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Neuropsychologia
journal homepage: www.elsevier.com/locate/neuropsychologia
a r t i c l e
i n f o
Article history:
Received 9 April 2011
Received in revised form
18 December 2011
Accepted 20 December 2011
Available online 13 January 2012
Keywords:
Episodic memory
Long-term binding
Encoding
Virtual reality
Aging
Dementia
Mild cognitive impairment
a b s t r a c t
Most neuropsychological assessments of episodic memory bear little similarity to the events that patients
actually experience as memories in daily life. The rst aim of this study was to use a virtual environment
to characterize episodic memory proles in an ecological fashion, which includes memory for central
and perceptual details, spatiotemporal contextual elements, and binding. This study included subjects
from three different populations: healthy older adults, patients with amnestic mild cognitive impairment
(aMCI) and patients with early to moderate Alzheimers disease (AD). Second, we sought to determine
whether environmental factors that can affect encoding (active vs. passive exploration) inuence memory
performance in pathological aging. Third, we benchmarked the results of our virtual reality episodic
memory test against a classical memory test and a subjective daily memory complaint scale. Here, the
participants were successively immersed in two virtual environments; the rst, as the driver of a virtual
car (active exploration) and the second, as the passenger of that car (passive exploration). Subjects were
instructed to encode all elements of the environment as well as the associated spatiotemporal contexts.
Following each immersion, we assessed the patients recall and recognition of central information (i.e., the
elements of the environment), contextual information (i.e., temporal, egocentric and allocentric spatial
information) and lastly, the quality of binding. We found that the AD patients performances were inferior
to that of the aMCI and even more to that of the healthy aged groups, in line with the progression of
hippocampal atrophy reported in the literature. Spatial allocentric memory assessments were found
to be particularly useful for distinguishing aMCI patients from healthy older adults. Active exploration
yielded enhanced recall of central and allocentric spatial information, as well as binding in all groups. This
led aMCI patients to achieve better performance scores on immediate temporal memory tasks. Finally,
the patients daily memory complaints were more highly correlated with the performances on the virtual
test than with their performances on the classical memory test. Taken together, these results highlight
specic cognitive differences found between these three populations that may provide additional insight
into the early diagnosis and rehabilitation of pathological aging. In particular, neuropsychological studies
would benet to use virtual tests and a multi-component approach to assess episodic memory, and
encourage active encoding of information in patients suffering from mild or severe age-related memory
impairment. The benecial effect of active encoding on episodic memory in aMCI and early to moderate
AD is discussed in the context of relatively preserved frontal and motor brain functions implicated in
self-referential effects and procedural abilities.
2011 Elsevier Ltd. All rights reserved.
1. Introduction
Episodic memory may be described as the conscious recollection of personal events combined with their phenomenological
Corresponding author at: Memory and Cognition Lab, 71 avenue Edouard Vaillant, 92774, Boulogne-Billancourt, France. Tel.: +33 1 55 20 59 22;
fax: +33 1 55 20 58 53.
E-mail address: pascale.piolino@parisdescartes.fr (P. Piolino).
0028-3932/$ see front matter 2011 Elsevier Ltd. All rights reserved.
doi:10.1016/j.neuropsychologia.2011.12.013
and spatiotemporal encoding contexts (Tulving, 2002). The multiple components of memory (central and contextual information)
that together form a complete episodic memory are thought to be
linked through a process known as binding (Kessels, Hobbel, &
Postma, 2007), mainly supported by the hippocampus (Slotnick,
2010). Numerous studies have demonstrated that episodic memory
impairment is one of the hallmarks of early clinical manifestations of Alzheimers disease (AD) (Hodges, 2006) and amnesic
mild cognitive impairment (aMCI) (Petersen et al., 2001, 1999). In
parallel, some researchers have reported reduced volume in the
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neuropsychological studies have used VR to test memory in pathological aging. Previous studies have mainly focused on navigational
processes. Some studies with aMCI patients (Cushman, Stein, &
Duffy, 2008) have found a close relationship between performance
in virtual and real environments. Moreover, other studies with
AD patients (Burgess, Trinkler, King, Kennedy, & Cipolotti, 2006;
Drzezga et al., 2005; Zakzanis, Quintin, Graham, & Mraz, 2009)
have specically found allocentric spatial impairments. Widmann,
Beinhoof and Riepe (2012) immersed AD patients and healthy participants in a virtual environment to assess the learning of verbal
material in situations that imitate natural conditions. AD patients
were found to be impaired in free memory recall of shop names
compared to healthy participants, and the impairment was more
marked than that observed with classical list-learning. The study
argued that list-learning paradigms wrongly estimated the memory capacities of patients in every day situations. Recently, we
developed a virtual reality test that seeks to reect the denition of
episodic memory more closely than other standard neuropsychological tests (for review, Plancher, Nicolas, & Piolino, 2008). Various
aspects of episodic memory (what, where, when, and binding)
were evaluated in a population of young adults and healthy older
adults after they drove a car in a virtual environment representing
a city with different, but specic, areas and elements (Plancher,
Gyselinck, Nicolas, & Piolino, 2010). We observed a difference
between the healthy aged controls and younger participants in
memory for spatiotemporal context and binding. Moreover, the virtual test was sensitive to the older subjects memory complaints,
which was contrary to the standard verbal episodic memory test.
