1-amnestic mild cognitive impairment and probable alzheimers disease 2009

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The assessment of recognition memory using the Remember/Know procedurein amnestic mild cognitive impairment and probable Alzheimers disease

Carol Hudon a,b,*, Sylvie Belleville c,d, Serge Gauthier e

a cole de psychologie, Universit Laval, Qubec, CanadabCentre de recherche Universit Laval Robert-Giffard, Qubec, QC, CanadacCentre de recherche de lInstitut universitaire de griatrie de Montral, Montral, QC, CanadadCentre de recherche en neuropsychologie et cognition, Universit de Montral, QC, CanadaeMcGill Center for Studies in Aging, Montral, QC, Canada

a r t i c l e i n f o

Article history:Accepted 28 January 2009Available online 27 February 2009

Keywords:Alzheimers diseaseAmnestic mild cognitive impairmentRemember/KnowRecognition memoryEpisodic memoryAutonoetic consciousnessNoetic consciousnessRecollectionFamiliarity

a b s t r a c t

This study used the Remember/Know (R/K) procedure combined with signal detection analyses to assessrecognition memory in 20 elders with amnestic mild cognitive impairment (aMCI), 10 patients withprobable Alzheimers disease (AD) as well as matched healthy older adults. Signal detection analyses rstindicated that aMCI and control participants were comparable on general recognition performance. Asregards AD patients, they were impaired relative to both aMCI and healthy elders. When assessingRemember and Know responses the aMCI group showed diminished sensitivity for Remember responsesbut intact Know responses compared to healthy elders. In contrast, AD patients showed decreased sen-sitivity for both Remember and Know responses compared to control and aMCI participants. Theresponse bias index revealed that AD patients were more liberal than aMCI and control participants whenproviding Know responses. On the other measures, response bias was comparable between the groups.Overall, this study indicates that the R/K procedure can characterize different aspects of recognitionmemory performance in persons with aMCI or AD.

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1. Introduction

It is well known that Alzheimers disease (AD) is preceded by apreclinical phase during which prodromal symptoms can be de-tected. Although not widely accepted, the concept of amnestic mildcognitive impairment (aMCI) corresponds to this pre-AD stage in asignicant proportion of older adults (Gauthier et al., 2006; Peter-sen, 2004). It has been shown that episodic memory impairment inaMCI represents a sensitive marker of incipient AD (Petersen &Morris, 2003; Tierney et al., 1996). A challenge of research in thiseld is to characterize and understand the memory impairmentof elders with aMCI. To this end, one must determine which epi-sodic memory processes, or components, are defective and sparedin these persons. It is also important to determine to what extentaMCI and AD patients are comparable or different in terms of im-paired and intact memory processes. Ultimately, this will help cli-nicians identifying AD-like symptoms in older adults with aMCI,which is a prerequisite for development implementation ofadapted preventive and therapeutic interventions that could delay

the onset of AD. This in turn could potentially alleviate the publichealth issues associated with cognitive decline in aging.

Older adults with aMCI can have several types of cognitive def-icits including, for example, executive impairment (Traykov et al.,2007) and language dysfunction (Taler & Phillips, 2007). However,as emphasized in a recent review of the literature, episodic mem-ory has been by far the most studied cognitive function in olderadults with aMCI (Belleville, Sylvain-Roy, de Boysson, & Menard,2008). The memory impairment in these persons can be evidencedusing classical procedures such as delayed (Tierney et al., 1996),free (Jack et al., 1999), and cued (Ivanoiu et al., 2005) recall of aword list. The decit was suggested to result from impairment ofa number of memory processes, or components, including acquisi-tion and consolidation of information (Moulin, James, Freeman, &Jones, 2004), memory for gist and detail information (Hudonet al., 2006), and associative memory (Troyer et al., 2008). In recentyears, a number of studies have also indicated impaired perfor-mance using recognition procedures in older adults with aMCI(Barbeau et al., 2004; Bennett, Golob, Parker, & Starr, 2006; Ribeiro,Guerreiro, & De Mendonca, 2007). Recognition procedures havesome advantages over other memory tasks. One is that recognitionmemory is relatively impervious to the effect of healthy aging andthus, impairment on this kind of task might stand out as a qualita-tive marker of AD (Bennett et al., 2006). Accordingly, it has been

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* Corresponding author. Address: Centre de recherche Universit Laval Robert-Giffard, 2601, ch. de la Canardire F-4500, Qubec, QC, Canada G1J 2G3. Fax: +1 418663 5971.

E-mail address: [email protected] (C. Hudon).

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proposed that recognition procedures could help in the identica-tion of elders with aMCI who are in the process of developingdementia (Barbeau et al., 2004; Guedj et al., 2006).

