Neuropsychology Copyright 2007 by the American Psychological Association

2007, Vol. 21, No. 5, 549 –558 0894-4105/07/$12.00 DOI: 10.1037/0894-4105.21.5.549

Amnestic Mild Cognitive Impairment: Difference of Memory Profile in

Subjects Who Converted or Did Not Convert to Alzheimer’s Disease
Roberta Perri and Laura Serra Giovanni Augusto Carlesimo and Carlo Caltagirone
Foundation IRCCS Santa Lucia Foundation IRCCS Santa Lucia and
University of Rome “Tor Vergata”

The Early Diagnosis Group of the Italian Interdisciplinary Network on Alzheimer’s Disease

Episodic long-term, short-term, and implicit memory were investigated in 79 elderly subjects who fulfilled criteria
for the amnestic form of mild cognitive impairment (a-MCI; i.e., by having an idiopathic amnestic disorder with
absence of impairment in cognitive areas other than memory and without confounding medical or psychiatric
conditions) and who developed Alzheimer’s disease (AD) after 2 years as well as in 111 subjects affected by a-MCI
who did not develop dementia. Results document a memory profile in a-MCI subjects characterized by preserved
short-term and implicit memory and extensive impairment of episodic long-term memory. In virtually all episodic
memory indexes examined (learning, forgetting, recognition abilities), a-MCI subjects who converted to AD were
more severely impaired than were subjects who did not become demented. This memory profile, which closely
resembles that exhibited by amnestic patients with bilateral mesial–temporal lobe lesions, confirms a precocious
phase in preclinical AD characterized by selective involvement of mesial–temporal areas and worsening of the
memory impairment as atrophic changes progress in hippocampal structures. In this context of pervasive episodic
memory impairment, tests assessing the free recall of verbal material following a delay interval demonstrated the
greater sensitivity to memory deficits of a-MCI subjects who developed AD.

Keywords: episodic memory, implicit memory, mild cognitive impairment, Alzheimer’s disease

Much experimental work investigating the qualitative profile of
memory dysfunction in Alzheimer’s disease (AD) documents the
pervasive impairment of declarative long-term memory, that is, the
Roberta Perri and Laura Serra, Foundation Istituto di Ricovero e Cura a
Carattere Scientifico (IRCCS) Santa Lucia, Rome, Italy; Giovanni Augusto
Carlesimo and Carlo Caltagirone, Foundation IRCCS Santa Lucia and Uni-
versity of Rome “Tor Vergata,” Rome, Italy; the Early Diagnosis Group of the
Italian Interdisciplinary Network on Alzheimer’s Disease. Group members and
centers participating in the study are as follows: Fondazione Don Gnocchi,
Milano: M. Alberoni; Ospedale S. Gerardo, Monza: I. Appollonio; Instituto
Nazionale Riposo e Cura Anziani (INRCA) – C. da Mossa, Ascoli Piceno: S.
Bonaiuto; Ospedale Niguarda, Milano: G. Bottini; Università di Parma, Parma:
P. Caffarra; Università Tor Vergata and Fondazione Santa Lucia, Roma: C.
Caltagirone; II Università di Napoli, Napoli, S. Carlomagno; Ospedale S.
Salvatore, L’Aquila: A. Carolei and P. Sucapane; Ospedale Sant’Anna, Fer-
rara: P. De Bastiani; Università di Milano, Milano: M. Di Luca; Clinica Santa
Maria HSR, Castellanza: M. Franceschi; Ospedale Ca’ Foncello, Treviso: M.
Gallucci; Azienda Ospedaliera di Verona, Verona: G. Gambina; Arcispedale
Santa Maria Nuova, Reggio Emilia: E. Ghidoni; Ospedale C. Besta, Milano: F.
Girotti; Università La Sapienza, Roma, F. Giubilei; Ospedale degli Infermi di
Rimini, Rimini: S. Lorusso; IRCCS Fondazione Maugeri, Veruno: C. Mar-
chetti; Università di Palermo, Palermo: R. Monastero; Università La Sapienza,
Roma, C. Mina; Università di Brescia, Brescia: A. Padovani; Azienda Osped-
aliera Sant’ Antonio Abate, Gallarate: M. Perini; Centro Regionale Alzheimer
– Passirana di Rho, Milano: C. Pettenati; Università di Sassari, Sassari: M.R.
Piras; Università degli Studi, Ancona: L. Provinciali; Policlinico Universitario,
Messina, A. Quartarone and A. Graceffa; Università di Perugia, Perugia: U.
Senin; Ospedale Santa Chiara, Pisa: G. Tognoni; Azienda Sanitaria Locale
(ASL) 15, Cuneo: P. Zagnoni; Bracco - Spa, Milano: E. Grossi and R. Savarè.
Correspondence concerning this article should be addressed to Roberta
Perri, Fondazione IRCCS Santa Lucia, Via Ardeatina, 306, 00179, ROMA,
Italy. E-mail: r.perri@hsantalucia.it
explicit form of memory that permits the conscious recall or
recognition of previously experienced facts or events. Poor encod-
ing of incoming information during the learning phase, accelerated
forgetting rates, and increased sensitivity to interference during
retrieval have all been documented in AD (see Spaan, Raaijmak-
ers, & Jonker, 2003, for a review). These deficits are consistent
with the neuropathology of the disease, which extensively and
precociously affects the mesial–temporal lobe (MTL) structures
(Braak, Braak, & Bohl, 1993) known to be critically involved in
declarative long-term memory functioning (Squire, 1992). In ad-
dition to declarative memory, there is evidence that repetition
priming, an implicit form of memory, and short-term memory are
also impaired in AD patients (Fleischman et al., 1999; Carlesimo,
Fadda, Sabbadini, & Caltagirone, 1996). Because short-term mem-
ory and repetition priming are supported by different neocortical
regions than is explicit long-term memory, their impairment is
generally considered a sign that the neuropathology from the MTL
structures has progressed to the associative neocortical areas in the
temporal, parietal, and frontal lobes (Desgranges et al., 1998;
Fleischman & Gabrieli, 1999; Perry & Hodges, 1996).
Subjects suffering from the amnestic type of mild cognitive
impairment (a-MCI) have a high risk of developing AD (Petersen
et al., 2001). A recent study carried out by the Italian Interdisci-
plinary Network on Alzheimer’s Disease (Perri, Carlesimo, Serra,
Caltagirone, & the Early Diagnosis Group, 2005) documented
impairment of several indexes of explicit long-term memory func-
tioning in a relatively large group of a-MCI subjects. Indeed,
compared with a group of healthy control subjects, these patients
showed poor learning and increased forgetting rates of verbal and
visual material and reduced effectiveness of semantic encoding to
improve subsequent verbal recall. In contrast, a-MCI subjects’

