Recollection and Familiarity in Amnesic Mild Cognitive Impairment

Laura Serra, Marco Bozzali, Mara Cercignani,and Roberta Perri

Foundation IRCCS Santa Lucia, Rome

Lucia Fadda, Carlo Caltagirone,and Giovanni A. Carlesimo

University of Rome Tor Vergata, Rome and Foundation IRCCSSanta Lucia, Rome

Objective: To investigate whether, in patients with amnesic mild cognitive impairment (a-MCI), recog-nition deficits are mainly due to a selective impairment of recollection rather than familiarity. Methods:Nineteen patients with a-MCI and 23 sex-, age-, and education-matched healthy controls underwent twoexperimental investigations, using the Process Dissociation Procedure (PDP) and the Remember/Know(R/K) procedure, to assess the differential contribution of recollection and familiarity to their recognitionperformance. Results: Both experimental procedures revealed a selective preservation of familiarity ina-MCI patients. Moreover, the R/K procedure showed a statistically significant impairment of recollec-tion in a-MCI patients for words that were either read or anagrammed during the study phase.Conclusions: A-MCI is known to be commonly associated with a high risk of conversion to Alzheimer’sdisease (AD). Several previous studies have demonstrated a characteristic impairment of episodicmemory in a-MCI, with an early dysfunction of recognition. Our findings are consistent with theknowledge of neurodegeneration occurring in AD, which is characterized, at the earliest disease stages,by a selective involvement of the entorhinal cortex. Moreover, the current study supports the dual processmodel of recognition, which hypothesizes recollection and familiarity to be independent processesassociated with distinct anatomical substrates.

Keywords: memory, recollection, familiarity, mild cognitive impairment

Mild cognitive impairment (MCI) is commonly associated witha high risk of conversion to Alzheimer’s disease (AD), with anestimated conversion rate of 10–15% per year (Petersen et al.,2001). Several clinical presentations of MCI have been described(Davis & Rockwood, 2004). In the most common condition, mem-ory loss is the predominant symptom (amnesic MCI, a-MCI).Although a-MCI is considered to be the most frequent prodromalstate of AD (Petersen et al., 2001), this condition includes aheterogeneous group of subjects with different rates of conversionto dementia (Larrieu et al., 2002).

Neurofibrillary tangles and amyloid plaques are the neuropatho-logical landmarks of AD. Neurofibrillary tangles initially involvethe entorhinal cortex, which is part of the mesial temporal lobe(MTL). Subsequently, they extend to Ammon’s horn and otherneocortical areas (Braak & Braak, 1995; Gomez-Isla et al., 1996).Conversely, from the earliest stages of the disease, the depositionof amyloid plaques is more prominent in the neocortical structures(Markesbery et al., 2006). This succession of pathophysiologicalevents that take place in the brains of AD patients is thought tounderlie their progressive clinical manifestations. In this perspec-tive, the subjective memory impairment experienced by individu-als with a-MCI might be further characterized using more specificneuropsychological instruments.

There is a broad consensus that at least two types of processesare involved in episodic memory recognition: recollection, theconscious reexperience of a previous event, and familiarity, thefeeling of having previously encountered a stimulus with no asso-ciated contextual information (Hintzman, Caulton, & Levitin,1998; Mandler, 1980; Yonelinas & Levy, 2002). Indeed, severalempirical dissociations have been reported in the literature docu-menting the reciprocal independence of recollection and familiar-ity. First, a variety of experimental manipulations of memorytasks, regarding either the encoding or the retrieval phase, havebeen shown to exert different (and sometimes opposite) effects onrecollection and familiarity (Yonelinas, 2002). For example, it hasbeen repeatedly demonstrated that meaning-based compared withperceptual-based encoding of the material to be learned increasesrecollection more than familiarity; conversely, changing the per-ceptual characteristics of the memorandum between study and testphase (e.g., changing the presentation modality from visual toauditory) leads to a decrease in familiarity but not recollection.Second, in healthy individuals, dissociable electrophysiological(e.g., Klimesch et al., 2001) and functional neuroimaging patterns(Daselaar, Fleck, Prince, & Cabeza, 2006; Yonelinas, Otten, Shaw,& Rugg, 2005) have been correlated with recollection and famil-iarity. In particular, Skinner and Fernandes (2007) reported thatrecollection processes recruit additional cortical areas at the levelof frontal and parietal lobes with respect to familiarity processesand that these two memory processes are related to activation indifferent regions of the MTL. Finally, there is neuropsychologicalevidence that recollection and familiarity have separable anatom-ical and neurochemical substrates within the MTL (Aggleton &Brown, 1999; Bozzali, MacPherson, Dolan, & Shallice, 2006;Henson, Hornberger, & Rugg, 2005). Indeed, although patientswith damage confined to the hippocampal formation are selec-

Laura Serra, Marco Bozzali, and Mara Cercignani, Neuroimaging Lab-oratory, Foundation IRCCS Santa Lucia, Rome; Roberta Perri, Clinical andBehavioural Neurology, Foundation IRCCS Santa Lucia, Rome; LuciaFadda, Carlo Caltagirone, and Giovanni A. Carlesimo, Department ofNeuroscience, University of Rome Tor Vergata, Rome, and Clinical andBehavioural Neurology, Foundation IRCCS Santa Lucia, Rome.

Correspondence concerning this article should be addressed to GiovanniA. Carlesimo, Fondazione IRCCS Santa Lucia, Via Ardeatina 306, 00179Rome, Italy. E-mail: memolab@hsantalucia.it

Neuropsychology © 2010 American Psychological Association2010, Vol. 24, No. 3, 316–326 0894-4105/10/$12.00 DOI: 10.1037/a0017654

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tively impaired in the recollection component of episodic retrieval(Bastin et al., 2004; Turriziani, Serra, Fadda, Caltagirone, & Car-lesimo, 2008; Yonelinas et al., 2002), a recent single-case study(Bowles et al., 2007) reports poor familiarity but normal recollec-tion following a surgical resection of the left perirhinal cortex.However, some authors do not support this view, considering thehippocampus and the perirhinal cortex as structures that cooperatein recollection and familiarity processes (Squire, Wixted, & Clark,2007).