One aim of the present study, which follows-up on results
obtained by Plancher et al. (2010), was to use this new VR test to
determine changes in the various components of episodic memory
in pathological aging by comparing aMCI and AD patients with a
new population of healthy aged controls. In addition, we aimed to
test whether environmental inuences on encoding could improve
memory performance. Precisely, we sought to determine if active
exploration of the virtual environment improves memory compared to passive exploration. It has been previously demonstrated
that presenting information in the memory environment can serve
as compensatory support for decient self-initiated processing
and can enhance memory performance (Craik, 1983, 1986; Luo &
Craik, 2008; Naveh-Benjamin, Craik, & Ben-Shaul, 2002, for review).
For example, positive effects of environmental support have been
observed when older participants beneted from the provision of
more elaborate pictorial information (Park, Puglisi, & Smith, 1986;
Schacter, Israel, & Racine, 1999) or context and semantic organizational structure of materials (Park, Smith, Morrell, Puglisi, & Dudley,
1990). An active exploration involves cognitive processes that are
different than those engaged during passive exploration. In particular, personal involvement is higher in active exploration, which
may potentially result in a self-reference effect that is known to
improve memory, even in aging (Gutchess, Kensinger, & Schacter,
2010; Lalanne et al., 2010; Ruby et al., 2009). In addition, encoding information through motion may solicit, even if it is far from
real movements, some procedural skills. Self-referential effect and
procedural skills mainly depend on medial prefrontal cortex (Craik
et al., 1999; Kelley et al., 2002; Martinelli, Sperduti, & Piolino,
in press), striatum and motor cortex respectively (Nilsson et al.,
2000; Nyberg et al., 2001; Pennartz, Ito, Verschure, Battaglia, &
Robbins, 2011; Squire, 2004). These processes and the underlying
cortical structures would be partially preserved in mild AD (Chase
et al., 1984; Grady et al., 2003). Learning based on implicit procedural skills appears to be one of the best preserved skills found
in AD patients (Deweer et al., 1994; Deweer, Pillon, Michon, &
Dubois, 1993; Gabrieli, Corkin, Mickel, & Growdon, 1993; Hirono
et al., 1997; Lipinska & Backman, 1997; Van Halteren-van Tilborg,
Scherder, & Hulstijn, 2007). Further, some studies have previously
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2. Methods
2.1. Participants and experimental design
Twenty-one healthy older participants (17 female and 4 male; mean age = 76.95;
SD = 5.8; min = 67, max = 88), 15 aMCI patients (8 female and 7 male; mean
age = 78.06; SD = 5.76; min = 70, max = 88), and 15 patients with AD (13 female and
2 male; mean age = 76.53; SD = 5.51; min = 69, max = 88) voluntarily participated in
this study. Early to moderate AD and aMCI patients were recruited from hospitals
in Paris, France, according to the criteria of the National Institute of Neurological
Disorders and Stroke and the Alzheimers Disease and Related Disorders Association (McKahnn et al., 1984). MCI participants met the criteria for an amnestic
single-domain form of MCI as dened by Petersen et al. (2001). The clinical diagnostic criteria for aMCI included the presence of a memory complaint, impaired
memory function (recall performance on a standard episodic memory test 1.5
standard deviations below age- and education-matched norms), preserved general
cognitive function, intact activities of daily living, and the absence of dementia.