549
550 PERRI ET AL.
performance was substantially normal on short-term and implicit
memory tasks, thus supporting the view that the preclinical phase
of AD is characterized by precocious involvement of the hip-
pocampal structures and substantial sparing of extra-MTL asso-
ciative neocortical areas. However, these results were obtained on
the whole a-MCI sample, irrespective of whether individual sub-
jects eventually developed dementia. Thus, although an impair-
ment of short-term and/or implicit memory function characterized
the subjects in the incipient phase of dementia, perhaps this deficit
could not be detected when the entire a-MCI population was
investigated.
The present study was aimed at investigating both quantitative
and qualitative differences in the memory deficit that characterizes
a-MCI subjects who have an absence of impairment in cognitive
areas other than memory, who do not have confounding medical or
psychiatric conditions, and who will develop AD dementia
within 2 years in comparison with those of subjects who will not
develop dementia. For this purpose, we compared performances on
declarative long-term, short-term, and implicit memory tasks ob-
tained at the beginning of the study by examining 111 a-MCI
subjects who did not develop dementia during a 2-year follow-up
period with those obtained by examining 79 a-MCI subjects who
did develop AD during that period.
Method
Subjects
a-MCI Subjects
The experimental sample of the present study was composed of
190 a-MCI subjects (82 male and 108 female; mean age ⫽ 70.1
years, SD ⫽ 7.2; mean years of education ⫽ 7.6, SD ⫽ 3.5) who
were followed for 2 years. The subjects were taken from a sample
of 269 subjects (115 male and 154 female; mean age ⫽ 70.3 years,
SD ⫽ 6.9; mean years of education ⫽ 7.9, SD ⫽ 3.8) recruited
in 29 neurological and geriatric centers that are part of the Italian
Interdisciplinary Network on Alzheimer’s Disease (see list in the
author note). Enrollment was initiated with 50 – 80-year-old out-
patients who had at least 5 years of formal education and had been
referred to a neurologist or a geriatrist for the first time for a
memory disturbance. All subjects whose memory disorders were
confirmed by an informant assistant, who had no history of focal
brain pathology, and who did not meet the diagnostic criteria for
dementia were submitted to a broad neuropsychological, clinical,
behavioral, and functional screening evaluation to determine
whether they fulfilled the criteria for a-MCI.
The neuropsychological screening evaluation included the fol-
lowing: episodic long-term memory (immediate and 15-min de-
layed recall of a 15-word list, Carlesimo, Caltagirone, & Gainotti,
1996; short story recall, Novelli et al., 1986), short-term memory
(Digit Span and Corsi Block Tapping task, Orsini et al., 1987),
executive functions (phonological and categorical word fluency,
Carlesimo, Caltagirone, & Gainotti, 1996; Spinnler & Tognoni,
1987), language (Token Test and Naming subtest of Aachener
Aphasia test, Spinnler & Tognoni, 1987; De Blese et al., 1986),
problem-solving (Raven’s Coloured Progressive Matrices, Car-
lesimo, Caltagirone, & Gainotti, 1996), attention (attentive matri-
ces, Spinnler & Tognoni, 1987), constructional praxis (copy of
drawings and copy of drawings with landmarks, Carlesimo, Calta-
girone, & Gainotti, 1996) and general cognitive efficiency (Mini-
Mental State Examination [MMSE], Measso et al., 1993). For each
test in the battery, Italian normative data were available for score
adjustment on the basis of sex, age, and education as well as for
normality cutoff scores, which were determined as the lower limit
of the 95% tolerance interval for a confidence level of 95% (see
Spinnler & Tognoni, 1987, and Carlesimo, Caltagirone, & Gain-
otti, 1996).
The clinical assessment included clinical and cognitive history,
standard neurological examination, standard blood and chemistry
examinations, thyroid hormone levels, syphilis serologic testing,
vitamin B12 and folic acids levels, chest x-ray, electrocardiogram,
and neuroradiological examination (CT or MR). The behavioral
battery consisted of Beck’s Depression Inventory (Beck & Steer,
1987) and Hamilton’s Anxiety (Hamilton, 1960) scales. The sub-
jects’ autonomy in social and daily living activities was investi-
gated by means of the Clinical Dementia Rating (CDR; Hughes,
Berg, Danziger, Coben, & Martin, 1982) and Instrumental Activ-
ities of Daily Living (Lawton & Brody, 1969) scales.
Inclusion criteria for subjects in the a-MCI group were the follow-
ing: (a) subjective memory impairment corroborated by an assistant
and confirmed by a score below the normality cutoff on at least one
of the three episodic memory tests of the neuropsychological screen-
ing battery; (b) nonfulfillment of the Diagnostic and Statistical Man-
ual of Mental Disorders (DSM–IV) criteria for dementia (American
Psychiatric Association, 1994); (c) preserved general cognitive func-
tions and absence of impairment in cognitive areas other than mem-
ory, as confirmed by normal scores on the MMSE (normality cutoff
score: 24; Measso et al., 1993) and on all tests of the neuropsycho-
logical screening battery that assessed cognitive functions other than
episodic memory; (d) no or very mild impact of the memory deficit on
the subject’s activities, as confirmed by a normal score on instrumen-
tal activities of daily living and by a total CDR score of 0.5, consistent
with a minimal change in the patient’s habits; (e) lack of any evidence
of neurological or systemic pathology able to induce memory disor-
ders, as confirmed by normal thyroid functioning, vitamin B12 and
folic acid levels, syphilis serologic results, neurological examination
and CT or MR brain imaging negative for focal lesions (minimal
diffuse changes or minimal lacunar lesions of white matter were
admitted); (f) absence of moderate to severe depression and/or anxi-
ety, as confirmed by scores on Beck’s Depression Inventory and
Hamilton’s Anxiety that were consistent, at most, with mild depres-
sion or anxiety (14 was the highest acceptable for both scales).
All a-MCI subjects enrolled in the original study were admin-
istered the experimental neuropsychological memory battery
within 30 days from completion of the screening phase. Then they
were invited to follow-up evaluations after 12 (12 f-up) and 24 (24
f-up) months during which they were again submitted to the
clinical examination and the neuropsychological, behavioral, and