From a neuropsychological perspective, a number of differentapproaches have been used to estimate the relative contribution ofrecollection and familiarity to recognition (see Yonelinas, Kroll,Dobbins, Lazzara, & Knight, 1998, for a review). One method isthe so-called Process Dissociation Procedure (PDP; Jacoby, 1991),which is based on the assumption that when subjects recognize anitem by recollection they should also be able to determine whenand where they initially studied it; by contrast, familiarity-basedrecognition does not imply the retrieval of additional contextualinformation. In this procedure, the relative contribution of recol-lection and familiarity to recognition memory can be separated bycomparing the performance obtained at a traditional memory task(in which recollection and familiarity affect performance in thesame direction) with that obtained at a memory task in which theeffects of recollection are placed in opposition to those of famil-iarity. Another approach for quantifying recollection and familiar-ity is the Remember/Know Procedure (R/K; Tulving, 1985), inwhich participants are requested to give a subjective judgment ofthe nature of their recognition, responding “remember” if they canconsciously recollect a previously studied item or “know” if theyfeel an item only familiar in absence of a sure recollection. Then,the probability of “remember” responses can be used as an indexof recollection, while the probability that an item is familiar isequal to the conditional probability that it received a “know”response because it was not recollected (Yonelinas & Jacoby,1995).

So far, only a few studies on a-MCI patients have investigatedthe relative contribution of recollection and familiarity to theirrecognition performance. In the first of these studies (Westerberget al., 2006), a dissociation in individuals with a-MCI betweenreduced recollection and spared familiarity was assumed to bebased on their poor performance on a yes/no recognition task andtheir normal performance on a forced-choice recognition task. Theother two studies (Anderson et al., 2008; Wolk, Signoff, & Deko-sky, 2008), which used a PDP to estimate recollection and famil-iarity, reached different conclusions. Indeed, while Anderson et al.(2008) reported poor recollection but normal familiarity in theira-MCI patients, Wolk et al. (2008) observed a comparable impair-ment of recollection and familiarity.

The present study was aimed at further investigating the relativecontribution of familiarity and recollection processes to the epi-sodic recognition performance of a group of patients with a-MCI.In view of the conflicting data reported in previous studies thatused the PDP (Anderson et al., 2008; Wolk et al., 2008), the mainnovelty of the present study is that both the PDP and the R/Kprocedure were used for process estimation. The final goal was toprovide converging evidence, from a plurality of methods, that ADat a preclinical stage is characterized by a dissociation betweenimpaired recollection and normal familiarity, thus supporting theidea of earlier and preferential involvement of the entorhinal

cortex (with the relative sparing of the perirhinal cortex) in theprogression of AD pathology. Alternatively, the simultaneous useof PDP and R/K procedures made it possible to assess the hypoth-esis that the discrepant data in the literature are actually due tomethodological issues related to the particular kind of paradigmused for process estimation (Wolk et al., 2008).

Method

Subjects. Nineteen patients (F/M: 9/10; mean [SD] age: 71.9[9.7] years; mean [SD] education level: 12.9 [4.3] years) who metthe diagnostic criteria for single-domain a-MCI (Petersen & Mor-ris, 2005) and who were attending a specialized dementia clinicwere recruited for the present study. All patients complained ofmemory disorder that was confirmed by an informant assistant, didnot report any history of focal brain pathology, and did not meetthe diagnostic criteria of National Institute of Neurological andCommunicative Diseases and Stroke/Alzheimer’s disease and Re-lated Disorders Association (NINCSD-ADRDA; McKhann et al.,1984) for the diagnosis of probable AD. All patients underwent anextensive clinical, neuropsychological, behavioral, and functionalevaluation to verify that they fulfilled the criteria for the amnesicform of MCI. Major systemic, psychiatric, and other neurologicalillnesses were carefully investigated and excluded in all patients.For each patient, a T2-weighted MRI scan was reviewed by anexpert neuroradiologist, who excluded the presence of any relevantmacroscopic abnormality (e.g., significant signs of concomitantcerebrovascular disease). The mean (SD) Mini Mental State ex-amination (MMSE; Folstein, Folstein, & McHugh, 1975) score ofa-MCI patients (adjusted for age and education according toMeasso et al., 1993) was 25.5 (1.6), ranging from 23.8 to 28.5.None of the recruited patients reported a score above 0.5 on theClinical Dementia Rating (CDR; Hughes, Berg, Danziger, Coben,& Martin, 1982). Patients included in the study had to obtain ascore below the normality cut-off on at least one of the threeepisodic memory tests of the neuropsychological screening battery(see below) and a performance above the normality cut-off scoreson tests exploring all other cognitive domains.

A group of 23 healthy volunteers (F/M: 11/12; mean [SD]age: 66.9 [10.3] years; mean [SD] education level: 12.9 [4.3]years) who did not significantly differ with the patient group forage, sex, and education served as controls for the PDP and R/Kexperimental procedures. None of the healthy subjects (normalcontrols, NCs) showed any cognitive problems or evidence ofcognitive deficits on neuropsychological testing.

Local ethical committee approval was received and writteninformed consent was obtained from each subject before studyinitiation.

Neuropsychological assessment. To identify a group of sub-jects who fulfilled the inclusion criteria (isolated memory deficits),all MCI patients underwent an extensive neuropsychological bat-tery. Verbal episodic long-term memory was evaluated using theImmediate and Delayed recall of a 15-Words List test (Carlesimo,Caltagirone, & Gainotti, 1996) and the Immediate and Delayedrecall of the Short Story test (Carlesimo et al., 2002). Visuospatialepisodic long-term memory was evaluated by the Immediate andDelayed recall of Rey’s Complex Figure (Carlesimo et al., 2002).Short-term memory was evaluated using the Digit span and theCorsi Block Tapping task (Orsini et al., 1987). Executive functions

317SPECIAL SECTION: RECOLLECTION AND FAMILIARITY IN A-MCI

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were explored using the Phonological Word Fluency (Carlesimo etal., 1996), the Categorical Word Fluency (Spinnler & Tognoni,1987), the Trail Making (Giovagnoli et al., 1996), and the Atten-tive Matrices (Spinnler & Tognoni, 1987) tests. Language abilitieswere assessed using the Naming subtest of Aachener’s Aphasiabattery (De Blese et al., 1986). Problem-solving abilities wereinvestigated using Raven’s Colored Progressive Matrices (Car-lesimo et al., 1996). Constructional praxis was assessed using theCopy of simple drawings with and without landmarks test (Car-lesimo et al., 1996) and Rey’s Complex Figure (Carlesimo et al.,2002). For all of these tests, we used Italian normative data forscore adjustment (sex, age, and education) and for normalitycut-off scores, which were determined as the lower limit of the95% tolerance interval for a confidence level of 95% (see Car-lesimo et al., 1996, and Spinnler & Tognoni, 1987).