Surprisingly, recognition impairment has not been constantlyreported in aMCI. For example, a previous work from the presentauthors indicated that using the Deese-Roediger/McDermott(DRM) false recognition paradigm, older adults with aMCI werenot impaired compared to healthy elders (Hudon et al., 2006). Onthe opposite, Westerberg and colleagues (2006) reported impair-ment of recognition memory in persons with aMCI and their re-sults indicated that the impairment is more important on yesno compared to forcedchoice procedures. Likewise, Bennettand colleagues (2006) showed that while persons with aMCI wereimpaired on both yesno and forcedchoice recognition tests, theyesno test was the best to predict whether or not participants be-longed to the aMCI group. The inconsistencies between the resultsof the previous studies could be explained by the fact that, as is thecase of all memory tasks, recognition is not a pure measure of puta-tive underlying cognitive processes. Successful recognition actuallydepends on a number of processes which might be differentially af-fected by AD or aMCI. According to dual-process conceptions, it hasbeen proposed that recognition memory actually reects the con-tribution of both recollection (a process involved in retrieving thecontextual information of an event) and familiarity (a process in-volved in retrieving an event with no further association with con-textual information) and that their relative contribution torecognition performance can depend on the task design. For exam-ple, recollection is more necessary for accurate performance inyesno than forcedchoice recognition tasks. On the contrary,familiarity is more important in forcedchoice than yesnotasks (Bastin & Van der Linden, 2003). Hence, performance of indi-viduals with aMCI may have varied between studies because thetasks used to assess recognition differed in terms of their prerequi-site for either process. In other words, depending on the extent towhich a given recognition task relies on altered and/or preservedmemory processes, performance of persons with aMCI woulductuate.

There are indications in the literature that recollection andfamiliarity are not equally impaired in aMCI. Namely, the resultsof Westerberg and colleagues (2006) reported above suggestedthe existence of impaired recollection and probably intact familiar-ity in aMCI. This hypothesis has been conrmed recently by Ander-son and colleagues (2008) using a process-dissociation procedurewhere a recognition task was conducted twice (with different setsof words) under inclusion and exclusion instructions. The demon-stration of intact familiarity in elders with aMCI is interesting be-cause it could well account for our previous nding ofunimpaired performance of these individuals in the DRM proce-dure (Hudon et al., 2006). Indeed, the DRM task involves presenta-tion of a very large number of related items that are thus morelikely to be recognized on the basis of familiarity processes only.

Despite increasing evidence that recollection is impaired andfamiliarity is intact in aMCI, one should note that this dissociationhas been challenged recently. First, using a Receiver OperatingCharacteristics procedure, Ally, Gold, and Budson (in press) indi-cated that elders with MCI were impaired in both recollectionand familiarity. Similar ndings were obtained by Wolk and col-leagues (2008) using two paradigms that were modications ofthe process-dissociation procedure (Jacoby, 1991) and one proce-dure that utilized the task-dissociation methodology (Yonelinas,2002). It is difcult at this point to explain why these authors haveobtained ndings different from those of Anderson and collabora-tors but in the discussion of their paper, Wolk and colleagues rec-ommended to carry out further experiments using otherparadigms in order to conrm their ndings. The Remember/Know(R/K) procedure was among their recommendations. Following this

suggestion, the present study used the R/K procedure to character-ize the recognition memory impairment of older adults with aMCI.

The R/K paradigm has been initially developed by Tulving(1985) and it is generally used in the context of yesno recognitiontasks. The paradigm requires the examinee to decide on whetherrecognition of a previously encountered event is based (Rememberresponse) or not based (Know response) on remembering of con-textual information about the event. Although there are controver-sial results (Donaldson, 1996; Wais, Mickes, & Wixted, 2008),many authors consider that Remember responses can be used toestimate recollection, whereas Know responses can be used to esti-mate familiarity (for a review, see Yonelinas (2002)). Rememberand Know responses can also be conceived as measures of two dis-tinct states of awareness in recognition memory that is, autonoeticand noetic consciousness, respectively (Gardiner & Richarson-Kla-vehn, 2000; Wheeler, Stuss, & Tulving, 1997). Autonoetic con-sciousness recreates and gives an impression of reliving previousevents and experiences. By contrast, noetic consciousness relatesto awareness of facts and events without reliving them mentally.According to both theoretical standpoints, Remember and Knowresponses are viewed as reecting cognitive processes that contrib-ute to recognition in a distinct manner (for a unitary conception,see Donaldson (1996); Starns and Ratcliff (2008)).

Several authors have used the R/K procedure to compare thememory functioning of healthy older vs. young adults. Based ontwo literature reviews (Light, Prull, LaVoie,&Healy, 2000;Yonelinas,2002), it appears that compared to young adults, healthy elders con-sistently showed decrease of Remember responses. On the otherhand, results regarding Know responses have been less consistent,with either preservation or decrease of these responses in elderscompared to young adults. According to Yonelinas (2002), the con-troversial results regarding Know responses could be accountedforby the levelof recollection in theparticipantsof each study.Whenrecollection (or Remember responses) is high, there would be de-crease of familiarity (or Know responses) in healthy aging. On theopposite, familiarity would be preserved when recollection is low.

To our knowledge, no research to date has used the R/K para-digm in older persons with aMCI. As argued above, this endeavoris necessary to better characterize and understand the recognitionmemory impairment of these individuals. Assuming that aMCI rep-resents preclinical AD in several individuals, predictions regardingthe status of Remember and Know responses in aMCI can be for-mulated based on previous studies with AD patients. Althoughthe number of such studies is limited, results revealed consistentlythat AD patients provide less Remember responses than healthyolder adults (Dalla Barba, 1997; Rauchs et al., 2007). In contrast,Know responses were reported to be either unimpaired relativeto controls (Dalla Barba, 1997) or tended to be increased (Rauchset al., 2007). These ndings suggest that the R/K paradigm can beused to distinguish between impaired and intact aspects of recog-nition memory in AD. More precisely, they are consistent with thepresence in AD of either a larger impairment of recollection overfamiliarity or a disproportionately impaired autonoetic conscious-ness over noetic consciousness. Whether the same pattern is foundin aMCI is unknown as, to our knowledge, no studies have used theR/K procedure in these persons.