functional assessments administered in the screening phase. This
permitted classifying them as still having MCI or as developing
dementia. Criteria for MCI classification at follow-ups included (a)
nonfulfillment of the DSM–IV criteria for dementia (American
Psychiatric Association, 1994); (b) preserved general cognitive
functions as confirmed by normal scores on the MMSE; and (c) no
or very mild impact of the cognitive impairment on the subject’s
activities, as confirmed by a total CDR score ⱕ0.5. Patients were
diagnosed as having dementia when they fulfilled the DSM–IV
criteria for dementia. Subjects who did not fulfill the clinical
 MEMORY PROFILE IN AMNESTIC MCI SUBJECTS
criteria for dementia but who obtained an MMSE score less
than 24 or a total CDR score greater than 0.5 were classified as
having an uncertain diagnosis. Subjects who did not undergo the
entire neuropsychological, behavioral, and functional assessment
at one of the two follow-ups were considered dropouts.
In this study, we present data collected from the 111 a-MCI
subjects who still received the diagnosis of MCI after the 2-year
observation period (nonconverters) and the 79 a-MCI subjects who
converted to AD in the same period (converters). Diagnosis of
probable AD was established by using the National Institute of
Neurological and Communicative Diseases and Stroke/Alzhei-
mer’s Disease and Related Disorders Association criteria (Mc-
Khann et al., 1984). Of the 79 patients who were not included in
the present study, 2 died, 4 developed a form of dementia different
from AD, 7 received an uncertain diagnosis, and 66 were dropouts.
The 66 subjects who dropped out did not differ from the sample of
subjects who completed the follow-ups as to demographic charac-
teristics and performance levels on the tests of the screening
neuropsychological battery (data not shown, F ⬍ 2.54 in all
comparisons, p consistently ns), thus suggesting they were ran-
domly missing with respect to baseline memory impairment.
Control Subjects
Eighty-seven healthy subjects (36 male and 51 female; mean
age ⫽ 68.04 years, SD ⫽ 10.8; mean years of education ⫽ 8.13
years, SD ⫽ 4.2), recruited through the Foundation IRCCS Santa
Lucia of Rome, volunteered to participate in the study as normal
control subjects (NCs). Inclusion criteria were (a) absence of
active or previous neurological or psychiatric disorders, (b) no
history of alcohol or drug abuse, (c) absence of subjective memory
disturbance, and (d) normal general cognitive functions as con-
firmed by an MMSE score greater than 24.
As shown in Table 1, the 111 a-MCI subjects who still received
the diagnosis of MCI at the 24 f-up (nonconverters), the 79 a-MCI
who were diagnosed as having converted to AD at this time
(converters), and the 87 NCs were comparable for education and
gender distribution. However, converters were older than were
both nonconverters and NCs who, in turn, did not differ from each
other. Mean scores obtained by nonconverters, converters, and
NCs on the MMSE significantly differed, with converters perform-
Table 1
Demographic Data and Average MMSE Scores (With Standard Deviations) of Nonconverter,
Converter, and NC Groups
Nonconverter Converter
Measure (n ⫽ 111) (n ⫽ 79)
Sex
Men 47 35
Women 64 44
Age (years) 67.8 (7.5) 73.2 (5.5)a,b
Education (years) 7.7 (3.6) 7.5 (3.2)
MMSE 27.7 (1.7)c 26.3 (1.9)a,b
Note. NC ⫽ normal control; MMSE ⫽ Mini-Mental State Examination.
a
Converters vs. nonconverters significant difference ( p ⬍ .000).
b
Converters vs. NCs significant difference ( p ⬍ .000).
c
Nonconverters vs. NCs significant difference ( p ⬍ .01).
551
ing significantly worse than did nonconverters who, in turn, per-
formed significantly worse than did NCs.
Experimental Memory Battery
The experimental memory battery, which was described in a
previous study (Perri et al., 2005), explored episodic long-term and
implicit memory. The contribution of short-term memory to the
immediate free recall of a word list was also investigated.
Episodic Memory
Word-list recall (Carlesimo et al., 1998). Two lists of 16
words (semantically related and unrelated) were used. The first list
was composed of 16 unrelated nouns of concrete objects, the
second of 16 words, 4 for each of four semantic categories (ani-
mals, fruit, tools, clothing). For each list, the test consisted of five
consecutive immediate free-recall trials, followed by a 15-min
delayed recall trial (score range ⫽ 0 –75 and 0 –15 for immediate
and delayed recall, respectively).
Word-list recognition (Carlesimo et al., 1998). Two lists were
used, one for the unrelated condition and one for the related
condition. Each list included the 16 words from the studied list
and 16 new words. The recognition lists were presented 15 min
after delayed recall of the respective list. Two separate scores for
correct recognition of the studied items (hit rates) and for incorrect
recognition of the unstudied items (false alarms) were computed
(range ⫽ 0 –16 in both cases).
Prose recall (Carlesimo et al., 2002). The subject was asked
to recall a short story immediately after its oral presentation by the
examiner and following a 20-min interval without repetition. Sep-
arate scores were given for immediate and delayed recall accord-
ing to the number of informative units reported (range ⫽ 0 – 8).
Rey’s Figure Form B reproduction. The test (Carlesimo et al.,
2002) consisted of freehand copying, followed by an immediate
and a delayed (15-min later) reproduction of the Rey’s Complex
Figure from memory without re-presentation. Separate scores were
given for copying and for immediate and delayed tests according
to accuracy of the figure reproduction (range ⫽ 0 –36).
Implicit memory. Verbal repetition priming was evaluated
with a stem completion test (Graf, Squire, & Mandler, 1984). The
NC
(n ⫽ 87) ␹2 F p df
.149 ns 2
36
51
68.0 (10.9) 12.0 ⬍.000 2, 274
8.1 (4.3) 0.7 ns 2, 274
28.4 (1.8) 26.8 ⬍.000 2, 274
552 PERRI ET AL.
subjects read 20 words one at a time and then rated each word on
a 5-point pleasantness scale. Five min after, 40 three-letter word
stems (20 belonging to words of the studied list, 20 to words of an
unstudied list) were presented visually one at a time. The subjects
were asked to complete each stem with the first word that came to
mind. The level of priming was established as the difference
between stems completed with words from the studied list and
stems completed with words from the unstudied list.
Visual–perceptual repetition priming was investigated by a