NCs were screened using the following neuropsychological testbattery: Immediate and Delayed recall of a 15-Words List (Car-lesimo et al., 1996), Immediate and Delayed recall of the ShortStory test (Carlesimo et al., 2002), Immediate and Delayed recallof Rey’s Complex Figure (Carlesimo et al., 2002) and the MMSE(Folstein et al., 1975; Measso et al., 1993).

Experimental procedures for recognition and familiarityquantification.

PDP procedure. Stimuli for this experiment consisted of 160five-letter words, with a frequency of occurrence in the Italianlanguage ranging from 2 to 331 per million (mean value 27.1;Bortolini, Tagliavini, & Zampilli, 1971). The 160 words weredivided into two 80-word sets, which were comparable for fre-quency of occurrence and were used for the entire procedure. Theprocedure included two study phases, respectively, followed bytwo recognition phases, one for the inclusion condition and one forthe exclusion condition. The assignment of lists to conditions wascounterbalanced across subjects. In each study phase, 25 wordswere presented visually and 30 were administered as auditoryitems. Two separate encoding conditions were adopted, respec-tively, for visually presented items: 13 words to be read aloud bythe examined subject and 12 words presented in an anagramformat to be solved. In fact, based on many studies in the literatureon the generation effect (e.g., Gardiner, 1988; Jacoby, 1983), weexpected that recognition accuracy and, particularly, recollectionscores would be higher for words that had been anagrammed thanfor words that had been read. Moreover, since previous studieshave also documented a reduced generation effect in the perfor-mance of memory disordered patients (Verfaellie & Treadwell,1993), we expected that impaired recollection in patients witha-MCI would be particularly severe for words that had beengenerated.

Anagrams were created by underlining the second and fourthletters of a word, keeping them in their correct positions and thenrandomly reversing two of the remaining three letters (e.g., “loplo”as anagram of “pollo”). Using these criteria, the target word is theonly possible solution. Before starting each study phase, subjectswere instructed about the different modalities of item presentation(visual and auditory) and about the encoding processing they hadto perform: repeating (word listened to) or reading aloud (wordwritten in its correct form) the presented words or solving thevisually presented anagrams. They were also instructed to memo-rize each item administered in the study phase, regardless of itspresentation modality, for a subsequent memory test. To become

familiar with the anagram task, subjects performed five practiceexamples before the study began. Whenever subjects solved ananagram incorrectly during the study phase, they were encouragedto try again for a maximum of 1 min. If they failed again, theexaminer provided them with the correct solution. The test phasesincluded two different tasks, inclusion and exclusion, which beganafter the subjects had completed the corresponding study phases.Each test phase (inclusion or exclusion) included the visual pre-sentation of all previously studied words (25 visual and 30 audi-tory items) intermixed with 25 unstudied words (new items).During the inclusion condition, subjects were requested to judgewhether they had seen the presented word in the study phase (olditem) or not (new item). During the exclusion phase, subjects wereasked to indicate as “old” only those words they had previouslylistened to and to respond “new” to all other words (visuallypresented in the study phase and unstudied words). The inclusioncondition always preceded the exclusion condition.

For each subject, the contribution of recollection and familiarityto recognition performance was estimated using the dual-processsignal detection model (Jacoby, Toth, & Yonelinas, 1993; Yoneli-nas et al., 1998). In this model, familiarity reflects a signal detec-tion process like that underlying standard d� tables, which incor-porates response biases into the estimates. In fact, subjects producea false alarm when their feeling of familiarity for a new itemexceeds the subjective response criterion. As a consequence, fa-miliarity is measured as a difference between the average famil-iarity of the old and the new items (Yonelinas et al., 1998). In theI condition, subjects can correctly accept (responding “yes”) thewords previously seen either because they recollect them or be-cause they feel the items are familiar without recollecting thespecific related context. Consequently, the probability of respond-ing “yes” in the I condition is computed as “Recollection �Familiarity [1 � Recollection]”. Conversely, in the E condition,subjects can incorrectly accept a word (responding “yes” to apreviously seen word) only if the items are familiar but notrecollected as having been seen. Consequently, the probability ofresponding “yes” to a previously seen word in the E condition isequal to “Familiarity [1 � Recollection].” In order to estimate theeffect of the recollection process, the probability of accepting an itemin the E condition incorrectly is subtracted from the probability ofaccepting an item in the I condition correctly, Recollection � P(“yes”|oldI) � P(“yes”|oldE). Finally, the familiarity process is esti-mated as the probability of accepting an item in the E conditionincorrectly divided by the recollection, Familiarity � P (“yes”|oldE)/(1 � Recollection).

Remember/Know procedure. A new set of 80, five-letter Ital-ian words (mean [range] frequency 27.3 [1–83] per million; Bor-tolini et al., 1971) was selected for this experimental procedure,which again included a study phase followed by a recognitionphase. The study phase was identical to that used in the PDPprocedure, including the same proportion of visually presenteditems to be read aloud, auditorily presented items to be repeatedaloud, and visually presented anagrams to be solved. In the rec-ognition phase, subjects were administered a list of items, includ-ing all the words previously presented intermixed with 25 newwords, and were required to respond “remember,” “know,” or“new” to each item. They were instructed to respond “remember”if they recollected the specific context (modality of presentation) inwhich the word had been previously presented. They were in-

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structed to respond “know” if they were sure the item had beenpresented during the study phase but could not recollect the spe-cific presentation modality. Finally, subjects were instructed torespond “new” if they did not think the item had been presentedduring the study phase. After the word recognition task wascompleted, subjects’ ability to remember the correct study contextof each word (Source Memory) was also evaluated. They werepresented with the whole word list again and had to decide for eachword whether it had been previously presented as an item to beread or anagrammed, or as an auditory stimulus.

We used the dual-process signal detection model to incorporatethe response bias in the Remember-Know procedure (Yonelinas &Jacoby, 1995). In this procedure, subjects can respond “remember”when an item is recollected, and the probability of the “remember”response is used as an estimate of recollection. Recollection isestimated by subtracting the proportion of false “remember” re-sponses from the proportion of true “remember” responses andthen dividing this number by the probability of obtaining a true“remember” response, Recollection � (Recollectionold � Recol-lectionnew)/(1 � Recollectionnew). Conversely, subjects can re-spond “know” if an item is familiar but not recollected. Familiarityis computed as the probability of accepting an old item correctly,Knowold/(1 � Recollectionold), and accepting a new item incor-rectly, Knownew/(1 � Recollectionnew). Subsequently, the famil-iarity estimate is converted to d� (Yonelinas et al., 1998).