To summarize, there has been a recent proliferation of studiessuggesting impaired recognition memory in elders with aMCI.However, there is uncertainty in the literature regarding the sourceof the recognition impairment in these individuals. The principalobjective of the present study was to characterize the recognitionmemory impairment of older adults with aMCI and patients withprobable AD using the R/K paradigm. Another objective was tocompare the performance of aMCI and AD patients in order todetermine to what extent the pattern of impairment of these indi-viduals is similar, both quantitatively and qualitatively. Three

172 C. Hudon et al. / Brain and Cognition 70 (2009) 171179


groups of participants (aMCI, AD, healthy older adults) were as-sessed using a yesno recognition task that required the produc-tion of Remember and Know responses for items recognizedcorrectly (hits) or erroneously (false alarms) by the participants.One important and original aspect of our study was to complementthe calculation of response rates by the inclusion of signal detec-tion analyses. Signal detection allows calculating indices of mem-ory that are independent of the response bias of the participants.The information provided by this method regarding response biasand decision criterion is critical for a proper interpretation of yes/no judgement tasks. It is also important for proper interpretation ofthe rate of Remember and Know responses. Based on the literaturein AD patients, it was hypothesized that Remember responseswould be diminished in both aMCI and AD groups compared tohealthy older adults. As regards Know responses, no impairmentshould be observed in any clinical group.

2. Methods

2.1. Participants

The participants in this study included 22 older adults withaMCI and 17 patients with probable AD. From these cohorts, twoindividuals with aMCI and seven patients with AD were excludedfrom the analyses because they did not understand the R/K instruc-tions. The following analyses were thus performed using the dataof 20 persons with aMCI and 10 patients with AD. This study alsoincluded a group of 23 healthy older adults matched for age andeducation to aMCI and AD participants.

Older adults with aMCI were recruited from consecutivelyencountered patients in memory clinics. They were diagnosed asaMCI by experienced neurologists or geriatricians. All participantsfrom this group met the criteria for single-domain aMCI (n = 3) ormultiple-domain aMCI (n = 17), as proposed by Petersen (2004).They all had a memory complaint, which was corroborated byan informant when possible. All aMCI participants had impairedperformance (more than 1.5 SD below expected performancebased on normative data) on any of the memory tests used inthe neuropsychological battery (see below for the description ofthe battery). Those with single-domain aMCI had no other cogni-tive impairment whereas persons with multiple-domain aMCI hadimpaired performance in one or more other cognitive domain. Noparticipant had a signicant decrease of functional autonomy. Fi-nally, no aMCI individual had dementia on the basis of the clinicalassessment.

Contrary to aMCI participants, patients with AD met the criteriaof the National Institute of Neurological and Communicative Disor-ders and Stroke-Alzheimers Disease and Related Disorders Associ-ation (McKhann et al., 1984) for probable AD and the DSM-IVclinical criteria for dementia of the Alzheimer type (American Psy-chiatric Association., 1994). They were diagnosed by experiencedneurologists or geriatricians. Participants were included in theAD group if the severity of their illness was mild (n = 6; scoreP 24on the Mini-Mental State ExaminationMMSE), or mild-to-moder-ate (n = 4; score between 18 and 23 on the MMSE).

To summarize, the diagnosis of aMCI and AD was done based onclinical information. It relied on current validated clinical criteria(NINCDS-ADRDA and DSM-IV) and was done by clinicians whowere not informed of the patients scores on the experimental task.

Healthy older adults were volunteers recruited from the com-munity through advertisements. They had good physical and men-tal health and they showed normal cognitive functioning i.e., theyall scored above the 1.5 SD cut-off on standardized neuropsycho-logical tests (see below). The control participants were matched topatients according to age and years of education.

All participants completed a comprehensive battery of clinicaland neuropsychological tests (see Table 1). The battery includedmeasures of depressive symptoms (Hoyl et al., 1999), instrumentalactivities of daily living (Hbert, Guilbault, Desrosiers, & Dubuc,2001), general cognitive status (Folstein, Folstein, & McHugh,1975), executive functions (Regard, 1981), information processingspeed (Wechsler, 1997), visuoconstructive abilities (Rey, 1960), vi-sual perception (Benton, Hamsher, Varney, & Spreen, 1983), nam-ing (Calero, Arnedo, Navarro, Ruiz-Pedrosa, & Carnero, 2002), andepisodic memory (Rey, 1960; Signoret, 1991; Van der Linden, Coy-ette, Poitrenaud, & GREMEM, 2004). Age-stratied norms wereused for all neuropsychological tests. Testing and scoring of thesetests were accomplished by the rst author and by senior researchassistants (RA) with a masters degree in neuropsychology. The RAswere supervised by the second author, who is an experienced scho-lar in clinical neuropsychology.