fragmented picture identification test (Heindel, Salmon, & Butters,
1990). The test material consists of 14 line drawings with seven
different levels of fragmentation. In the first session, the subjects
were presented with the most fragmented version of a first set of 7
drawings and were requested to try to identify them. Progressively
less degraded versions of drawings that had not been identified
were presented in the subsequent trials until the subject was able to
identify all of the drawings. In the second session, the following
day, the same testing procedure was used for the same and for a
new set of 7 drawings presented in random order. Depending on
the degradation level at which the subjects were able to identify the
drawing, they received a score from 7 (maximum fragmentation)
to 1 (nonfragmented version) for each drawing. The improvement
in performance passing from identification of the new set of
drawings to identification of the old set of drawings in the second
session was a measure of perceptual memory for specific items
(repetition priming). Informed consent was obtained from all sub-
jects prior to the study.
Data Analysis
The average scores obtained by converters, nonconverters, and
NCs on the tests of the experimental memory battery were ana-
lyzed by performing multiple-way analyses of covariance
(ANCOVAs) with group as a three-level between-subjects factor
and test conditions as within-subjects factors. Because of a differ-
ence in the mean age of the groups, age was inserted as a covariate
factor. When results of the principal analyses were significant, post
hoc comparisons were performed by the least significant difference
test to reveal the crucial differences between groups.
Results
A summary of the most important findings that emerged from a
comparison of the performances of nonconverter, converter, and
NC groups on the tests of the experimental memory battery is
reported in Table 2. Cohen’s d effect size measure for the main
comparisons between groups is also reported in this table and, in
particular, for the converters versus nonconverters comparisons. A
graphic of the main effect sizes is shown in Figure 1.
Explicit Long-Term Memory
Word-List Recall
Learning rate. The results of a three-way Group ⫻ Type of
List ⫻ Trial ANCOVA revealed a significant difference between
groups, F(2, 185) ⫽ 62.91, p ⬍ .001: The converter group recalled
less words than did the nonconverter group which, in turn, recalled
less words than did the NC group ( p ⬍ .001 in both cases; Table
2). The type of list effect, F(1, 186) ⫽ 12.97, p ⬍ .001, was due
to better average recall from the related (5.88) than from the
unrelated (5.54) list. The Group ⫻ Type of List interaction was
significant, F(2, 186) ⫽ 6.14, p ⫽ .003. In fact, although on
average NCs recalled significantly more words from the related
than the unrelated list (7.78 vs. 7.01, p ⬍ .001), the nonconverter
and converter groups recalled a comparable number of words from
the two lists (5.43 vs. 5.33 and 4.43 vs. 4.27, respectively; p ⫽ ns
in both cases). The significant trial effect, F(4, 744) ⫽ 338.56, p ⬍
.001, was an expression of the learning process passing from the
first to the fifth recall trial. The Group ⫻ Trial interaction was
significant, F(8, 744) ⫽ 21.57, p ⬍ .001. Indeed, the learning rate,
based on the improvement in performance passing from the first to
the fifth immediate recall trial, was significantly higher in the NC
than in the nonconverter group ( p ⬍ .001) and in the nonconverter
than in the converter group ( p ⫽ .04; Table 2). Finally, the
Group ⫻ Type of List ⫻ Trial interaction was not significant
(F ⫽ 0.46).
Short-term memory component. It is generally held that
whereas immediate recall of early and mid-list items in a word list
is an expression of pure long-term memory processes, the retrieval
of the last few items in a list represents the overlapping of short-
term and long-term memory processes (Carlesimo, Fadda, et al.,
1996; Koppenaal & Glanzer, 1990; Waugh & Norman, 1965). We
adopted Waugh and Norman’s method (1965) and calculated the
short-term memory component implicated in recall of the terminal
items of the list (serial positions 15 and 16) by correcting perfor-
mance accuracy over the middle part of the list (serial positions 10
and 11), considered as the most reliable estimate of the long-term
memory contribution to recall.1 A one-way ANCOVA showed that
nonconverter, converter, and NC groups did not differ with regard
to the cumulated short-term memory values corresponding to trial
positions 15 and 16, F(2, 226) ⫽ 1.15 (Table 2).
Semantic encoding. We analyzed the ability to take advantage
of the semantic relatedness between words on a list to improve
recall by studying clustering behavior in the free recall of the
categorized list (i.e., the tendency to recall words belonging to the
same category in immediate succession). To this aim, we com-
puted, for each immediate recall trial of the semantically related
list, the adjusted ratio of clustering score, developed by Roenker,
Thompson, and Brown (1971) and used in previous studies of
aging and memory (Delis et al., 1991; Carlesimo et al., 1998). A
Group ⫻ Trial two-way ANCOVA revealed a significant differ-
ence between groups, F(2, 229) ⫽ 8.14, p ⬍ .001. Post hoc
comparisons showed significantly better average adjusted ratio of
clustering scores in NCs than in nonconverters ( p ⫽ .02) and
converters ( p ⬍ .001); the difference between the two a-MCI
subgroups approached significance ( p ⫽ .08; Table 2).
Forgetting. The forgetting rate passing from the last immedi-
ate to the delayed recall trial of both related and unrelated lists was
investigated by a three-way Group ⫻ Type of List ⫻ Trial (5th
immediate vs. 15-min delayed) ANCOVA. The critical Group ⫻
Trial interaction was highly significant, F(2, 186) ⫽ 14.4, p ⬍
1
Waugh and Norman (1965) suggested the following formula: STMi ⫽
Ri – LTMi / 1 – LTMi where STMi and LTMi represent the probability of
item i being retained in STM and LTM, respectively; Ri is the probability
of recalling an item belonging to the recency part of the curve. STM ⫽
short-term memory; LTM ⫽ long-term memory.
Table 2
Summary of Most Relevant Performance Scores Exhibited by the Nonconverter, Converter, and NC groups on the Tests of the Neuropsychological Experimental Battery
Effect size (Nonconverter Effect size (NC Effect size (NC vs.
Measure Nonconverter Converter NC vs. converter) vs. converter) nonconverter)