Results

Neuropsychological assessment. According to the inclusioncriteria, all a-MCI patients scored within the normal range on all

tests exploring nonmemory cognitive domains but obtained at leastone abnormal score on the episodic long-term memory tests. Mostof the patients (42%) failed on only 1 of the 6 tests; 21% failedon 2 tests; 16% on 3 tests; another 16% on 4 tests; and theremaining 5% on 5 tests. No subject obtained abnormal scores onall tests administered (see Table 1).

Experimental procedures for recognition and familiarityquantification.

Process dissociation procedure. A-MCI patients and NCswere both fast and accurate at solving anagrams during the studyphase. In the two groups, the proportions of correctly solvedanagrams were .96 � .05 and .97 � .03, respectively. The pro-portion of “old” responses for studied and new items obtained bya-MCI patients and NCs in the inclusion and exclusion conditionsare summarized in Table 2.

In the inclusion condition, the probability of recognizing an itemas “old” (target) reflects hit rates for studied words and false alarmrates for new words. In the exclusion condition, the probability ofidentifying a target item reflects hit rates for words administered asauditory stimuli in the study phase and false alarm rates foranagrams, read words, and new words.

A group comparison showed no significant difference in cor-rectly classifying items administered as auditory stimuli in eitherthe inclusion, F(1, 40) � .53, p � .20, Cohen’s d � .24, or theexclusion condition, F(1, 40) � .59, p � .20, d � .25. In theinclusion condition, an analysis of variance (ANOVA) with Group(a-MCI vs. NCs) as between-subjects factor and Condition (readvs. anagrammed vs. new words) as within-subject factor showed anon significant Group effect, F(1, 40) � 0.15, p � .20; d � .07,

Table 1Mean (SD) Performance Scores Obtained by Amnesic Mild Cognitive Impairment (A-MCI) Patients and Healthy Controls on theEpisodic Memory Tests of the Neuropsychological Screening Battery. For the Other Tests of the Battery (Not Administered to NCParticipants), Mean (SD) of Performance Scores and Ranges of Percentile Scores Obtained by A-MCI Patients Are Reported

Cognitive function Neuropsychological test

Mean (SD) scores

a-MCI (n � 19) Controls (n � 23)

Global measure Mini Mental State Examination 25.5 (1.6) 27.1 (2.5)Long-term memory

Verbal Rey’s 15-word list (Immediate recall) 33.6 (6.4)�� 38.5 (4.9)Rey’s 15-word list (Delayed recall) 5.4 (2.5)�� 7.9 (2.1)Short Story test (Immediate recall) 4.5 (2.7)� 5.9 (1.1)Short Story test (Delayed recall) 3.5 (2.9)�� 5.8 (1.2)

Visuo-spatial Rey’s Complex Figure (Immediate recall) 12.9 (8.5)�� 19.9 (4.2)Rey’s Complex Figure (Delayed recall) 11.3 (8.3)�� 19.1 (4.2)

Percentile range

Short-term memoryVerbal Digit span 4.9 (0.6) 10–90%ileVisuo-spatial Corsi Block task 4.5 (0.8) 10–80%ile

Language Aachen’s Aphasia Test 92.6 (46.0) —Problem solving Raven’s Progressive Matrices 26.1 (5.8) 10–90%ileExecutive functions Attentional Matrices 45.5 (10.0) 10–75%ile

Trail Making TestPart A 71.6 (34.0) 10–80%ilePart B 136.0 (75.0) 10–80%ile

Phonological verbal fluency 26.4 (6.5) 10–95%ileCategorical fluency 13.6 (8.3) 10–85%ile

Praxis abilities Copy of drawings 9.46 (1.6) 10–100%ileCopy of drawings with landmarks 65.8 (4.3) 10–100%ile

� p � .05. �� p � .01.

319SPECIAL SECTION: RECOLLECTION AND FAMILIARITY IN A-MCI

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and a significant Condition effect, F(2, 80) � 115.46, p � .001.The post hoc analysis showed a higher rate of “old” responses foranagrammed words (M � .65) than for words that had only beenread (mean .44), F(1, 40) � 36.02, p � .025, d � .84. “Old”responses on anagrammed and read words were, in turn, morefrequent than on unstudied words (M � .18): new words versusanagrams, F(1, 40) � 285.8, p � .001, d � 2.37, and new versusread words, F(1, 40) � 75.9, p � .001, d � 1.17. The analysis alsoshowed a significant Group by Condition interaction, F(2,80) � 4.72, p � .011. An ANOVA, performed to qualify thisinteraction, revealed a larger increase in the proportion of “old”responses passing from the read to the anagrammed words andfrom the new to the anagrammed words in NCs as compared witha-MCI patients, F(1, 40) � 5.36, p � .03 and F(1, 40) � 9.22, p �.004. Conversely, the between-groups difference between hit rateson read words and false alarms on new words was not significant,F(1, 40) � .02, p � .20.

In the exclusion condition, a similar ANOVA applied to theproportion of incorrect “old” responses for both visually studied

and new words revealed a Group effect that approached statisticalsignificance, F(1, 40) � 3.8, p � .058, d � .48, with the a-MCIpatients reporting an overall higher rate of incorrect “old” re-sponses (M � .31) than NCs (M � .21). The analysis also revealeda significant Condition effect, F(2, 80) � 9.16, p � .001. Thiseffect was explained by a hyper-inclusion rate for anagrams (M �.30) and read (M � .29) words as compared with new words (M �.18): new versus read words, F(1, 40) � 23.8, p � .001, d � .60,and new versus anagrams, F(1, 40) � 9.5, p � .003, d � .52, butthere was no difference between read and anagrammed words, F(1,40) � .17, p � .20, d � .04. Finally, the Group by Conditioninteraction did not approach significance, F(2, 80) � .06, p � .20.

Figure 1 shows the estimates of recollection (panel A) andfamiliarity (panel B) obtained by the dual process signal detectionmodel for a-MCI patients and NCs using the PDP. Estimates werederived separately for read and anagrammed words.

The comparison of the recollection process in a-MCI patientsand NCs was performed using an ANOVA with Group (a-MCI vs.NCs) as between-subjects factor and Condition (Read words vs.Anagrammed words) as within-subject factor. No significantGroup effect, F(1, 40) � .71, p � .20, d � .04, was found due tothe global amount (read � anagrammed words) of recollection,which was not different between the two groups (a-MCI: .22; NCs:.27). Conversely, a significant Condition effect, F(1, 40) � 21.1,p � .001, d � .84, emerged as a consequence of the higherrecollection for anagrammed (.33) than for read words (.15) in allsubjects. A significant Group by Condition interaction, F(1,40) � 4.54, p � .039, was also found. An ANOVA, performed toqualify this interaction, showed that the a-MCI patients had com-parable recollection for read (M � .17 � .15) and anagrammedwords (M � .27 � .23), F(1, 40) � 2.76, p � .10, d � .50, whereasNCs recollected more on anagrams than on read words (M � .40 �.28 and M � .13 � .19, respectively), F(1, 40) � 25.0, p � .001,d � 1.12. Moreover, a direct contrast of the two study conditions(read and anagrammed words) in a-MCI patients and NCs revealedno substantial group difference in recollecting read words, F(1,40) � .49, p � .20, d � .23, but a trend toward statisticalsignificance for worse recollection of anagrammed words in thea-MCI group, F(1, 40) � 2.69, p � .10, d � .51.