All participants gave their informed consent before beginning the study. The study
was performed in compliance with the Declaration of Helsinki. The healthy participants were recruited from a local panel of volunteers and also lled in a medical
questionnaire to verify that they had no previous neurological or psychiatric disorders and were not undergoing any treatments that would affect their cognition.
All participants had to meet several criteria prior to being included in this study:
no decit in color recognition (color blindness test), no hemi-neglect (clock test)
and a visual eld that covers a minimum angle of 46 (visual eld test). In addition,
the Mini Mental State Exam (MMSE) was used to evaluate the level of dementia
of each group (Folstein, Folstein, & McHugh, 1975). Healthy older adults scored
at least 27 (max = 30) (indicating an absence of dementia), AD patients scored at
least 14 (indicating an early to moderate stage of dementia) and aMCI patients
scored at least 24. Participants also received the minimal version of the Geriatric
Depression Scale (Clment, Nassif, Lger, & Marchan, 1997; Yesavage, 1988) to
ensure that depressive conditions would not affect the participants memory performance. Given that experiences with driving in real life could be related to abilities
used to drive a virtual car, all participants were required to have a drivers license.
Finally, the level of education and gender distribution was different among the
groups, as the aMCI patients level of education and number of men was signicantly greater than that of the other groups (p < .01, 8 female participants and 7
male participants). Thus, we included both variables as covariates in all statistical
analyses.
The present study manipulated three variables: population (healthy older adults,
aMCI patients, AD patients), exploration (active and passive) and recall (immediate
and delayed) within participants. Each exploration was associated with one environment. The assignment of the exploration to the environment and the order in
which participants encountered them were counterbalanced.
595
Table 1
Means and SDs of demographics and general neuropsychological abilities.
Older adults (n = 21)
AD patients (n = 15)
ANOVA/ANCOVAS
Age (years)
Level of educationd
Gender (male:female)
76.9 (5.8)
3.5 (1.5)
(4:17)
78 (5.7)
5 (1.7)
(7:8)
76.5 (5.5)
3.2 (1.5) b , **
(2:13)
Depression
Mini GDS (cut-off <2/5)
.4 (.9)
.1 (.3)
.8 (1.3)
F<1
Global cognition
MMSE
CDS
28.7 (.8)
22.7 (12.6)
26.5 (1.6)c , *
43.5 (14.5)c , *
Semantic abilities
Mill Hill
34.37 (7.1)
34.06 (7.6)
25 (7.3)a , *** , b , **
Executive functions
TMTA (s)
TMTB-A (s)
Inhibition
Forward span
Backward span
48.8 (13.4)
160.4 (119)
16.4 (23.8)
5.8 (.3)
3.4 (.9)
52.3 (24.1)
65 (46)
34.2 (17.5)
5.2 (1.1)c , *
2.8 (.6)c , *
Verbal memory
Immediate recall
Total recall (3 trials)
Delayed total recall
Intrusions
Perseverations
Recognition: hits/false recognitions
15.9 (.21)
46.8 (1.1)
15.9 (.2)
0
0
15.7 (.6)/(0)
13.6 (1.8)c , **
32.2 (8.4)c , ***
11.8 (3)
1.6 (1.4)c , **
.7 (1.5)
13.5 (1)/1(1)
Scores show impairment in Alzheimer disease (AD) relative to the mean scores of matched control older adults.
Scores show impairment in AD relative to the mean scores of amnesic Mild Cognitive Impairment (aMCI) patients.
c
Scores show impairments in aMCI relative to the mean scores of matched control older adults.
d
According to Poitrenaud. Level 1 = illiterate; 2 = able to read, write, count; 3 = 5 years of education, corresponding to the end of the elementary school; 4 = 8 years of
education; 5 = 10 years of education; 6 = Bachelors degree; 7 = postgraduate studies (Masters, Phd).
*
p < .05.
**
p < .01.
***
p < .001.
b
participants received instructions to not stop within the environment. Given that
each passive participant was matched with an active participant, the test times were
also globally matched across the conditions.
