review of Memory Stimulation Programs in Alzheimer´s Disease