MONITORAMENTO DA METAMEMÓRIA NA DOENÇA DE ALZHEIMER: UMA REVISÃO SISTEMÁTICA

Brandt, Michelle; Carvalho, Raquel Luiza Santos de; Belfort, Tatiana; Dourado, Marcia Cristina Nascimento

doi:10.1590/1980-57642018dn12-040002

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Dementia & Neuropsychologia

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Sumário

Original Article • Dement. neuropsychol. 12 (4) • Oct-Dec 2018 • https://doi.org/10.1590/1980-57642018dn12-040002 copiar

MONITORAMENTO DA METAMEMÓRIA NA DOENÇA DE ALZHEIMER: UMA REVISÃO SISTEMÁTICA

Autoria SCIMAGO INSTITUTIONS RANKINGS

RESUMO

Metamemoria é a consciência do próprio conhecimento e controle da memória, e refere-se à capacidade online de reunir informações sobre o estado atual do sistema de memória.

Objetivo:

Metamemória é a consciência sobre o próprio conhecimento e controle da memória. Nós conduzimos uma revisão sistemática para identificar os tipos de tarefa usadas para avaliar o monitoramento da metamemória, os estímulos usados nessas tarefas, suas limitações e resultados em pessoas com doenças de Alzheimer.

Métodos:

Esta revisão sistemática usou a metodologia PRISMA. Uma busca nas bases Pubmed, Scopus e Web of Science foi feita em Setembro de 2018. Foram identificados estudos experimentais em metamória e demência.

Resultados:

Foram incluídos 21 estudos que se enquadravam nos critérios de inclusão. As tarefas mais comuns foram “judgement of learning”, “feeling of knowing”, “judgement of confidence” and “global prediction”. As discrepâncias, em termos de monitoramento de metamemória, ainda necessitam de pesquisas futuras. O Rey Auditory Verbal Learning Test foi a lista de palavras mais usada. Pessoas com doença de Alzheimer são capazes de avaliar de forma acurada o seu funcionamento da memória, quando a avaliação é feita em um momento posterior. Eles tendem a superestimar seu funcionamento quando o julgamento é feito em uma visão de futuro.

Conclusão:

No contexto do comprometimento da metamemória, é necessário que clínicos e cuidadores procurem intervenções com o objetivo de identificar estilos compensatórios de funcionamento. Assim, esta revisão sistemática fornece evidências iniciais sobre o uso de medidas de metamemória como parte de avaliações mais amplas na doença de Alzheimer.

Palavras-chave:
metacognição; metamemória; demência; doença de Alzheimer; cognição