General exclusion criteria for all participants were: (1) history oftraumatic brain injury; (2) history of stroke (and other cerebrovas-cular disorders) or transitory cerebral ischemia; (3) former intracra-nial surgery; (4) history of neurological disorder of cerebral origin orassociatedwith another dementia state (e.g., multiple sclerosis, par-kinsonism, frontotemporal dementia); (5) history or actual diagno-sis of a psychiatric illness according to the DSM-IV (AmericanPsychiatric Association, 1994) criteria; (6) presence or history ofalcoholism/drug addiction according to the clinical criteria of theDSM-IV (American Psychiatric Association, 1994); (7) unstablemet-abolic or medical condition (e.g., uncontrolled diabetes, hypothy-roidism); and (8) general anesthesia in the last 12 months.

French was the primary language for every participant. All indi-viduals received monetary compensation (15$ per session) fortheir involvement in the study. Written informed consent was ob-tained at the start of the rst evaluation according to the declara-tion of Helsinki. The study was approved by the Ethical ResearchCommittee of the Institut universitaire de griatrie de Montral.

2.2. Materials

To construct the R/K test, a set of 60 concrete (e.g., fentrewin-dow) and abstract (e.g., angoissedistress) French words was rstdetermined. All words corresponded to frequent written or spokenwords according to the BRULEX database (Content, Mousty, & Ra-deau, 1990). Most of the selected words had two or three syllablesbut two items had four syllables. The selected words were dividedin two sets of 30 words. These two sets were comparable in termsof frequency and number of syllables of the words. One set in-cluded the 30 items that was presented during the study phaseand that were shown again as target items in the recognitionphase. Words in the other set of 30 items were used as lures inthe recognition phase. The phase during which each word setwas used was counterbalanced across participants. The experimentwas implemented and run with Psyscope 1.2.5 (Cohen, MacWhin-ney, Flatt, & Provost, 1993). Instructions were presented on thecomputer screen using Chicago 18 point font. Study words andlures were presented using Courrier 36 point font.

2.3. Procedure

Participants were assessed individually over two testing ses-sions. The neuropsychological battery described above was admin-istered during the rst session. The R/K procedure wasadministered 1 week later.

In the second testing session, participants sat approximately 1 min front of the computer screen and were informed that they wouldperform amemory test. In order to help the examinees understand-ing theR/K instructions, the experimentbeganwitha trainingphase.The instructionswere presented on the screen andwere read by the

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examiner. To maximize understanding of the distinction betweenRemember and Know responses, examinees were provided withtwo examples. In the rst example, which referred to a daily livingsituation, the examiner said: Imagine you recognize a person youencounter. If you can tell the name of that person, the place(s) you al-ready met her, etc., you can then say that you remember the person.On the contrary, if you recognize the person but cannot tell anything elseabout her, you could only say then that you know her. Another exam-ple was provided for application to a list of words (e.g., I rememberthat I thought about my last trip when I saw the word aircraft or Iknow the word aircraft was in the list, but I cannot remember any-thing else). Then the procedure for training proceeded in a manneridentical to that of the experimental phase (see below), but onlyeight words (four targets, four lures) were used.

In the study phase, 30 words were presented sequentially andrandomly in the center of the computer screen at a rate of 5 s perword. Participants were asked to read the words out loud and tryto memorize them. Between each item there was a 500 ms delay.Following the study phase, therewas a retention interval of approx-imately 5 min lled with an open discussion between the examineeand the examiner. Then, the recognition test was administered.Words that had to be recognized were presented sequentially and

randomly. Participants were asked to tell whether or not the wordsappearing on the screen had been studied previously. Words re-mained on the screen until the participants gave a response. Whenthe participant judged that the itemhadnot been studied previously(no response), the examiner presented the nextword in the recogni-tion list. Conversely, when the participant judged that the word hadbeen studied previously (yes response), the examiner instructedhim/her to indicatewhetherany information fromtheencodingcon-text could be remembered (Remember response), or if the word wasrecognized in the absence of any additional information regardingthe learning context (Know response). The R/K instructions were gi-ven following both hits and false alarms. Examinees were asked tobriey explain their response in order to ensure that they under-stood the difference between Remember and Know judgmentsthroughout the experiment. There were no time limits for givingyesno or R/K responses.

2.4. Data analyses

The analyses rst considered the general recognition perfor-mance of the participants taking into account the proportions ofhits and false alarms following yesno responses, as classically

Table 1Means (SD) and signicance levels of demographic and neuropsychological characteristics of participants.

Measure Controls aMCI AD ANOVA

(n = 23) (n = 20) (n = 10) F (2, 52) p

Participants characteristicsAge (years) 68.6 (8.2) 66.1 (7.6) 74.9 (7.0)a 4.3 .019Education (years) 14.7 (4.1) 14.6 (4.2) 13.7 (3.9)


measured. Namely, the hit score corresponded to the proportion oftrials for which participants responded yes to old items. The falsealarm score corresponded to proportion of trials for which partici-pants responded yes to new items. Then, because the hit and falsealarm rates can be inuenced by the decision criterion of the indi-viduals, we combined these scores to calculate an index of mem-ory, or sensitivity (A), that was independent of the responsecriterion (B00D) (see Donaldson, 1996). The A index is preferred overthe d score when distributions are not normal. Furthermore, Snod-grass and Corwin (1988) have shown that A is more appropriateand more sensitive than d in memory-impaired populations suchas AD patients. The A score ranges between 0 and 1, with 0.5 rep-resenting performance at chance level; higher scores indicate gooddiscrimination between old and new items. The B00D score rangesbetween 1 and 1; negative values indicate liberal respondingand positive values reect conservative bias. The A and B00D formu-las used in the present study were those that must be appliedwhen performance of participants is characterized by higher num-ber of hits compared to false alarms (see Snodgrass & Corwin,1988).