A similar ANOVA was performed to estimate the familiarityprocess. This analysis revealed no significant Group effect in theglobal amount of familiarity (a-MCI: .88; NCs: 1.12, respectively),

Table 2Mean (SD) Proportion of “Old” Responses for Words Listenedto, Read, or Produced as the Solution for Anagrams, and forUnstudied Words Obtained During the Inclusion and ExclusionConditions of the Process Dissociation Procedure (PDP) byA-MCI Patients and Healthy Controls. In the InclusionCondition, Target Items Included All Words PreviouslyPresented in the Study Phase. In the Exclusion Condition,Target Items Included Only Those Words Presented Previouslyin the Auditory Modalities. See Text for Further Details

Type of itemInclusioncondition

Exclusioncondition

A) a-MCI patientsAuditorily presented .58 (.24) .48 (.17)Visually presented for reading .47 (.28) .35 (.20)Visually presented as anagrams .60 (.26) .34 (.24)New .22 (.17) .23 (.23)

B) ControlsAuditorily presented .63 (.18) .53 (.22)Visually presented for reading .40 (.25) .26 (.17)Visually presented as anagram .69 (.20) .24 (.16)New .14 (.14) .13 (.17)

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Figure 1. Estimates (Mean and SE) of recollection (panel A) and familiarity (panel B) processes in a-MCIpatients and healthy controls obtained using the PDP.

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F(1, 40) � 1.51, p � .10, d � .32. By contrast, there was asignificant Condition effect due to the anagrammed words thatprovided a greater feeling of familiarity than read words when bothgroups were considered together (M � 1.12 and M � .78, respec-tively) F(1, 40) � 18.14, p � .001, d � .64. The Group byCondition interaction was not significant, F(1, 40) � 1.94, p � .10,as both groups’ anagrammed words (a-MCI: mean 1.02 � .92;NCs: mean 1.41 � .67) produced a greater feeling of familiaritythan read words (a-MCI: mean .73 � .67; NCs: mean .82 � .60),F(1, 40) � 3.75, p � .05, d � .36 and F(1, 40) � 17.6, p � .001,d � .93, respectively. A visual inspection of the familiarity data inFigure 1 ( panel b) indicates that also in this case there was agreater difference between a-MCI and NCs for the anagrammedthan for the read words. To evaluate whether the deficit in recol-lection of anagrammed words in the a-MCI group was indeedgreater than the deficit in familiarity, we compared the z-scores(referenced to the NC group’s means and SDs) for the two com-ponents (-.47 � .84and �.57 � 1.37, respectively). A repeatedmeasures ANOVA revealed no significant difference, F(1, 18) �.09, p � .20, d � .09.

Remember/Know procedure. Also in this case, during thestudy phase, patients and NCs made very few errors in solving theanagrams (proportion of correct responses .95 � .04 and .96 � .03,respectively). Table 3 shows the performances obtained by a-MCIpatients and NCs using the R/K procedure.

For the auditorily presented words, an ANOVA with Group(a-MCI vs. NCs) as between-subjects factor and Condition (Re-member vs. Know) as within-subject factor showed no Groupeffect, F(1, 40) � .26, p � .20, d � .09. A significant Conditioneffect was found, F(1, 40) � 30.0, p � .001, d � 1.41, due to thehigher proportion of words judged as “Remember” (.42) ratherthan “Know” (.16) in both groups. There was also a significantGroup by Condition interaction, F(1, 40) � 4.75, p � .03, due tothe greater production of “Know” responses in a-MCI patientscompared to NCs, F(1, 40) � 4.55, p � .035, d � .65. Conversely,a difference approaching significance emerged for the higher num-ber of remember responses in NCs than in a-MCI patients, F(1,40) � 3.06, p � .08, d � .54.

Considering the visually presented words, two ANOVA modelswere adopted to investigate differences in the proportion of “Re-member” and “Know” responses given. In both cases, Group(a-MCI vs. NCs) was used as between-subjects factor and Condi-tion (read words vs. anagrammed words vs. new words) as within-subject factor. For the “Remember”“ condition, there was noGroup effect, F(1, 40) � 1.11, p � .20, d � .24, but there was asignificant Condition effect, F(2, 80) � 51.4, p � .001. Thisfinding was due to the more frequent “Remember” response foranagrams than for read and new words (anagrams M � .42 � .27,read M � .26 � .23, new M � .12 � .14): anagrams versus read,F(1, 40) � 21.6, p � .001, d � .64, and anagrams versus new, F(1,40) � 94.4, p � .001, d � 1.44. Moreover, “Remember” responseswere also more frequent for read than for new words, F(1,40) � 38.1, p � .001, d � .79. The Group by Condition interactionwas statistically significant, F(2, 80) � 3.79, p � .03. An ANOVAmade to qualify this interaction revealed that the passage from readwords to anagrams produced a comparable increase in “Remem-ber” responses in the two groups, F(1, 40) � 1.44, p � .20.Conversely, a trend toward a significantly larger increase in theNCs than in the MCI group emerged in the passage from the newwords to the read words, F(1, 40) � 3.11, p � .08. Finally, asignificantly larger increase in Remember responses in NCs than ina-MCI patients was noted passing from unstudied to anagrammedwords, F(1, 40) � 6.97, p � .01.

For the “Know” responses, there was a Condition effect, F(2,80) � 8.13, p � .001, due to the similar proportion of anagrammedand read words judged as familiar (M � .20 � .15 and M � .19 �.15, respectively), F(1, 40) � .01, p � .10, d � .07, and a lowerproportion for new words (M � .12 � .11): anagram versus new,F(1, 40) � 10.3, p � .002, d � .61, and read versus new, F(1,40) � 14.3, p � .001, d � .53. No Group effect, F(1, 40) � 1.81,p � .10, d � .28, or Group by Condition interaction, F(1, 40) �.55, p � .20, was observed.