Immediately after the immersion, the participants performed recall and recognition tests that assessed their episodic memory of the environment. We used a series
of oral memory tests that were previously validated by a VR study on memory and
aging (Plancher et al., 2010). After 20 min, the participants performed the delayed
recall in a similar manner to the rst immediate recall. Likewise, the participants
also performed the neuropsychological tests during an interval of 20 min. Following, the participants were also immersed in a second environment, either as active
or passive explorers (the counterpart to the rst immersion), and were instructed
to follow the same procedure. After the second immediate recall, the participants
performed other neuropsychological tests. Subjects were assessed on two different
days to avoid overly long sessions.
2.4.3. Immediate recall test
When participants remembered an element, they had to spell out any remembered details as well as the associated spatiotemporal context. The experimenter
would note all recalls on a structured grid of responses. There was no specic order in
the recall of the components. Once the element was recalled, the participants could
then provide contextual recall in any order. The participants were never probed. For
each recall test, the instructions were associated with an example as follows:
Fig. 1. Overview of the city environment and picture of a specic area (newsstand with a man and a bench on the right).
596
- Try to remember all the elements you saw in the town (e.g., a girl, the post ofce,
the restaurants, a bench) (what, maximum = 35)
- Give as many perceptual details about the elements as possible (e.g., the girl was
wearing an orange t-shirt) (details)
- Situate the elements in time: were they at the beginning, the middle, or at the
end of the town? (when)
- Situate the elements of the scene to each other (e.g., the girl was to the left of
the post ofce) (allocentric where)
- Try to remember if you turned left or right after the element (egocentric where).
For example, one possible answer could be: at the beginning of the town (when),
there was a park (what) and a girl (what); the girl was wearing an orange tee-shirt
(detail); she was in front of the park (allocentric where); I turned left after this scene
(egocentric where). In total, 5 min were allowed for each verbal recall. Two experts
rated each memory and any difference of opinion between the experts was discussed
until a consensus was reached.
In addition, we computed a binding score. For each element recalled, we noted
whether the participants recalled the associated components (details, when, allocentric where and egocentric where). For example, if they recalled the shops, did they
recall where, when and the details associated with this element? The binding score
for a subject is the sum of all the contextual recalls associated with the elements
recalled. For example, if one participant recalled 5 elements with 1 piece of temporal information, 2 details and 4 allocentric spatial recalls in total, they had a binding
score of 7.
2.4.4. Recognition
The recognition task was composed of written sentences presented on the computer screen that described the presence of elements (e.g., there was a church in
the town), spatial relationships between elements (e.g., a man was at the right of
the newsstand), and temporal relationships between elements (e.g., the train station was before the fountain). There were eight sentences per category: the correct
response to half of the sentences was yes and to the other half was no. The test
included a total of 24 sentences. Participants gave their answers orally. The correct answers were split into what recognitions, where recognitions, and when
recognitions and corresponded to the number of correct hits and correct rejections. A recognition can rely on an episodic recollection (autonoetic consciousness)
as well as on a feeling of familiarity (noetic consciousness). To learn about the quality
of the recognitions in more detail, we complemented the recognition task with the
Remember/Know/Guess (recollection/familiarity/uncertainty) paradigm after each
recognition test (Gardiner, 1988, 2001; Tulving, 1983, 1985). In this paradigm, the
subjects were asked to verbalize aloud a judgment about the quality of their state
of mind associated with each of their recognitions. A recollection judgment means
that the subject based his/her recognition on the recollection of a specic event and
was re-experiencing it with details and the source of acquisition (e.g., I can mentally
view the train station in the town). A familiarity judgment corresponds to a feeling
of familiarity in the absence of any such recollection (e.g., I know the train station
was at the beginning of the town, but I cannot view it mentally). A guess judgment indicates that a subject was not sure of the response (e.g., I assume that there
was a train station). This category was added so that Know (K) responses would
not depend on the degree of uncertainty (Mntyl, 1993). To take independent
scores into account, we calculated the recollection (autonoetic consciousness) and
familiarity (noetic consciousness) scores as the mean with the following formula:
Recollection = R/n (n = maximum number of correct recognitions, i.e., = 8 by category) and Familiarity = (K/n)/(1 recollection score) recommended by Yonelinas,
Kroll, Dobbins, Lazzara, and Knight, 1998).
2.4.5. Delayed recall test
The delayed recall task was identical to the immediate recall task, with the
exception that it was administered 20 min after immersion. The instructions and
scores were documented similarly to those of the immediate recall task (please see
above). There was no delayed recognition test.
3. Results
The levels of education and gender were included as controlled
variables in all of the statistical analyses.