Data were then analyzed by taking into account the subjectiveexperience of the participants in recognizing items. These analysesseparated Remember responses and Know responses. First, propor-tions of Remember (or Know responses) were computed on hitsand false alarms. As in the meta-analysis of Donaldson (1996),the denominator for determining the proportions was the totalnumber of possible hits or false alarms. In the present study, thedenominator was thus 30 in all cases. It corresponded to totalnumber of possible hits or false alarms. Second, we calculatedagain indices of sensitivity (A) and response criterion (B00D) usingthe method described above.

Finally, some authors have proposed that the probability to giveKnowresponses shouldbeestimatedusingan independencemethod.This is based on the fact that in the R/K procedure, Know responsesare independent from Remember ones (i.e., only one type of re-sponse is permitted for every given item). The examinees are in-structed to give a Know response when an item is familiar and notrecollected. However, there is evidence in the literature that Knowresponses can reect multiple processes and not only familiarity(see Yonelinas (2002)). Analyzing only the proportion of Know re-sponses alone can hence lead to an underestimation of the familiar-ity process (Yonelinas, 2002). According to the independencemethod, thehit and false alarmrates of Knowresponses are adjustedto consider the probability that items given a Remember responseare familiar to some extent. A corrected estimate of Know responsescan be derived from the following formula, as described in Yonelinas(2002): F = Know/(1 Remember). The result of the computationprovides an estimate of the probability that an item received a Knowresponse given it did not receive a Remember response.

The statistical analyses were performed using SPSS 13.0. (SPSSInc., Chicago, Il). On demographic (age, education) and clinicalmeasures, the aMCI and AD groups were compared to theirmatched controlled group using one-way ANOVAs. The distribu-tions of gender in the groups were compared using the PearsonChi-Square test. In the experimental task, group comparisons wereperformed on each measure. Given the signicant mean age differ-ence between the participants of the aMCI and AD groups, datafrom the experimental task were entered in different ANOVAs withGroup as a between-subject factor and Age as a covariate. To com-pare main group effects, pairwise comparisons were also calcu-lated on each dependent variable using the Bonferroniadjustment for multiple comparisons. Finally, Pearson r correla-tions were used in the aMCI and AD groups to estimate the associ-ation between performance on the R/K task and that of a clinicaltest (RL/RI-16) assessing episodic memory. In all analyses above,the alpha level was set at p 6 .05.

3. Results

3.1. Demographic and clinical data

Table 1 presents the demographic and clinical characteristicsof the participants. The three groups were comparable in termsof years of education and gender distribution. However, therewas a signicant difference regarding the mean age of partici-pants. This was due to the fact that patients from the AD groupwere signicantly older than participants from the aMCI group(p < .05). As a result, the age factor was used as a covariate.

On clinical measures, participants from all groups reportedvery few depressive symptoms and they were comparable onthat measure. As regards IADLs, the aMCI group was compara-ble to control individuals, but the AD group was signicantlyimpaired compared to both control and aMCI participants. Theneuropsychological measures indicated that aMCI participantswere signicantly impaired relative to the control group ontasks of information processing speed and verbal episodicmemory (i.e., immediate and delayed story recall and meannumber of words on the free recall trials of the RL/RI-16 test).AD patients showed signicant impairment relative to healthycontrols in all cognitive domains. They were also impaired com-pared to aMCI participants on all tests, except Digit Symbol andBoston Naming.

Table 2 reports the four indices (hits, false alarms, sensitivity,and response bias) obtained on general recognition, Remember re-sponses, and Know responses. Furthermore, the table includes theresults (F and p values) of the Group and Age effects for eachdependent variable.

3.2. General recognition performance

The analyses of general recognition performance revealed thatall groups were comparable in terms of hit rate. On the false alarmrate, aMCI participants were comparable to healthy older adults,but AD patients made signicantly more false alarms than boththe control and aMCI groups. Regarding the sensitivity score (A),the analyses revealed that persons with aMCI were comparableto control elders in discriminating old versus new items. As forthe AD patients, this score was signicantly impaired comparedto both matched controls and aMCI participants. Finally, aMCI par-ticipants had a neutral-to-conservative response bias (B00D) andthey did not differ from controls on that measure. The criterionof AD patients was somewhat liberal being on average below zero.The response criterion of AD patients was similar to that of aMCIparticipants. Relative to control individuals, the response criterionof the AD group was seemingly dissimilar but the difference wasnot signicant statistically (p = .052).