Study	Sample	Measures	Tasks	Main results
1. Cosentino et al., 2016	49 - mild to moderate AD (22 - awareness 27 - unaware)	• A modified version of anosognosia rating scale. • A modified episodic FOK task. • PVLT • Executive Functioning • Phonemic fluency test	• Prospective condition - prospective judgments for each item in response to written questions. • Retrospective condition - identical to the prospective condition, with the additional component of a retrospective evaluation after every item, regardless of accuracy. • Feedback condition - identical to the prospective condition, except that the examiner provided feedback regarding recognition memory performance after each item. • Metamemory accuracy - relative accuracy of all item by item judgements.	• There was a significant interaction effect between accuracy and the aware group. The unaware group made higher FOK ratings for incorrect responses than did the aware group. There was no difference in FOK ratings between groups for correct responses. The analysis of association between awareness, FOK ratings, memory accuracy varied across task condition showed a main effect of accuracy - the FOK ratings varied depending on memory accuracy. There was no main effect of group or task condition.
2. Cosentino et al. 2015	14 - AD moderate 20 - HE	• Metamemory test: • Digit span; • PVLT • Biber figure learning test • GPG • MRI	• AD - one condition: standard. • HE - three conditions - standard, query or feedback. • Standard - Participants were asked to make prospective judgments for each item in response to written questions. • Query - identical to the standard, with the additional component of a retrospective evaluation after each item. • Feedback - identical to the standard except that the examiner provides feedback regarding memory performance after each item.	• Performance on the metamemory test was not significantly associated with education. Metamemory performance was associated selectively with right insular volume. The left insula has also been implicated in supporting aspects of self- awareness and we sought to determine the robustness of the apparent right lateralization.
3. Cosentino et al., 2011	42 - mild AD50 - HE	• MMSE • PVLT • ACED • Clinical ratings of awareness • Modified FOK task	• The examiner read about five people (their name and something about their background). After the first learning trial, predictions for memory performance were acquired one at time for each item. The participants had to select the correct answer in eight possible -The answer choices included the correct response, the correct answers for the remaining 4 stimuli, and 3 new distractors. • Feedback condition - the examiner told the participant if their answer was correct or incorrect prior moving onto the next item.	• There was no difference in metamemory score as a function of task condition. There was no difference in metamemory as a function of stimuli set in HE or AD group. Participants of both groups demonstrated no variability in their prediction. Awareness was particularly important for decision making capacity. Decision making-capacity related to medication management was diminished in the unaware group.
4. Souchay et al., 2002	16 - AD 16 - HE 16 - YA	• MMSE • WCST • FAS • Stroop test • Logical memory test • Buschke selective reminding test • FOK accuracy Index	• The subjects were asked to recall the target that corresponded to a given cue. They had to underline the words seen earlier. The FOK judgment response was either a yes or no. After making the FOK predictions, the recognition task was administered.	• FOK_- no differences were found in the proportion of yes and no judgment in the three groups. • FOK accuracy - The AD patients made significantly fewer hits and more misses for yes judgment than older subjects. Prediction errors were more frequent for yes judgments than for no judgments. AD patients tended to overestimate their performance. No significant difference was found between younger and older adults.
5. Correa et al., 1996	20 - AD 18 - MCI 18 - HE	• Standard neuropsychological test battery • MIA Questionnaire • BCRP • RAVLT • BVRT • Word and animal fluency tests	• Estimation of performance accuracy following the administration of selected memory test (i.e. postdictions of number of previously recalled words/designs). Rey Auditory Verbal Learning Test.	• AD Patients tended to overestimated their performance on the BCRP and RAVLT, while memory-impaired and control subjects showed a slight tendency to underestimated their performance. The discrepancy between postdiction and actual scores on the BCRP and RAVLT across groups was not significantly correlated with delayed recall, self-report memory change, informant report of memory change, the discrepancy between self- and informant report of memory change, intrusions or the proportion of correct intrusions. The AD subjects were not fully aware of their memory deficits.
6. Pappas et al., 1992	20 - AD 12 - HE	• KnowMemFOK test EpiMem FOK test	• KnowMemFOK test - The subjects were instructed to rate their confidence that their answer was correct using a 6-category scale. EpiMem FOK test - the subjects read each incomplete sentence for which they had failed to recall the correct answer. They were asked to indicate their FOK and, immediately thereafter, the sentence and 6 alternatives ending were read with the subject asked to select one.	• KnowMemFOK test - The AD patients answered significantly fewer questions than did the controls. The patients and controls did not differ in their percentage of correct recognitions bat they differ in their FOK. • EpiMem FOK test - The AD patients were profoundly impaired on the recall test. Neither the controls nor the AD group were able to predict their recognition performance.