3.1. Neuropsychological assessment
ANCOVAs were conducted on each score to test for differences
between populations on neuropsychological tests (see Table 1 for a
summary of the results). As classically observed, the MMSE scores of
AD patients were less than those of aMCI patients, and those of aMCI
patients were less than those of the control group. Importantly,
the reverse pattern was observed for CDS scores. Furthermore, AD
patients were impaired on the Mill Hill, TMTA, and TMTB-A tests
Fig. 2. Recall performance (raw score) for what score according to population (older
adults, aMCI patients and AD patients) and exploration (active and passive).
597
Fig. 3. Recall performance (raw score) for detail score according to population and
exploration.
Fig. 5. Recall performance (raw score) for binding score according to population,
exploration and recall.
healthy older, aMCI and AD participants respectively). No significant differences appeared between the aMCI and healthy groups.
In addition, an interaction between population and recall (F(2,
47) = 6.5, p < .01, 2p = .22) showed that only AD (means of .8 and
1.6 for immediate and delayed recalls respectively) and aMCI
patients (means of 4.2 and 3.3) presented a difference between
immediate and delayed recalls (p < .001). Finally, a triple interaction (F(2, 46) = 6.5, p < .01, 2p = .23) indicated that aMCI patients
(p < .01) (means of 4.8 and 3.5 for active and passive exploration
respectively) and the control group (p < .01) (means of 4.7 and 3.6)
performed better after an active exploration but only at immediate
recall.
An effect of population on the egocentric where score (F(2,
47) = 38.7, p < .001, 2p = .63), was observed, indicating that AD
patients (mean of 1.1) (p < .001) and aMCI patients (mean of 3.2)
(p < .01) recalls were decient compared with healthy older adults
(mean of 4.3). Again, aMCI patients presented a smaller decit than
AD patients (p < .001). No signicant interaction was found.
An effect of population on the allocentric where score (F(2,
47) = 28.4, p < .001, 2p = .55), was observed (see Fig. 4), indicating
that AD (p < .001) and aMCI patients (p < .001) recalled signicantly
less allocentric spatial information than healthy older adults, with
aMCI patients exhibiting less impairment than AD patients (p < .01).
In addition, an effect of exploration (F(1, 47) = 5.3, p < .05, 2p = .10)
showed that active exploration led to lesser impairment in allocentric recall for all groups. No signicant interaction was found.
An effect of population on the binding performance (F(2,
47) = 39.4, p < .001, 2p = .63), was observed (see Fig. 5), indicating
that AD patients (p < .001) linked together less information than
older adults and aMCI patients (p < .001). The effect of population
interacted with recall (F(1, 47) = 3.5, p < .05, 2p = .13), indicating
that the aMCI patients delayed recall, but not immediate recall,
Fig. 4. Recall performance (raw score) for allocentric where score according to
population and exploration.
598
Table 2
Synthesis of signicant results (effects of population, exploration and recall) observing in the VR episodic memory assessment.
Effects
Population
Exploration
What
Details
When
Recall
Where egocentric
Where allocentric
Binding
Recognition
AD: Alzheimer disease; aMCI: amnesic mild cognitive impairment; OA: older adult.
Table 3
Intercorrelations between the VR test and CDS and between the Grober and Buchke memory test and CDS. Only signicant correlations are presented (p < .05).
Recall
What
CDS
OA
aMCI
AD
Recognition
Details
When
Ego where
Allo where
Binding
.50
.71
.81
What
Where
.52
.82
.81
Recall
Recognition
.59
.67
.56
599
600
601
Lalanne, J., Grolleau, P., & Piolino, P. (2010). Self-reference effect and episodic memory in normal aging and Alzheimers disease: Myth or reality? Psychologie &
Neuropsychiatrie du Vieillissement, 8, 277294.
Lacz, J., Vlcek, K., Vyhnlek, M., Vajnerov, O., Ort, M., Holmerov, I., et al. (2009).
Spatial navigation testing discriminates two types of amnestic mild cognitive
impairment. Behavioural Brain Research, 202, 252259.
Lekeu, F., Van der Linden, M., Moonen, G., & Salmon, E. (2002). Exploring the effect
of action familiarity on SPTs recall performance in Alzheimers disease. Journal
of Clinical Experimental Neuropsychology, 24, 10571069.