3.3. Remember and Know responses

Remember responses given by the participants on hits werediminished in both aMCI and AD relative to the control individualsand there was no difference between the former groups on thatmeasure. On false alarms, persons with aMCI were comparable tocontrol participants. However, AD patients gave signicantly moreRemember responses following a false alarm compared to healthyolder adults. When the sensitivity score was considered, the anal-yses revealed that both aMCI and AD groups were impaired com-pared to healthy older adults. The AD group also performedworse than persons with aMCI. Finally, all groups were comparableas regards the response bias. Namely, the three groups in this studyused a conservative criterion on average when they gave Remem-ber responses.



The Know responses on hits were comparable between groups.For the Know responses on false alarms, aMCI participants werecomparable to control participants. However, the AD group gavemore Know responses following a false alarm relative to both con-trol and aMCI participants. The same pattern of results was ob-tained concerning the sensitivity score. Namely, while the aMCIand control groups were comparable, the AD group was impairedrelative to both control and aMCI participants. Finally, the responsebias scores indicated the presence of a comparable conservativecriterion between aMCI and control participants. On the otherhand, the criterion was signicantly less conservative in the ADgroup than in the control and aMCI groups.

Know responses were further analyzed using the independencemethod. This provided a corrected Know level that takes into ac-count the Remember level. Results are presented in Table 3. Usingthis method, both the aMCI group and the AD patients had intactprobability of Know responses compared to healthy older adults.

A last series of analyses examined whether performance ofaMCI and AD patients in the R/K (as assessed by the different sen-sitivity indices) was associated with performance on two clinicalmeasures of episodic memory (free and total recall scores on theRL/RI-16). Results of the Pearson r correlations are reported in Ta-ble 4. Overall, the analyses in the aMCI group revealed that Recog-nition and Remember sensitivity scores were signicantlyassociated with both free and total recall as assessed by the RL/RI-16. However, there was no association between the sensitivity

index for Know responses and the two clinical measures of epi-sodic memory. In the AD group, no signicant correlation was ob-served between the experimental and clinical measures.

4. Discussion

The principal objective of this study was to better understandand characterize the recognition memory decit of older personswith aMCI or AD. This was done using the R/K procedure and byanalyzing responses based on the signal detection theory. Anotherobjective was to compare, both quantitatively and qualitatively,performance of aMCI and AD participants on the R/K task. On gen-eral recognition performance, results from the signal detectionanalyses indicated no impairment in aMCI participants comparedto control individuals. However, AD patients were signicantly im-paired on this measure relative to both aMCI and healthy elders.When assessing separately performance on Remember and Knowresponses, signal detection revealed that Remember responseswere signicantly diminished in both aMCI and AD groups com-pared to control participants, with more severe impairment inthe AD than in the aMCI group. Know responses were comparablebetween aMCI and healthy elders, but they were diminished in theAD group compared to both control and aMCI groups. Of note, theimpairment of Know responses in AD patients was not evidencedwhen using the independence method. In sum, the present ndingsreveal that the R/K procedure can characterize performance on rec-

Table 2Means (SD) and signicance levels of different estimates of hits, false alarms, sensitivity (A) and response bias (B00D) of participants.

Measure Controls aMCI AD Group effect Age effect

(n = 23) (n = 20) (n = 10) F(2, 52) p F (1, 52) p

RecognitionHits 0.87 (0.11) 0.83 (0.16) 0.75 (0.20) 1.4 .260 6.8 .012False alarms 0.08 (0.10) 0.12 (0.13) 0.45 (0.30)***c 15.4 .000 1.3 .263Sensitivity (A) 0.89 (0.10) 0.83 (0.11) 0.62 (0.13)***b 16.5 .000 5.0 .030Response bias (B00D) 0.39 (0.68) 0.15 (0.68) 0.28 (0.71) 3.1 .056


ognition memory tasks in aMCI and AD patients. This study alsoindicates that the R/K procedure can distinguish memory perfor-mance of aMCI persons from that of healthy elders or AD patients.

Before discussing these ndings, it is important to note that thenumber of test items was relatively small in the present studycompared to what is used in studies of younger adults relying onthe R/K procedure. A fairly small number of items were used to re-duce the likelihood of a oor effect in AD patients. However, onecould argue that our task was too simple for the control group, thusyielding possible ceiling effects in some of these participants. Inturn, this could have skewed to some extent the response bias(B00D) results. However, close inspection of the data revealed thatonly two control participants (8.7%) had a hit rate of 1. Thus, therewas no signicant ceiling effect in participants of the controlgroup.

The absence of general recognition impairment in the aMCIgroup is at odd with recent studies indicating that recognitionmemory is impaired in these persons (Barbeau et al., 2004; Bennettet al., 2006; Ribeiro et al., 2007; Westerberg et al., 2006) but con-sistent with other studies indicating unimpaired recognition (Hu-don et al., 2006). These differences across studies could arisefrom methodological differences (number of items, time to recog-nition, etc.), from differences in patient characteristics, from sam-ple size issues or nally, from differences in the processes thatare involved in the recognition task used. As regards the AD group,the recognition impairment was signicant in the present studyand conrmed previous ndings with similar samples (Diesfeldt,1990; Hudon et al., 2006).