Explicit long-term memory

Word list recall

Learning Immediate recall 5.38e (1.4) 4.35a,c (1.1) 7.40 (1.9) 0.81 1.96 1.21
Learning rate (I vs. V trial) ⫹3.0e (1.8) ⫹2.2b,c (1.7) ⫹4.9 (1.7)
Semantic 0.3 0.7 0.4
Encoding (related list) ARC Score ⫹0.12f (0.3) ⫹0.03c (0.3) ⫹0.24 (0.3)
Forgetting Decline (V Imm. vs. Delayed ⫺2.42f (1.6) ⫺3.30b,c (1.6) ⫺1.86 (1.2)
recall)
Recognition d⬘ score 1.71e (1.3) 1.04a,c (1.1) 3.32 (1.4) 0.55 1.81 1.19
C score 0.69e (1.2) 0.38b,c (0.8) 1.91 (0.9) 0.39 1.79 1.15
Prose recall
Learning Immediate recall 3.97e (2.2) 3.05a,c (2.0) 5.68 (1.4) 0.43 1.52 0.92
Forgetting Decline (Imm. vs. Delayed recall) ⫺0.6 (2.4) ⫺1.08d (2.4) ⫺0.21 (1.2)
Rey’s Figure Form B
Learning Immediate recall 15.3f (6.8) 11.4a,c (7.2) 17.58 (5.6) 0.55 0.95 0.36
Forgetting Decline (Imm. vs. Delayed recall) ⫺1.25 (4.4) ⫺2.77b,d (5.9) ⫺0.69 (2.3)

Short-term memory

Word list recall

Serial position curve Positions 15–16 1.03 (0.5) 1.1 (0.5) 1.16 (0.5) ⫺0.14 0.11 0.25

Implicit memory

Stem completion Studied words 6.98 (4.1) 6.27 (3.9) 5.16 (2.5)
Unstudied words 3.26 (3.1) 2.93 (2.7) 2.10 (1.5)
MEMORY PROFILE IN AMNESTIC MCI SUBJECTS

Priming effect ⫹3.72 (3.7) ⫹3.34 (2.8) ⫹3.06 (2.5) 0.11 ⫺0.10 ⫺0.21
Fragmented picture identification test Old figures 4.36 (0.8) 3.78 (1.0) 4.51 (0.8)
New figures 3.68 (0.6) 3.66 (1.1) 3.63 (0.7)
Priming effect ⫹0.68 (0.7) ⫹0.12a,c (0.7) ⫹0.88 (0.6) 0.80 ⫺1.16 ⫺0.30