Lenzi, D., Serra, L., Perri, R., Pantano, P., Lenzi, G. L., Paulesu, E., et al. (2011). Single domain amnestic MCI: A multiple cognitive domains fMRI investigation.
Neurobiology of Aging, 32, 15421557.
Lezak, M. D., Howieson, D. B., & Loring, D. W. (2004). Neuropsychological assessment
(4th ed.). Oxford, England: Oxford University Press.
Lipinska, B., & Backman, L. (1997). Encoding-retrieval interactions in mild
Alzheimers disease: The role of access to categorical information. Brain and
Cognition, 34, 274286.
Luo, L., & Craik, F. I. M. (2008). Aging and memory: A cognitive approach. Canadian
Journal of Psychiatry, 53, 346353.
Mntyl, T. (1993). Knowing but not remembering: Adult age differences in recollective experience. Memory & Cognition, 21, 379388.
Martinelli, P., Sperduti, M., & Piolino, P. (in press). Neural substrates of the
self-memory system: New insights from a meta-analysis. Human Brain
Mapping, doi:10.1002/hbm.22008.
Mayes, A. R. (1988). Human organic memory disorders. Cambridge: Cambridge University Press.
McKahnn, G., Drachman, D., Folstein, M., Katzman, R., Price, D., & Stadlan, E. M.
(1984). Clinical diagnosis of Alzheimers disease: Report of the NINCDS-ADRDA
work group under the auspices of the Department of Health and Human Services
Task Force on Alzheimers disease. Neurology, 34, 934939.
McNair, D., & Kahn, R. (1983). Self-assessment of cognitive decits. In T. Crook, S. Ferris, & R. Bartus (Eds.), Assessment in geriatric psychopharmacology (pp. 137143).
New Canaan, CT: Powley.
Naveh-Benjamin, M., Craik, F. I. M., & Ben-Shaul, L. (2002). Age-related differences in
cued recall: Effects of support at encoding and retrieval. Aging, Neuropsychology,
and Cognition, 9, 276287.
Nilsson, L. G., Nyberg, L., Klingberg, T., berg, C., Persson, J., & Roland, P. (2000).
Activity in motor areas while remembering action events. NeuroReport, 11,
21992201.
Nyberg, L., Petersson, K. M., Nilsson, L. G., Sandblom, J., Aberg, C., & Ingvar, M.
(2001). Reactivation of motor brain areas during explicit memory for actions.
NeuroImage, 14, 521528.
Park, D. C., Puglisi, J. T., & Smith, A. D. (1986). Memory for pictures: Does an agerelated decline exist? Psychology and Aging, 1, 1117.
Park, D. C., Smith, A. D., Morell, R. W., Puglisi, J. T., & Dudley, W. N. (1990). Effects of
contextual integration on recall of pictures by older adults. Journal of Gerontology: Psychological Sciences, 45, 5257.
Pennartz, C. M., Ito, R., Verschure, P. F., Battaglia, F. P., & Robbins, T. W. (2011). The
hippocampal-striatal axis in learning, prediction and goal-directed behavior.
Trends in Neurosciences, 34, 548559.
Perani, D., Bressi, S., Cappa, S. F., Vallar, G., Alberoni, M., Grassi, F., et al. (1993).
Evidence of multiple memory systems in the human brain. A [18F] FDG PET
metabolic study. Brain, 116, 903919.
Perri, R., Carlesimo, G. A., Serra, L., & Caltagirone, C. (2005). Early diagnosis group of
the Italian interdisciplinary network on Alzheimers disease. Characterisation of
memory prole in subjects with mild cognitive impairment. Journal of Clinical
and Experimental Neuropsychology, 27, 10331055.
Perri, R., Serra, L., Carlesimo, G. A., & Caltagirone, C. (2007). Italian interdisciplinary
network on Alzheimers disease, early diagnosis group. Neuropsychology, 21,
549558.
Petersen, R. C., Doody, R., Kurz, A., Mohs, R. C., Morris, J. C., Rabins, P. V., et al.
(2001). Current concepts in mild cognitive impairment. Archives of Neurology,
58, 19851992.
Petersen, R. C., Smith, G. E., Waring, S. C., Ivnik, R. J., Tangalos, E. G., & Kokmen,
E. (1999). Mild cognitive impairment: Clinical characterization and outcome.
Archives of Neurology, 56, 303308.