Study	Sample	Measures	Tasks	Main results
1. Szajer & Murphy, 2013	143 - early to moderate AD 143 - HE	• Odor Recognition - Memory Task • Odor Threshold	• The participant was presented a sequence of odor. For each item participant were instructed to respond "yes" if the stimulus had been previously presented during the familiarity phase, and "no" if it had not.	• The control group performed significantly better confidence interval on episodic recognition memory task than did the AD group, however, both groups reported levels of confidence that failed to accurately differentiate between correct and incorrect responses. • Education level emerged as a significant predictor of confidence levels for incorrect responses and false alarms. No significant effect of diagnosis was found.
2. Gallo et al., 2012	18 - mild AD 18 - HE	• Metamemory task • AQD	• Participants studied object words and correspondent pictures presented as colored photos or as line drawings, and then took a picture recollection test followed by a confidence judgment.	• Reduced accuracy in AD participants compared to controls • AD participants were less likely to make high-confidence responses than were controls • The average for correct responses was greater than incorrect response in all groups. Calibration error scores were significantly greater in the AD group compared to control group • AD participants demonstrated some accuracy • AD insight into their cognitive decline, as their self-ratings of everyday problems were greater than the self-ratings problems reported by controls. • Participants with mild AD were able to use confidence judgments to track the accuracy of their responses on a recollection test.
3. Moulin et al., 2003	16 - AD 16 - HE	• CANDEX assessment tool • MMSE • Family interview • Laboratory screening	• Participants need select the word that they had seen before from the new word. This could be done either visually (by pointing) or verbally. • After selecting the word, they thought to be a target in each pair they were presented and rate how confident they were that they had selected the correct answer from the pair.	• AD group memory performance was worse than control group. • AD group is less confident in their memory performance than control group. • Both groups are accurate at assigning confidence to their recognition performance and the lack of a group difference suggests that the AD participants are accurate as controls in assigning confidence to their recognition performance.

Study	Sample	Measures	Tasks	Main results
1.Genon et al., 2016	17 - HE 23 - mild probable AD	• Memory task • MRI	• A subjective prediction/judgment about face-name memory task with unfamous people (episodic items) and famous people (semantic items). The participant had to choose among four levels to indicate his/her primary subjective judgment.	• Memory performance - the AD participants had significantly lower recognition performance than HE for episodic items but had a similar recognition performance for semantic items. • Subjective judgment for hits - In AD group, predictions low hits was significantly higher than predictions high hits. • Correlation between episodic memory measures and gry matter density in AD - The brain regions most reably identified inclued the right medial temporal lobe (with both hippocampus and parahippocampal córtex), posterior cingulate córtex (PCC) and ventrolateral pré-frontal córtex (VLPFC).
2.Thomas et al., 2013	Experiment 1: 27 - YA, 31 - HE, 24 - Very Mild AD Experiment 2: 26 - YA, 58 - HE, 32 - Very Mild AD Experiment 3: 27 - YA, 31 - HE, 24 - Very Mild AD	• Three levels of associated strength cue-word: unrelated, weakly associated, and strongly associated	• Experiment 1: JOL was made immediately followed each pair. Participants had 8s in which to make a response. • Experiment 2: JOL were made immediately after the cue-target presentation; therefore both the cue and target were likely available to participants during a given prediction. For participants to accurately predict memory performance, they are required to discount what they know during study and adopt the perspective of the examinee. • Experiment 3: One third consisted of a category cues paired with exemplars of the category (e.g., "vegetable-carrot"). One third of the pairs consisted of words that rhymed (e.g., hurt-dirt), and one third consisted of the first two letters of the target as the cue (e.g., ba-balloon).	• Intact metamemory monitoring processes in both older adults and people with DAT. Within the context of an episodic JOL task, both groups of participants demonstrated above chance prediction accuracy. • Neither normal nor pathological aging impaired the extraction and use of intrinsic cues on JOL. • However, the results of the first two experiments do suggest that the effective use of intrinsic cues changes as function of both normal and pathological aging. • All groups of participants demonstrated changes in performance as a function of extrinsic cues. However, younger and nondemented older adults demonstrated a steeper rise in performance between the letter and rhyming cue conditions as compared with people with AD.
3. Clare et al., 2010	236 - HE 67 - AD 13 - mixed dementia (AD and vascular)	• MMSE • MARS • RBMT • RBMT-E • MFS • MPS • The National Adult Reading Test • The Hospital • Anxiety and Depression Scale • The Positive Affect Index	• MFS or MFS-S - The participant is asked to judge how often she/he would be able to achieve this • MARS, MFS-S, MFS-I and MPS made as each sub-test of the RBMT or RBMT-E. • MFD - compering self- and informant rating by means of a corrected discrepancy score. • MPR - comparing postdiction rating (MPS) and objective test (RBMT) by means of a ratio score.	• -AD made significantly lower self-ratings of memory functioning and performance, and had significantly lower informant ratings of memory functioning, than controls. • -AD participants also differed significantly from controls on the memory functioning (MFD) and memory performance (MPR) discrepancy indices, reflecting greater discrepancies between self- and informant ratings and between postdiction ratings and objective test score. • Between one-half and two-thirds of participants with AD overestimate compared to either informant ratings or objective test score to a degree that is extremely rare in control group. A much smaller proportion of AD participants underestimate.