Interestingly, despite the absence of general recognition impair-ment in the aMCI group, there was a dissociation between im-paired Remember and intact Know responses in theseparticipants. This pattern of results has implications for neuropsy-chological assessment of older adults. It emphasizes the impor-tance of assessing the processes involved in recognition memoryin the context of early diagnosis of AD. That is, an individual withaMCI may apparently show no decit of recognition memory basedon age- and education-stratied norms but the use of more renedtests can reveal selective disturbances of some of the underlyingprocesses. On the whole, the present results suggest that the nat-ure of the subjective experience of older adults while performinga recognition judgement task might help differentiating those withaMCI from those with healthy cognitive aging.

The present study also suggests that the R/K procedure can helpdifferentiating aMCI from AD patients. Namely, contrary to aMCIparticipants, patients from the AD group showed impairment forboth Remember and Know responses. The decrease of Rememberresponses in our AD group agrees with results from previous stud-ies (Dalla Barba, 1997; Rauchs et al., 2007). However, the decreaseof Know responses evidenced in the present AD sample differsfrom results of previous work showing preserved Know responses

in these patients (Dalla Barba, 1997; Rauchs et al., 2007). The dis-crepancy between the present and previous ndings can be ac-counted for by differences in the methods used to estimate Knowresponses. This is well illustrated in the present study as therewas signicant impairment in the AD group using signal detectionanalyses, but no impairment using the independence method. Theuse of signal detection in the present study had the advantage oftaking into account the response bias of examinees. Hence, inspec-tion of Table 2 clearly indicates that while AD produced a largenumber of Know responses on words that have been presented,they also produced numerous Know responses on words that havenever been presented in the study phase. This pattern is reectedby their low sensitivity index and by their somewhat neutral re-sponse bias for Know responses. Unfortunately, response bias isnot taken into account using the independence method and thisis probably the reason why no impairment was revealed in AD pa-tients using this approach.

In the aMCI group, there were signicant correlations betweenperformance on the clinical memory measures and the sensitivityindices for general recognition performance and Remember re-sponses. Interestingly, clinical memory measures were not relatedto Know responses. This provides some validity to the use of freeand total recall measures for clinical diagnosis and characterizationof aMCI. Furthermore, this pattern of results may suggest thatRemember and Know responses do not rely on similar memoryprocesses. Thus, by itself the correlation analyses provide somesupport to the dual-process theories of memory. In AD patients,though the correlations were in the same direction as the aMCIgroup, they failed to reach signicance. This is probably due tothe fact that other factors account for the variance in this more se-vere group of participants. In addition, because our study was notdesigned to do correlation analyses, it was also somewhat under-powered here.

One may note that the response bias of AD patients was ratherliberal for general recognition (B00D = .28) but either very conser-vative for Remember responses (B00D = .82) or somewhat conserva-tive for Know (B00D = .32) responses. To explain this intriguingpattern, one must rst consider that using the B00D estimate, the re-sponse bias for Remember and Know responses is independentfrom the response bias for general recognition performance. Inaddition, the response bias results suggest that AD patients saidold most of the time when they were instructed to distinguishbetween old and new items during recognition performance. How-ever, when these patients were asked to qualify their subjectiveexperience during recognition, they provided Remember responsespreferentially in the presence of hits. On a cognitive perspective,this could be accounted for by the fact that Remember responsesnecessitate the use of specic (or contextual) information encodedwith the items and memory for this type of information is likely se-verely impaired in AD patients. Thus, AD may be more inclined to

Table 4Correlations between the sensitivity (A) indices in the Remember/Know task and performance on a clinical episodic memory test.

Measure aMCI AD

Recognition (A) Remember (A) Know (A) Recognition (A) Remember (A) Know (A)

RL/RI-16 free recalla Pearson r coefcient .494 .467 .350 .330 .442 .205p .027 .050 .131 .352 .201 .570n 20 18 20 10 10 10

RL/RI-16 total recallb Pearson r coefcient .550 .694 .238 .308 .419 .348p .012 .001 .313 .387 .228 .324n 20 18 20 10 10 10

Abbreviations: aMCI = elderly persons with amnestic mild cognitive impairment; AD = patients with probable Alzheimers disease; RL/RI-16 = preuve de rappel libre/rappelindic 16 items.

a This score was calculated as the mean number of words retrieved over the three free recall trials.b This score was calculated as the mean total number of words retrieved on all free plus cued recall trials.



provide Remember responses for hits because those may be theonly items for which they have encoded or retained contextual de-tails. On the other hand, general recognition performance or theformulation of Know responses would rely on a more general sub-jective feeling and accordingly, the associated response bias wouldbe more liberal. Obviously, this is a speculative interpretationwhich would deserve further investigation.

Parallels can be made between the present results and thosefrom studies that investigated recollection and familiarity with dif-ferent procedures. First, despite the existence of contradictoryndings (Ally et al., in press; Wolk, Signoff, & Dekosky, 2008), thedecrease in Remember responses and the preservation of Know re-sponses observed in aMCI are consistent with studies supporting adissociation between impaired recollection and intact familiarityin similar samples (Anderson et al., 2008; Westerberg et al.,2006). Second, the decrease in both Remember and Know re-sponses in the AD group coincide with the hypothesis that bothrecollection and familiarity are impaired in this clinical condition(Westerberg et al., 2006). Be this as it may, and because there isa debate in the literature regarding the processes assessed byRemember and Know responses (Donaldson, 1996; Wais et al.,2008), one could question the idea that our R/K procedure actuallymeasured recollection and familiarity. According to an alternativeconception, Remember and Know responses can be conceived asmeasures autonoetic and noetic consciousness, respectively (Gard-iner & Richarson-Klavehn, 2000; Wheeler et al., 1997). The presentstudy was not aimed at resolving this theoretical debate. It never-theless indicates that the R/K paradigm can dissociate different as-pects of recognition performance, as other procedures (e.g.,process-dissociation) did in the past.