Note. Data are presented as M (SD). Effect sizes are Cohen’s d. NC ⫽ normal control; ARC ⫽ adjusted ratio of clustering.
a
Nonconverters vs. converters significant difference ( p ⬍ .001).
b
Nonconverters vs. converters significant difference ( p ⬍ .05).
c
Converters vs. NCs significant difference ( p ⬍ .001).
d
Converters vs. NCs significant different ( p ⬍ .05).
e
Nonconverters vs. NCs significant difference ( p ⬍ .001).
f
Nonconverters vs. NCs significant difference ( p ⬍ .05).
553
554
Explicit long-term memory
Short-term memory
Implicit memory
1
-0.2 0 0.2 0.4
Figure 1. Effect sizes from the converters versus nonconverters comparisons on the explicit long-term,
short-term, and implicit memory tests. d⬘ was a measure of the memory effect, that is, of the subject’s ability to
discriminate between previously studied and unstudied words; C was a measure of the subject’s overinclusion
strategy. ARC ⫽ adjusted ratio of clustering.
.001. Planned comparisons revealed a smaller immediate-delayed
recall decline in the NC than in the nonconverter group ( p ⫽ .032),
which, in turn, forgot less than did the converter group ( p ⫽ .003;
Table 2). The three-fold Group ⫻ Type of List ⫻ Trial interaction
was also significant, F(2, 186) ⫽ 5.97, p ⫽ .003. Indeed, whereas
NCs forgot significantly less from the related than the unrelated list
(–1.55 vs. –2.19, p ⬍ .01), the nonconverter group forgot a
comparable number of words from the two lists (–2.63 vs. –2.22,
p ⫽ ns), and the converter group forgot more from the related than
the unrelated list (–3.64 vs. 2.95, p ⫽ .045).
Word-list recognition. Performance on the recognition tests
for both the related and unrelated word lists was scored according
to the signal detection theory (Kamman, 1970). Therefore, two
indices were calculated: d⬘ was a measure of the memory effect,
that is, of the subject’s ability to discriminate between previously
studied and unstudied words; C was a measure of the subject’s
overinclusion strategy. The mean d⬘ scores obtained by the three
groups were analyzed by a two-way Group ⫻ Type of List
ANCOVA. The significant group effect, F(2, 265) ⫽ 60.41, p ⬍
.001, was due to NCs scoring significantly higher than did non-
converters ( p ⬍ .001) who, in turn, obtained a significantly higher
d⬘ score than did converters ( p ⬍ .001; Table 2).
The mean C scores obtained by the three groups were also
analyzed. The significant group effect, F(2, 264) ⫽ 47.83, p ⬍
.001, was due to the significantly higher NC group than noncon-
verter group C score ( p ⬍ .001), which, in turn, was significantly
higher than that of the converter group ( p ⫽ .046; Table 2). Also
the Group ⫻ Type of List interaction was significant, F(2,
265) ⫽ 3.96, p ⫽ .02. In fact, NCs made fewer false alarms on the
unrelated than the related list (C ⫽ 2.07 vs. 1.78, p ⫽ .017),
whereas nonconverter and converter groups made a comparable
number of false alarms on the two lists (C ⫽ 0.61 vs. 0.77 and 0.42
vs. 0.34, respectively).
Prose Recall
Performance scores on the immediate and delayed recall of the
short story were analyzed by a two-way Group ⫻ Trial (immediate
PERRI ET AL.
Word List Immediate Recall
Word List – ARC Score
Word List Recognition d´ score
Word List Recognition C score
Prose Immediate Recall
Rey’s Figure Immediate Recall
Word List - Serial Position Curve
Fragmented Identification Picture test - Priming
Stem Completion - Priming
0.6 0.8 1
vs. delayed) ANOVA. The group effect, F(2, 270) ⫽ 55.56, p ⬍
.001, revealed better recall in NCs (5.58) than in the nonconverter
group (3.67), which, in turn, recalled better than did the converter
group (2.51; in all cases p ⬍ .001). The Group ⫻ Delay interac-
tion, F(2, 270) ⫽ 3.20, p ⫽ .042, was due to the higher perfor-
mance decrement passing from immediate to delayed recall in the
converter group with respect to NCs ( p ⫽ .012); the forgetting rate
in the nonconverter group fell between those of the NC and
converter groups and did not significantly differ from either group
(Table 2).
Rey’s Figure Form B Reproduction
Performance scores obtained by the three groups on the imme-
diate and delayed reproduction of Rey’s Figure were analyzed by
a two-way Group ⫻ Trial ANCOVA. To correct for the construc-
tive ability of each individual subject, performance scores on the
copy test were inserted in this analysis as a covariate. The signif-
icant group effect, F(2, 263) ⫽ 19.10, p ⬍ .001, was due to the
higher memory scores of NCs (17.18) than nonconverter subjects
(14.7; p ⫽ .003) who, in turn, remembered significantly more than
did converter subjects (10.1; p ⬍ .001). The Group ⫻ Trial
interaction, F(2, 264) ⫽ 4.52, p ⫽ .012, revealed that the perfor-
mance decrement passing from the immediate to the delayed
reproduction test in the converter group was larger than that shown
by the nonconverter group ( p ⫽ .02) and NCs ( p ⫽ .004), which
did not differ reciprocally (Table 2).
Implicit Memory
Stem Completion
Performances on the stem completion test were submitted to a
two-way Group ⫻ Study Condition (unstudied vs. studied words)
ANCOVA. The group effect, F(2, 271) ⫽ 7.08, p ⫽ .001, was due
to the fact that NCs completed significantly less stems with words
from the experimental list (both studied and unstudied; 3.63) than
nonconverter (5.12) and converter (4.61) groups ( p ⬍ .001 and
 MEMORY PROFILE IN AMNESTIC MCI SUBJECTS 555