Study	Sample	Metamemory'sassessment	Measures	Tasks	Main results
1. Rosen et al., 2014	12 - FTD 14 - AD 35 - HE	• FOK • EOL • JOL • Retrospective CR • Response to feedback	EOL, memory encoding, JOL • Free Recall • FOK and recognition memory • Retrospective Confidence ratings (item-by-item) • Response to feedback	• EOL, memory encoding, JOL - after learning the word list, show the first word in each pair and asked to remember the second word pair. After seeing two examples, asked to say how many pairs they would likely be able to recall - predict how many of the words they would recognize from among the choices. • Free Recall - participants were shown the first word in each pair, one at time, and asked to recall the associate for each. • FOK and recognition memory - participants were shown the first word in each pair, one at a time, and reminded the correct associate among them. • Retrospective Confidence Ratings (item-by-item) - participants were shown the first word in each pair, one a time, and asked to rate their confidence that they had chosen the correct associate. • Response to feedback - participants had to rate how many pairs they had recalled correctly. Immediately following this feedback, they were asked to make another recall prediction about if give a similar list pair how many pairs will be remembered.	• Recognition predictions were higher then recall predictions in all groups. • AD and FTD patients appropriately lowered their estimates based on task conditions and experience with the specific stimuli. • Recall prediction 2 was higher than actual in all groups. FTD patients rated themselves similar to controls. • Significant impairments in FOK accuracy in FTD and AD, the deficit appeared more severe in FTD. • FTD participants used moderately confident and not very confident less often and used just guessing more often than controls. AD participants used moderately confident, not very confident and just guessing more often than controls. • Controls distributed their responses fairly evenly across all four FOK ratings but used the just guessing rating less than the others. AD patients responses were skewed toward lower ratings. FTD patients responses were quite aberrant. Most of their responses fell into the highly confident or just guessing categories. • The relationship between retrospective confidence and accuracy was significantly different in FTD and AD compared with controls. • Recall prediction 3, was lower than all prior predictions in all three groups. However, FTD patients did not lower their prediction commensurate with their score.
2. Shaked et al., 2014	109 - Mild to moderate AD 50 - HE	• Global cognition	• MMSE • PVLT • Biber figure learning test • FAS • GPG	• Global metamemory judgments prior to and following the presentation of the individual items, as well as judgments for each individual item. • Immediately after the first learning trial, predictions for memory performance were acquired - eight possible answers • The tester did not give feedback and moved on the next item.	• Metamemory was associated with both nonverbal fluency as well as nonverbal memory. • The study failed to find a significant association between metamemory and letter fluency, a verbally based executive task. • Neuropsychological evidence has indicated the involvement of right prefrontal regions in both metamemory and nonverbal executive tasks.
3. Schmitter-Edgecombe & Seelye, 2011	20 - AD 20 - HE	• Global prediction • On line e Offline metamemory	• Medical interview CDR • The telephone interview of cognitive status-modified • Memory Functioning Questionnaire • RAVLT • MFQ	• A global performance prediction paradigm - predicted the number of word they would remember both prior to after completing a list -learning memory test (online assessment memory). • Self-ratings about their everyday memory failures (offline assessment memory).	• AD group demonstrated poorer episodic memory performance than controls and overestimated their episodic memory performance. The AD group was significantly less accurate than control group. • AD group overestimated their everyday memory abilities. AD group learned disproportionately fewer words across the five learning trials than HE. AD group was able to successfully modify their predictions based on task experience. The memory predict accuracy of the AD group did not differ from the control group at postexperience. The memory prediction of the AD group was significantly better postexperience than at preexperience. Patients with AD were able to monitor their performances and subsequently use this information to derive more accurate postexoerience performance expectations.