Figure 2 shows the estimates of recollection (panel A) andfamiliarity (panel B) obtained by the dual process signal detectionmodel for a-MCI patients and NCs when undergoing the R/Kprocedure. For consistency with the PDP procedure, estimates ofrecollection and familiarity were computed only for read andanagrammed words.

An ANOVA on recollection estimates with Group (a-MCI vs.NCs) as between-subjects factor and Condition (read vs. ana-grammed words) as within-subject factor revealed a significantGroup effect, F(1, 40) � 4.38, p � .04, d � .50. This was due toa reduced recollection in a-MCI patients as compared with NCs(Ms � .20 � .26, and .33 � .26, respectively). There was also asignificant Condition effect, F(1, 40) � 19.6, p � .001, d � .77,due to the anagrams, which were recollected more than the readwords (M � .36 � .27, M � .18 � .22, respectively). Finally, therewas no Group by Condition interaction, F(1, 40) � .54, p � .20.

The same analysis for the familiarity process revealed no Groupeffect, F(1, 40) � .08, p � .20, d � .08, or Condition effect, F(1,40) � .74, p � .20, d � .17. This was respectively due tocomparable d scores across groups (a-MCI: M � .70 � .72; NCs:mean: .76 � .79) and to the same amount of familiarity foranagrams and read words (anagrams: M � .79 � .78; read words:M � .67 � .65). Finally, there was no interaction between Groupand Condition, F(1, 40) � .13, p � .20.

Table 3Mean (SD) Proportion of Words Identified as “Old” by PatientsWith A-MCI and Healthy Controls in the Remember/KnowProcedure. Responses to Studied Items Are Reported SeparatelyAccording to the Different Modalities of Administration (WordsListened to, Read, or Produced as the Solution for Anagrams).Responses Are Also Divided According to the Subjective Feelingof Familiarity (Remember/Know). See Text for Further Details

Type of item Remember Know

A) a-MCI patientsAuditorily presented .36 (.23) .20 (.17)Visually presented for reading .23 (.20) .23 (.16)Visually presented as anagram .35 (.29) .22 (.18)New .13 (.16) .13 (.09)

B) ControlsAuditorily presented .49 (.21) .11 (.08)Visually presented for reading .30 (.25) .16 (.12)Visually presented as anagram .49 (.24) .17 (.13)New .11 (.12) .11 (.11)

321SPECIAL SECTION: RECOLLECTION AND FAMILIARITY IN A-MCI

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The proportion of words for which a-MCI patients and NCscorrectly identified the study context is summarized in Table 4.Two ANOVA models were employed to test the accuracy ofsource memory for Know and Remember responses given tovisually presented words (read and anagrammed words). Also inthis case, responses to auditorily presented items were not consid-ered. The ANOVA including the words that received a Rememberresponse showed a Group effect, F(1, 40) � 7.76, p � .008, d �.54, due to lower accuracy in remembering the correct studycontext in a-MCI patients compared with NCs (M � .22 � .30,M � .40 � .36, respectively). There was also a Condition effect,F(1, 40) � 20.5, p � .001, d � .96, due to better accuracy foranagrams than for read words (M � .46 � .28, M � .17 � .34,respectively). A Group by Condition interaction, F(1, 40) � 6.06,p � .018, was also observed. An ANOVA made to qualify thisinteraction revealed that a-MCI patients recognized at the samerate the study context for read and anagrammed words, F(1,40) � 1.99, p � .10, d � .44, whereas NCs were more accurate onanagrammed than on read words, F(1, 40) � 26.4, p � .001,d � 1.57. As for words judged as “Know,” an ANOVA did notreveal any significant Group effect, F(1, 40) � .03, p � .10, d �.03. Indeed, the two groups showed comparable accuracy in re-membering the study context for visually presented words (a-MCI:M � .29 � .34; NCs: M � .28 � .35). Conversely, there was aCondition effect, F(1, 40) � 5.12, p � .03, d � .57, due to a better

source memory for anagrammed than for read words (M � .37 �.37 and � .19 � .28, respectively). Finally, the Group by Condi-tion interaction was not significant, F(1, 40) � .18, p � .10, asboth groups showed a similar increase in accuracy passing fromread to anagrammed words.

Comparison between the process dissociation and Remem-ber/Know procedures. In view of the partially discrepant re-sults obtained using the two process estimating procedures, weentered both sets of estimates into the same analysis to comparethem directly and to ascertain whether the two experiments led todifferent patterns of deficits. A first mixed ANOVA with Proce-dure (PDP vs. R/K) and Condition (read vs. anagrammed words)as within-subject factors were used to compare the recollectionestimates obtained by a-MCI patients and NCs. Neither the Pro-cedure effect, F(1, 40) � .60, p � .20, d � .12, nor the Proce-dure � Condition interaction, F(1, 40) � .97, p � .20, approachedstatistical significance. However, a trend toward a significant in-teraction emerged when the recollection estimates obtained on thetwo procedures by a-MCI and NCs were contrasted for read words,F(1, 40) � 2.95, p � .09, but not for anagrammed words, F(1,40) � .11, p � .20. As noted above, the two groups differed in therecollection estimates for the read words derived from the R/K butnot from the PDP. Conversely, both procedures highlighted asignificant difference between groups for the anagrammed words.The discrepancy between the two procedures in detecting or not adeficit of recollection for read words in the a-MCI group wasactually due to a different estimate of this component in the NCgroup. Indeed, while a similar estimate emerged from the PDP andR/K procedures for the group of a-MCI individuals (.17 � .15 and.13 � .19, respectively), F(1, 40) � .11, p � .20, d � .23, a trendtoward a significant difference emerged for the NC group (.13 �.19 and .23 � .24, respectively), F(1, 40) � 3.07, p � .08, d � .42.

A second mixed ANOVA model compared the familiarityscores obtained by a-MCI patients and NCs on the two procedures.In the overall comparison, a significant interaction emerged be-tween Procedure and Condition, F(1, 40) � 4.49, p � .04. Indeed,the familiarity estimates for the read words obtained from the PDP(.78 � .62) and R/K (.67 � .65) procedures did not differ, F(1,40) � .56, p � .20, d � .17. Conversely, the familiarity estimatefor the anagrammed words was significantly higher in the PDP(1.22 � .81) than in the R/K (.79 � .78) procedure, F(1,40) � 5.77, p � .02, d � .54. However, neither the Group effect,F(1, 40) � 1.45, p � .20, d � .20, nor the interactions involvingthe Group factor, Group � Procedure, F(1, 40) � .42, p � .20, and

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Figure 2. Estimates (Mean and SE) of recollection (panel A) and familiarity (panel B) processes in a-MCIpatients and healthy controls obtained using the R/K procedure.