p ⫽ .025, respectively), which did not differ one from each other studied and unstudied words. We wanted to obtain an index of
( p ⫽ ns). The study condition effect, F(1, 272) ⫽ 327.22, p ⬍ sensitivity and specificity from the subjects’ performances on the
.001, revealed a robust priming (6.14 vs. 2.77 for words on the four delayed recall tasks of the memory battery that demonstrated
studied and unstudied lists, respectively), which, as revealed by a higher sensitivity to the memory deficit in the converter group
nonsignificant Group ⫻ Study Condition interaction, F(2, (unrelated and related word lists, prose recall, and Rey’s Figure
272) ⫽ 1.08, did not differ among the groups (Table 2). recall), so we computed an average z score on the four tasks for
each subject and calculated the number of subjects in the converter
Fragmented Picture Identification Test and nonconverter groups who performed over 1.5 standard devi-
ations below the NC group mean. This cumulative index of de-
Performance scores of the second session of the fragmented layed recall reached a sensitivity of 75% and a specificity of 68.5%
picture identification test were submitted to a two-way ANCOVA in discriminating subjects in the converter and nonconverter
with group as between-factor and drawing set (old figures vs. new groups.
figures) as within-factor. The group effect was nonsignificant, F(2,
265) ⫽ 1.53. Instead, the drawing set effect was significant, F(1,
266) ⫽ 165.65, p ⬍ .001. Indeed, the average identification score Discussion
was significantly lower in the new (3.66) than in the old set of In the present research, we investigated episodic long-term,
figures (4.22), revealing a significant overall repetition priming short-term, and implicit memory abilities in a group of a-MCI
effect. The Group ⫻ Trial interaction was also significant, F(2, subjects with absence of impairment in cognitive areas other than
266) ⫽ 25.07, p ⬍ .001, because of a highly significant priming memory and without confounding medical or psychiatric condi-
effect in NCs and in the nonconverter group ( p ⬍ .001 in both tions at the time of clinical diagnosis. We attempted to define
cases) and a lack of significant priming in the converter group differences between subjects who showed substantial cognitive
(F ⫽ 2.27; Table 2). stability and subjects who progressed toward AD during a 2-year
period. Results showed that subjects who converted to AD in the
Sensitivity and Specificity of Individual Tests to a-MCI following 2 years were more severely impaired than were subjects
Subjects’ Episodic Memory Deficit who did not progress toward dementia during the same period of
time on virtually all of the episodic memory indexes examined.
To evaluate the sensitivity and specificity of the individual tests
Tests assessing the delayed free recall of verbal and visual material
of the experimental battery in detecting episodic memory deficits
demonstrated the greater sensitivity to the memory deficit in con-
of subjects with a-MCI, we calculated the number of subjects in
verter subjects.
the converter and nonconverter groups who obtained scores below
the normality cutoff on each test of the memory battery that we had
normative data for (Table 3). For the recognition tests, we calcu- Episodic Long-Term Memory
lated a single score as the sum of the correct recognition of both
We found that a-MCI subjects’ ability to learn verbal and visual
material was defective compared with those of NCs, in agreement
with previous reports (Perri et al., 2005; Petersen et al., 1999).
Table 3
Poor learning abilities were particularly evident in a multitrial
Percentage of Subjects in the Nonconverter and Converter
word-list recall task in which a-MCI subjects showed less perfor-
Groups Who Scored Below the Normality Cutoff on the
mance improvement in performance passing from the first to the
Experimental Memory Battery and the Delayed Recall
fifth recall trial. In all tasks, the learning impairment was more
Cumulative Index
severe in converter than in nonconverter subjects.
Test Nonconverter Converter Analysis of the forgetting rate quite consistently documented a
larger performance decrement passing from immediate to delayed
Unrelated word list recall in the converter than in the nonconverter group. It is possible
Immediate recall 21.6 35.4
Delayed recall 28.8 63.2
that short-term memory processes could have contributed to the
Recognition 27.0 38.0 immediate recall task. In fact, previous evidence has documented
Related word list comparable forgetting rates in early AD patients and NCs when the
Immediate recall 30.6 50.6 experimental paradigm removed the contribution of short-term
Delayed recall 41.4 77.2 memory processes to immediate recall (Kopelman, 1985; Car-
Recognition 31.5 54.4
Prose recall lesimo et al., 1998). As a result, the converter subjects’ accelerated
Immediate recall 24.3 35.4 forgetting rate (and, limited to the word-list recall tasks, that of the
Delayed recall 36.0 59.49 nonconverter subjects) can be interpreted as an expression of the
Rey’s Figure decay of short-term memory traces passing from immediate to
Immediate reproduction 8.1 17.7
Delayed reproduction 11.7 35.4
delayed recall that were not compensated by an adequate transfer
Delayed recall of information from short- to long-term memory stores.
Cumulative index 31.5 75 Our results confirmed the reduced ability of a-MCI subjects to
take advantage of the semantic structure of the memorandum to
Note. Normality cutoff was determined for each test in the battery as the
lower limit of the 95% tolerance interval for a confidence level of 95% and
improve their memory performance (Perri et al., 2005; Petersen et
for the index as scores over 1.5 standard deviations below the means of al., 1999). This deficit seemed comparably severe in both converter
normal control groups. and nonconverter subjects. Indeed, neither of the two groups
556 PERRI ET AL.
showed the better learning and reduced forgetting rate on the
related with respect to the unrelated word list that was evident in
the NC group performance. Nor did they show the increase in false
alarms in recognizing the related with respect to the unrelated
word list observable in the NC group (a confounding effect due to
the fact that the studied and unstudied words of the related list
belonged to the same semantic categories). Moreover, both a-MCI
groups showed poor semantic clustering of words on the related
list during recall. In this case, however, the deficit was particularly
evident in the patients with incipient AD. Indeed, the difference in
the semantic clustering score of converter and nonconverter groups
was near statistical significance.
The two word-list recognition tests documented reduced avail-
ability of memory traces and increased sensitivity to interference
from irrelevant material in converter and, to a lesser extent, in
nonconverter subjects. Indeed, the two groups obtained lower d⬘
and C scores (i.e., they recognized fewer studied items and made
more false alarms) than did NCs.
Short-Term Memory
Analysis of the short-term memory component in the immediate
recall of the unrelated word list supports the normality of this
memory component in subjects affected by a-MCI. The integrity of
short-term memory even in the converter group further strengthens