To some extent, the results of the present study may haveimplications for better understanding of the evolution of the neu-ropathology of AD from its preclinical to its clinical phase. For in-stance, previous studies have shown that recollection is relatedto hippocampal and parahippocampal activity while familiarity isprincipally associated with the activity in the perirhinal cortex(for a review, see Diana, Yonelinas, & Ranganath, 2007). Therefore,our results may point to a shift from hippocampal/parahippocam-pal pathology in aMCI to hippocampal/parahippocampal plus peri-rhinal pathology as individuals decline towards AD. Thisinterpretation does not necessarily imply that perirhinal abnor-malities are absent in elders with aMCI. On the contrary, one couldenvision that the presence of perirhinal pathology (and hence im-paired familiarity) in older adults with aMCI could represent agood predictor of future AD in these persons. This hypothesis willneed to be validated in longitudinal studies that include largersamples as well as neuroimaging techniques.

Our results have additional implications at the clinical level. Be-sides the importance of assessing the processes involved in recogni-tion memory in older adults, as discussed above, the present studyemphasize the need to develop sensitive clinical tests to distinguishbetween the intact and impaired memory processes in aMCI or toknow better which process is tapped by the tools that are currentlyused in clinical settings. This is a prerequisite for accurate diagnosisof older adults presenting with a memory complaint and for thedevelopment of adapted non-pharmacological interventions.

Some limitations of the present study deserve mention here.The rst is that our R/K procedure did not include the possibilityfor participants to provide Guess responses. Although previousauthors have shown that Guess responses are not fundamentallydifferent from Know responses (Hirshman, 1998) and that resultsof studies using Guess responses did not differ importantly fromresults of studies using the original R/K paradigm (Yonelinas,2002), one could argue that without the possibility of guessing,Know responses may be more likely. This could be especially thecase in persons with memory problems such as aMCI and AD pa-

tients. Indeed, persons with aMCI or AD have memory impairment(and potentially poor meta-memory) and thus, uncertainty regard-ing the studied vs. unstudied status of items is more likely in thesegroups. Since Know responses are typically given when one is lesssure that an item has been previously studied (Rotello, Macmillan,Reeder, & Wong, 2005), one could argue that Know responses weremore likely and Remember responses less likely in our aMCI andAD groups. These hypotheses will need to be veried in the future.

The second limit of this study relates to the constraints regard-ing the use of the R/K procedure in clinical settings. This task islengthy and its instructions can be difcult to understand in per-sons with memory impairment. An alternative procedure to assessthe subjective experience of patients on a recognition task could becondence rating (on a n-point scale). Recollection processesshould yield only high-condence recognition responses. In con-trast, familiarity would yield a wide range of condence responses.In the future, it would be interesting to investigate the sensitivityand the reliability of this kind of task in aMCI and AD patients. In-deed, condence-rating instructions are less complex than that ofthe R/K paradigm and thus, the former procedure could be moreamenable to patients with memory impairment.

The last limitation relates to the generalization of the results.The sample size were rather small and there was twice as manyaMCI as AD participants. Given the typical variability in cognitivedecits among AD patients, this could affect to some extent theconsistency of the results. In addition, the exclusion criteria inthe present study were very extensive. While this was aimed atinvestigating aMCI participants who were mainly in a pre-ADphase, it makes difcult the generalization of the results to thewhole aMCI population.

In conclusion, the present study indicated a decline of Remem-ber responses but intact Know responses in aMCI compared tohealthy older adults. In AD, Remember and Know were diminishedwhen response bias was considered. Hence, this study indicatesthat the R/K procedure can characterize different aspects of recog-nition memory performance in persons with aMCI or AD. Futurestudies should be conducted in order to determine to what extentthe present ndings are specic to aMCI and early AD among el-derly people. Meanwhile, we recommend for clinical practice toconsider assessment of recognition memory and its underlyingprocesses in older adults presenting with memory decits and,more particularly, in patients with aMCI.

Acknowledgements

This work was supported by a research grant from the CanadianInstitutes of Health Research (MOP-38063) and a Chercheur Na-tional Award from the Fonds de la recherche en sant du Qubec(FRSQ) to SB. It was also supported by postdoctoral scholarshipsfrom La Fondation des Gouverneurs (Institut universitaire de gri-atrie de Montral) and the Alzheimer Society of Canada to CH. Theauthors are grateful to E. Lepage, C. Proulx, and B. Boudia for theirassistance with the testing of participants, and to M.J. Kergoat(IUGM), H. Chertkow (Bloomeld Centre for Research in Aging),and V. Plante (Centre hospitalier universitaire de Qubec) for refer-ring aMCI and AD participants.

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