4. Galeone et al., 2010	25 - MCI 15 - mild DA 21 - HE	• OJ • Subjective rating of memory function	• Italian Interdisciplinary network on AD • MAC-Q • Frontal Assessment Batery • Subjective rating of memory function • Objective judgement task	• Six-items questionnaire (the subject had to rate, for every items, the presence of daily life memory failures on a likert scale rating from 0 to 4. Caregivers completed an informant version of the scale in order to obtain a discrepancy score (SRD). • Objective judgement task - three lists of 10 not-semantically related words comparable for length. • The participants had to predict how many words they would be able to recall (pre-study prediction). After, they studied the 10 words of the list, one at a time for 2s each, reading each word aloud. • Subjects were asked to predict again their performance (post-study prediction) and then recalled the words of the list. • After the recall, the subject and the examiner brietly commented the task but no explicit feedback on performance was given.	• The AD performing worse than the MCI and these, in turn, worse than the HE. • While for MCI and AD accuracy did not change across the three lists, the accuracy of the HE increased from list 1 to list 3. • The three groups were more accurate at the post-list judgement only for the first list. • The HE overestimated their performance at the beginning of the trial, but progressively revised their prediction so that, at the third list, this was virtually perfect. Both AD and MCI subjects consistently overestimated their performance across the three lists. • A consistent proportion of AD and MCI subjects had reduced awareness of their memory disturbances at the clinical interview.
5. Hannesdottir et al., 2007	92 - early or unspecified AD 92 - HE	• OJD • SRD	• The experimenter rating (OJD) • SRD scale • ERS • memory test for faces • RAVLT • digit span • trail making test • Language • Visuospational function • intrusional Erros	• Objective judgment discrepancy - the subject makes a judgment on his/her performance on the memory tests. Following each memory test item, the participant was asked to estimate the percentage/number if items successfully recalled from the memory test. • Subjective rating discrepancy - Contains questions pertaining to different aspects of memory ability in everyday life. Participants were required to rate their ability to perform certain memory related activities as well as to estimate the frequency with which they made errors. Subjective rating discrepancy to different aspects of memory. For the patients, the questionnaire was also administered to informants in third person. • The experimenter rating - The scale required the experimenter to rate the level of anosognosia for memory deficit. The participant reported difficulties. This scale was administered for patients only.	• All anosognosia assessment methods used in this study (the OJD, SRD and ERS) revealed a significant difference between AD patients, showing more anosognosia for their memory functioning than the comparison group. • OJD judgement might be more highly related to monitoring of ongoing memory performance in addition to self-efficacy beliefs and memory knowledge and the on-line process, which in turn may rely on frontal lobe functioning. • The SRD and ERS measures may pick up on the development of awareness, or otherwise, in relation to integrating information about efficacy in different settings over a long period of time. The SRD Global ratings scale was significantly correlated with the SRD memory scale, but this might be predicted because the scales use similar techniques. However, the ERS measure correlated with the SRD global rating scale, but not the SRD memory scale. The ERS measure and SRD global rating scale provide a more of an overview of anosognosic deficit in general than the more specific areas explored by the SRD memory scale.
6. Souchay et al., 2003	16 - AD 6 - FTD 16 - HE	• WMS-R • FCSRT • WCST • TMT • FAS • Global Prediction Accuracy	• Global memory prediction	• Participants wrote down the number of items they believed they would recall on the final paired-associate recall test (before study prediction).	• AD and FTD patients predicted recalling as many word as control subjects. For the predictions before and after study, the analysis did not reveal any significant difference between AD patients and control group. For FTD patients, there was no significant difference for the predictions made before or after study. A significant difference between AD and controls in prediction accuracy measures both before and after study, with AD patients predicting more than they recalled and control subjects recalling more than they predict. FDT and AD patients seemed to be less accurated than control subjects in predicting their memory performance. A significant group difference between AD and FTD was found only for after-study prediction accuracy score, with FTD patients predicting more than they recalled to a greater extent than AD patients.
7. Moulin et al., 2000	16 - AD 16 - HE	• JOL • Recall readiness	• MEEM • Family Interview • Laboratory screening • Liver and thyroid function • Calcium and syphilis • Medical examination • JOL instruction	• Participants had to estimate how many times a word had been seen. And were required to remember as many as items as possible. • Three phases to this experiment: presentation, recall and recognition.	• HE group were better than AD group. • Beneficit of repetition in both groups. • Dissociation in the AD group between judgments of learning and allocation of study time. • HE showed repetition effects for both study time and their explicit judgments of how well they have learned the items and this is not the case of AD group.