Table 4Mean (SD) Proportion of Words for Which the Study Context(Source Memory) Has Been Correctly Identified as Read orAnagrammed by A-MCI Patients and Healthy Controls on theRemember/Know procedure. Responses to Studied Items AreReported Separately According to the Different Modalities ofAdministration (Words Read or Produced as The Solution forAnagrams). Responses Are Also Divided According to theSubjective Feeling of Familiarity (Remember/Know). See Textfor Further Details

Type of item Remember Know

A) a-MCI patientsVisually presented for reading .15 (.26) .21 (.30)Visually presented as anagram .28 (.33) .36 (.37)

B) ControlsVisually presented for reading .18 (.29) .17 (.27)Visually presented as anagram .62 (.26) .39 (.38)

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Group x Condition, F(1, 40) � 1.13, p � .20, approached statis-tical significance. This indicates that a discrepancy exists betweenthe two procedures in estimating familiarity for anagrammedwords (in the sense of an overestimation by the PDP or anunderestimation by the R/K procedure). However, this discrepancydid not substantially alter the results obtained from the comparisonbetween the a-MCI and NC group (lack of a difference).

Discussion

Episodic memory deficits are the cognitive hallmark of patientswith a-MCI. Nevertheless, it is still unclear whether, and to whatextent, this memory impairment is due to deficits in the recollec-tion or the familiarity components of memory. To address thisissue, we screened a group of patients who strictly fulfilled thediagnostic criteria for a-MCI (Petersen et al., 2001). All of thempresented with a subjective complaint of memory loss, which wasconfirmed by an informant assistant. In all patients, a detailedneuropsychological assessment documented the presence of epi-sodic memory deficits and the absence of impairments in othercognitive domains. We estimated the relative contribution of rec-ollection and familiarity to the recognition performance of thesepatients by means of two independent procedures: PDP and R/K.Consistently with our hypothesis, the results obtained using theR/K procedure documented a selective impairment of recollectionin the group of a-MCI individuals, with a substantial preservationof familiarity. Indeed, compared with NCs, a-MCI individualsreported a significantly lower recollection estimate for both readand anagrammed words, with no significant difference in famil-iarity rates. Results obtained on the source memory task (i.e.,reduced accuracy in associating each word with its study condi-tion) further confirmed the memory deficit for contextual informa-tion in our group of a-MCI patients.

Results obtained using the PDP were far less supportive of aselective impairment of recollection in the individuals with a-MCI.In fact, no significant overall difference between groups emergedeither for the recollection or the familiarity process. Conversely, a(non significant) trend for the NCs to perform better than thea-MCI individuals on the anagrammed words was evident in bothrecollection and familiarity scores.

In view of the partially discrepant results obtained using thePDP and R/K procedures, in another analysis, we directly con-trasted the recollection and familiarity estimates obtained by thea-MCI and NC groups with the two procedures. For recollection,this analysis demonstrated that in the overall experimental groupthe two procedures provided comparable estimates for both readand anagrammed words. Nevertheless, while the two procedureswere consistent in highlighting a deficit for the anagrammed wordsin a-MCI individuals, R/K but not PDP highlighted a deficit in thea-MCI group for the read words. By contrast, for familiarity, wefound that in the overall experimental sample estimates for theanagrammed words derived from the R/K procedure were lowerthan those derived from the PDP. In any case, the two procedureswere consistent in describing a lack of difference between a-MCIand NC groups for both the read and the anagrammed words.

Our finding of a reduced contribution of recollection to therecognition memory performance of a-MCI individuals is substan-tially consistent with the previous literature. Indeed, two studiesusing PDP (Anderson et al., 2008; Wolk et al., 2008) and another

contrasting yes/no and forced choice recognition (Westerberg etal., 2006) consistently reported poor recollection in a-MCI patientsas compared with NCs. No previous studies have used the R/Kprocedure to investigate a-MCI patients. However, the only twostudies that adopted the R/K procedure to assess mildly dementedAD individuals reported a decrease of recollection (Dalla Barba,1997; Rauchs et al., 2007). The results of the present study extendthe finding of poor recollection estimated by the R/K procedure toindividuals with a-MCI. An unexpected finding of the presentstudy was the lower sensitivity of the PDP as compared to the R/Kprocedure in revealing a recollection deficit in a-MCI patients.Among other possible reasons for these partially discrepant data, itis our opinion that the PDP may have underestimated this com-ponent of the recognition memory in NCs. Indeed, as previouslynoted, NC individuals obtained substantially higher recollectionestimates for read words in the R/K procedure than in the PDP( p � .08). Such an effect may reflect a difficulty of healthyindividuals to recollect the words in the PDP, likely due to theintrinsic characteristics of this specific experimental paradigm. Infact, the instruction in the exclusion condition to label as “New”not only the unstudied words but also the words previously studiedin the visual modality might represent a confounding factor in theperformance of elderly individuals, thus resulting in an underesti-mation of their actual recollection abilities. In the group of a-MCIindividuals, estimates of recollection for the read words derivingfrom the two procedures did not differ. It should be noted, how-ever, that in these patients the estimate obtained with the R/Kprocedure was so low (.12) that it might have obscured an addi-tional reduction due to task difficulties intrinsic to the PDP. Furtherstudies are needed to identify experimental procedures that areable to provide the most reliable estimates of recollection whenapplied to normal elderly individuals and patients with cognitiveimpairment.

Our finding of a normal contribution of familiarity to the rec-ognition memory performance of a-MCI individuals is also inkeeping with most previous experimental work. Indeed, Andersonet al. (2008), who used the PDP to investigate a-MCI patients, andDalla Barba (1997) and Rauchs et al. (2007), who used the R/Kprocedure to investigate mildly demented AD patients, reportedsimilar familiarity estimates between patients and NCs. The pres-ence of a normal contribution of familiarity to the recognitionperformance in MCI individuals was also argued by Westerberg etal. (2006) on the basis of the normal accuracy of patients in aforced-choice recognition paradigm. One exception is the study byWolk et al. (2008), which reported a reduced familiarity compo-nent in a group of a-MCI individuals when a PDP paradigm wasused. In an attempt to interpret the discrepancy between their dataand previous data, Wolk et al. (2008) noted a potential pitfall in theestimate of familiarity from the subjective report of Remember andKnow responses in individuals with memory disorders. Indeed,because the nature of the task only allows for a know response inthe absence of recollection, it is likely that the simple examinationof the absolute level of know responses actually overestimates thecontribution of familiarity to the performance of individuals withmemory disorders. However, this was not the case in the presentstudy. Indeed, in keeping with the assumption that these processesare independent, we followed Yonelinas et al.’s suggestion (1998)to calculate familiarity as a proportion of items, given a knowresponse, over the number of items in which such a response can

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be given (1 minus proportion of remember responses). This en-sured us that the estimate of familiarity would not be artificiallyinflated by the low number of remember responses. Another reasonfor the discrepant results between our study and that from Wolk etal. may be the heterogeneous criteria employed for patient recruit-ment. In fact, in Wolk et al.’s (2008) study, which included 16a-MCI individuals and 21 NCs, the enrolment of patients exhibit-ing some additional frontal dysfunction (as demonstrated by sig-nificantly poorer average group performance on working memoryand verbal fluency tests in MCI patients than in NCs) mightexplain their comparable impairment of recollection and familiar-ity. In support of this hypothesis, it has been recently demonstratedthat patients with frontal lesions are selectively impaired in thefamiliarity component of recognition memory (MacPherson et al.,2008).