previous claims that although mild AD patients generally show a
short-term memory deficit (Orsini, Trojano, Chiacchio, & Grossi,
1988), this deficit may not appear in the preclinical phase of AD
(Backman & Small, 1998; Perri et al., 2005).
Implicit Memory
Both nonconverter and converter subjects disclosed a normal
priming effect in the stem completion test. Instead, on the frag-
mented picture identification test, converter subjects revealed re-
duced visual priming compared with both nonconverters and NCs.
These results seem to suggest the presence of intact priming for
verbal stimuli and reduced priming for visual data in MCI subjects
who eventually converted to AD. However, these results could
also reflect greater contamination caused by explicit memory pro-
cesses during performance of the fragmented picture identification
with respect to the stem completion test. In particular, explicit
memory could have favored the recognition of old figures in the
fragmented picture identification test, thus resulting in a larger
facilitation rate in nonconverter and NC groups than in converters.
Indeed, the high effect size produced by the comparison of priming
shown by converters with respect to nonconverters on this test is
similar to the one resulting from the comparison of the two groups
on the word-list immediate recall (i.e., on an explicit memory test)
but very different from the effect size produced by the comparison
of the priming shown by the two groups on the stem completion
test. In support of this view, a correlation analysis conducted on
the overall sample (converters, nonconverters, and NCs) revealed
that the priming scores on the stem completion test did not corre-
late with any of the performance scores on the explicit memory
tasks of the experimental battery (Pearson’s r consistently ⬍ .10).
Indeed, in the same subjects the size of the priming in the frag-
mented picture identification test correlated with the performance
scores on each of the explicit tests of the memory battery (Pear-
son’s r ranging from .15 to .29, p consistently ⬍ .02). Finally,
priming scores on the visual and verbal tests were not correlated
with each other (Pearson’s r ⫽ –.36).
To summarize, the present data confirm that the a-MCI subjects’
memory profile is characterized by preserved short-term and im-
plicit memory and extensive impairment of episodic long-term
memory (Perri et al., 2005). This memory profile, which closely
resembles that exhibited by amnestic patients with bilateral MTL
lesions (Gabrieli, 2001), supports a precocious phase in preclinical
AD characterized by selective involvement of the mesial–temporal
areas (Braak et al., 1993) and worsening of the memory impair-
ment as atrophic changes progress in the hippocampal structures
(Fox et al., 1996). This is consistent with the view that when
patients meet the criteria for a-MCI, at least in the absence of
comorbid conditions, it is highly probable that they have early AD
(Morris et al., 2001; Petersen et al., 2001). Increased sensitivity to
interference, as revealed by reduced ability to discriminate be-
tween experimental and irrelevant material in word recognition
tasks, could also be related to mesial–temporal pathology (see
Kopelman, 2002). However, reduced ability to inhibit incorrect
responses could also be due to a dysexecutive impairment related
to a frontal lobe pathology (Tierney et al., 1996). Finally, the
substantial integrity of implicit memory, as measured by word-
stem completion priming in subjects with a-MCI, supports the
view that perceptual priming, especially as related to functioning
of posterior cortical regions, may not be involved in the early
phases of the AD pathology (Fleischman et al., 2005).
These findings are only in apparent contrast with the frequently
reported involvement of many cognitive functions besides memory
in the preclinical phase of AD (such as executive functioning and
attention, but also verbal abilities, perceptual speed, or implicit
memory; Backman, Jones, Berger, Small, & Laukka, 2005; Spaan,
Raaijmakers, & Jonker, 2005). Indeed, because the aim of the
present study was to highlight the characteristics of the memory
deficit in the very early phases of AD, by selecting a-MCI subjects
we excluded those individuals whose pattern of cognitive impair-
ment suggested more diffuse brain involvement, even in the ear-
liest phases.
Although cognitive deficits have often been investigated in the
preclinical phase of AD (Petersen et al., 1999; Tierney et al.,
1996), this is the first systematic comparison of episodic long-
term, short-term, and implicit memory features in subjects with an
isolated memory deficit who either developed AD or did not. In the
present study, we document a qualitatively similar profile of mem-
ory impairment in the converter and nonconverter a-MCI groups
even though the amnestic syndrome of subjects with incipient AD
resulted systematically more severely. Indeed, for virtually all of
the episodic memory indexes examined (learning, forgetting, rec-
ognition abilities) a-MCI subjects who converted to AD in the
following 2 years were more severely impaired than were subjects
who did not progress toward dementia during the same period of
time. In this context of pervasive episodic memory impairment,
tests assessing the free recall of verbal and visual material follow-
ing a delay interval demonstrated greater sensitivity to the memory
deficit in converter subjects. However, because these memory
indexes were also those most sensitive to the memory deficit in the
nonconverter group, individual tests showed relatively low speci-
ficity in identifying subjects in the preclinical phase of AD. In any
case, the use of a combined performance index on the four delayed
 MEMORY PROFILE IN AMNESTIC MCI SUBJECTS
recall tasks of the memory battery permitted distinguishing con-
verter from nonconverter subjects with 75% sensitivity and 68.5%
specificity. This result supports the use of multiple tasks, all
exploring delayed free recall, to increase the diagnostic power of
neuropsychological tools in identifying a-MCI subjects progress-
ing toward dementia. However, note that this finding was obtained
in a population affected by memory deficits and at high risk for
developing dementia (Petersen et al., 2001). Therefore, some sub-
jects in the nonconverter group could develop dementia over a
longer period of time than the 2 years of the present observation.
For this reason, only a longer follow-up period will permit us to
better define the discriminative power of the individual episodic
memory tasks and of the entire memory battery.
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Accepted April 11, 2007 䡲

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are interested in, and describe your area of expertise. Be as specific as possible. For example,
“social psychology” is not sufficient—you would need to specify “social cognition” or “attitude
change” as well.

• Reviewing a manuscript takes time (1– 4 hours per manuscript reviewed). If you are selected to
review a manuscript, be prepared to invest the necessary time to evaluate the manuscript
thoroughly.

Write to Journals Office, American Psychological Association, 750 First Street, NE, Washington,
DC 20002-4242.