8. Moulin et al., 2000	16 - AD 16 - HE	• JOL • Ranking judgment	• MMSE • Family Interview • Laboratory screening • Medical examination • Neuropsychological examination	Experiment 1 • Recall readiness task. • immediate free recall test at the end of the list, with an unlimited time to recall. • After presentation of 10 words, there was a short recall • verbal free recall of the items that they had studied.JOL task: • This was the same as the recall readiness task, except that each item appeared for only 2s and was then masked. • Participants were prompted to rate how likely it was that they would be able to recall the word later. • Experiment 2 • Ranking judgment - two successive trials of the same test. • 1. Asked to rank the words in a different order (ranked the most easy to remember to most difficult) • 2. This order was reserved.	• Giving participants as long as they like to maximize their recall performance does not improve recall. • AD recall is much lower than controls. The older adults recall significantly more easy words than difficult words. The AD group gave JOLs that were as sensitive to objective difficulty as controls. AD group spends a lot longer studying the words than controls. Examining metamemory sensitivity to items differences using both JOL and recall readiness measures, reveals no evidence of a deficit in the AD group relative to non-diseased controls. Higher JOLs for words subsequently recalled. AD group were less discriminating in their JOL ratings. No clear benefit of extra study time in recall of items in either group. AD patients were as sensitive as older adults in the ratings (JOL) they gave to items. • Memory control and recall readiness - no significant differences between groups. • recall performance was not affected by whether items were ranked from difficult to easy words or vice versa, nor did this factor interact with any other. • The HE recalled significantly more items. • Participants were sensitive to the objective differences between words and make their ranking judgements accordingly. The AD was as sensitive as HE in ranking the words, and neither group is more or less sensitive in trial 1 compared to trial 2. • Participants recalled more of words they rank as easy than the words they rank as difficult.
9. Moulin et al., 2000	16 - AD 16 - HE	• Global Judgment of performance	• Recall readiness task • Judgment of learning task	Experiment 1 • The word list comprised 5 easy and 5 difficult items. • List 1 - participants studied each word for an unlimited time. • List 2 - presentation time was fixed (2s per word) and participants had to give each word a rating of how likely they were to subsequently recall it. Experiment 2 • 10 words, 4 list; • The word list comprised: Easy unrelated (E-U), difficult unrelated (D-U), easy related (E-R) and difficult related (D-R). • Two levels of relatedness: related in which all the items came from the same semantic category, and unrelated in which none of the items came from the same semantic category and unrelated in which none of items came from the same semantic category.	• The AD patients tend to overestimate their recall performance, but that they revise their predictions downward after encoding. • AD group was less accurate overall. Both groups were more accurate in the second list. • All groups make more accurate poststudy prediction than pre-study predictions. • Only AD group revises its predictions by a significant amount once they have been presented the list. The AD group monitoring its memory performance and revises its estimates of performance. • The HE group outperforming the AD group. • More words were recalled from the easy list. The HE group was sensitive to difficultly but the AD group not. • Participants recall significantly more words from the related lists, and the AD group did not benefit from relatedness to the same extent as the HE group. • The AD group did not differentiate between easy and difficult list in their predictions. There was a strong trend in the HE group to make higher predictions of performance for easy lists. • Both groups estimate that they will recall more words from the related lists and both are aware of the benefit of semantic relatedness to recall. • AD group poststudy predictions are not sensitive to item difficultly but are as sensitive to semantic relatedness as those of the HE group. • The AD group was more discrepant in their predictions than the HE group. • Participants were more accurate in their poststudy predictions.

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[1] Michelle Brandt. Rua Garibaldi 47 / apto 103 – 20511-330 Rio de Janeiro RJ – Brazil. E-mail: michelle.neurociencias@gmail.com