Our finding of a dissociation between poor recollection andnormal familiarity processes in individuals with a-MCI is consis-tent with the neuropsychological model that attributes distinctroles to different MTL regions with respect to recollection andfamiliarity (Aggleton & Brown, 1999). These processes have beenextensively investigated in patients with focal lesions of the mesialtemporal lobe (Cipolotti et al., 2006; Turriziani et al., 2008;Yonelinas et al., 2002), and evidence has been provided that thehippocampus is the key structure for recollection (Turriziani et al.,2008; Yonelinas et al., 2002) whereas the perirhinal cortex iscritical for familiarity (Bowles et al., 2007). More specifically, aparticular role in this complex circuit of information flow is likelyplayed by the entorhinal region. This structure includes a complexneuronal network that is strictly connected with other regions ofthe mesial temporal lobe, such as the perirhinal and parahippocam-pal cortices. The entorhinal cortex is known to be the major sourceof input for the hippocampus (Duvernoy, 1998). These two struc-tures constitute a common “functional unit,” which is essential foracquisition of new information about events (Squire & Zola-Morgan, 1991; Young, Otto, Fox, & Eichenbaum, 1997). Based onthe evidence that the earliest degenerative processes occurring inAD are located in the transentorhinal-entorhinal cortex (Braak &Braak, 1995), we can argue that the recollection deficits observedin our cohort of a-MCI patients were probably due to a discon-nection between the entorhinal cortex and the hippocampus (Stoubet al., 2006).

As noted above, the dual-process hypothesis of a relationshipbetween recollection and familiarity is not universally accepted.An alternative view is that recollection and familiarity representthe output of memory traces of different strengths and, conse-quently, that different portions of the MTL (particularly the hip-pocampus and the perirhinal cortex) play complementary roles inboth components of recognition memory (Manns, Hopkins, Reed,Kitchener, & Squire, 2003; Squire et al., 2007; Wais, Wixted,Hopkins, & Squire, 2006). In this view, the finding in our group ofa-MCI individuals of a poor recollection but a normal familiaritycontribution to recognition memory could be interpreted as theresult of a partial damage to MTL structures, causing the morecomplex recollection process to be disrupted but sparing the morerudimentary familiarity process. The results of the present studyare inconclusive in supporting one of these two alternative theo-ries. Nevertheless, they are consistent with growing evidence inthe neuropsychological literature that a dissociation between nor-mal recollection and reduced familiarity can also be observed in

neurological populations (Bowles et al., 2007; Davidson, Anaki,Saint-Cyr, Chow, & Moscovitch, 2006; MacPherson et al., 2008).Moreover, the existence of independent neural circuits that selec-tively underlie recollection and familiarity is not supported exclu-sively by neuropsychological data. Indeed, there are other sourcesof evidence, such as an event-related potentials investigation(Rugg & Yonelinas, 2003) that identified in vivo two functionallyand temporally dissociable neuronal populations that support theexistence of recollection and familiarity as independent processeson a functional and anatomical basis. Finally, a growing number offMRI studies have reported dissociable patterns of activity formeasures of familiarity and recollection (Daselaar et al., 2006;Montaldi, Spencer, Roberts, & Mayes, 2006; for a recent review,see Skinner & Fernandes, 2007).

In conclusion, the present study reports that a selective impair-ment of recollection is one of the earliest features of AD pathol-ogy. In light of previous neuropsychological evidence frompatients with focal brain damage and functional neuroimagingevidence from healthy individuals, our results support the idea thatrecollection and familiarity are independent processes associatedwith distinct anatomical substrates. In a-MCI patients, the selectivedeficit of recollection strongly suggests the presence of an earlybrain tissue damage localized to the entorhinal cortex. Furtherstudies involving patients at different stages of AD and combiningneuropsychological assessments of recollection and familiaritywith high anatomical resolution measures of brain tissue damageare needed to confirm this hypothesis.

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Bastin, C., Linden, M., Charnallet, A., Denby, C., Montaldi, D., Roberts,N., & Andrew, M. (2004). Dissociation between recall and recognitionmemory performance in an amnesic patient with hippocampal damagefollowing carbon monoxide poisoning. Neurocase, 10, 330–344.

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Received January 23, 2009Revision received September 1, 2009

Accepted September 4, 2009 �

Call for Papers: Journal of Experimental Psychology: Learning, Memory,and Cognition

Special Section on Neural Mechanisms of Analogical Reasoning

The Journal of Experimental Psychology: Learning, Memory, and Cognition invites submissionsof manuscripts for a special section on the Neural Mechanisms of Analogical Reasoning to becompiled by Associate Editor Miriam Bassok and Guest Editors Kevin Dunbar and Keith Holyoak.The goal of the special section is to showcase high-quality research that brings together behavioral,neuropsychological, computational, and neuroimaging approaches to understanding the cognitiveand neural mechanisms that are involved in analogical reasoning. The editors are seeking articles onanalogy and related cognitive processes (e.g., schema induction, metaphor, role-based relationalreasoning, category-based induction) that either present original research using methods of cogni-tive neuroscience or that present behavioral research (including studies of cognitive developmentand/or aging and studies of brain-damaged patients) strongly connected to the neural mechanismsof analogical reasoning.

The submission deadline is October 1, 2010. The main text of each manuscript, exclusive offigures, tables, references, or appendixes, should not exceed 35 double-spaced pages (approxi-mately 7,500 words). Initial inquiries regarding the special section may be sent to Miriam Bassok(mbassoku.washington.edu). Papers should be submitted through the journal’s submission portal(see www.apa.org/pubs/journals/xlm/) with a cover letter indicating that the paper is to be consid-ered for the special section.

326 SERRA ET AL.

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