Piolino, P., Desgranges, B., & Eustache, F. (2009). Episodic autobiographical memory over the course of time: Cognitive, neuropsychological and neuroimaging
ndings. Neuropsychologia, 47, 23142329.
Plancher, G., Guyard, A., Nicolas, S., & Piolino, P. (2009). Mechanisms underlying
the production of false memories for famous peoples names in aging and
Alzheimers disease. Neuropsychologia, 47, 25272536.
Plancher, G., Gyselinck, V., Nicolas, S., & Piolino, P. (2010). Age effect on components
of episodic memory and feature binding: A virtual reality study. Neuropsychology, 24, 379390.
Plancher, G., Nicolas, S., & Piolino, P. (2008). Contribution of virtual reality for neuropsychology of memory: Study in ageing. Psychologie et NeuroPsychiatrie du
vieillissement, 6, 722.
Putzke, J. D., Rickert, E. J., Duke, L. W., Marson, D., & Harrell, L. (2000). Differential automatic processing decits in early stage Alzheimers disease. Aging,
Neuropsychology and Cognition, 7, 112118.
Rabinowitz, J. C., & Craik, F. I. M. (1986). Specic enhancement effects
associated with word generation. Journal of Memory and Language, 25,
226237.
602
Risacher, S. L., Saykin, A. J., West, J. D., Shen, L., Firpi, H. A., & McDonald, B. C. (2009).
Baseline MRI predictors of conversion from MCI to probable AD in the ADNI
cohort. Current Alzheimer Research, 6, 347361.
Rsler, A., Seifritz, E., Kruchi, K., Spoerl, D., Brokuslaus, I., Proserpi, S-M., et al.
(2002). Skill learning in patients with moderate Alzheimers disease: A prospective pilot-study of waltz-lessons. International Journal of Geriatric Psychiatry, 17,
11551156.
Ruby, P., Collette, F., DArgembeau, A. D., Pters, F., Degueldre, C., Balteau, E.,
et al. (2009). Perspective taking to assess self-personality: Whats modied in
Alzheimers disease? Neurobiology of Aging, 30, 16371651.
Salmon, D. P., & Bondi, M. W. (2009). Neuropsychological assessment of dementia.
Annual Review of Psychology, 60, 257282.
Schacter, D. L., Israel, L., & Racine, C. (1999). Suppressing false recognition in younger
and older adults: The distinctiveness heuristic. Journal of Memory and Language,
40, 124.
Schultheis, M. T., Himelstein, J., & Rizzo, A. A. (2002). Virtual reality and neuropsychology: Upgrading the current tools. Journal of Head Trauma Rehabilitation, 17,
379394.
Serra, L., Bozzali, M., Cercignani, M., Perri, R., Fadda, L., Caltagirone, C., et al. (2010).
Recollection and familiarity in amnesic mild cognitive impairment. Neuropsychology, 24, 316326.
Slotnick, S. D. (2010). Does the hippocampus mediate objective binding or subjective
remembering? NeuroImage, 49, 17691776.
Spaan, P. E., Raaijmakers, J. G., & Jonker, C. (2003). Alzheimers disease versus normal ageing: A review of the efciency of clinical and experimental memory
measures. Journal of Clinical Experimental Neuropsychology, 25, 216233.
Squire, L. R. (2004). Memory systems of the brain: A brief history and current perspective. Neurobiology of Learning and Memory, 82, 171177.
Stroop, J. R. (1935). Studies of interference in serial verbal reactions. Journal of Experimental Psychology, 18, 643662.
Swainson, R., Hodges, J. R., Galton, C. J., Semple, J., Michael, A., Dunn, B. D., et al. (2001).
Early detection and differential diagnosis of Alzheimers disease and depression
with neuropsychological tasks. Dementia and Geriatric Cognitive Disorders, 12,
265280.
Troyer, A. K., Murphy, K. J., Anderson, N. D., Hayman-Abello, B. A., Craik, F. I., &
Moscovitch, M. (2008). Item and associative memory in amnestic mild cognitive
impairment: Performance on standardized memory tests. Neuropsychology, 22,
1016.
Tulving, E. (1983). Elements of episodic memory. New York: Oxford University Press.
Tulving, E. (1985). Memory and consciousness. Canadian Psychologist, 26, 112.
Tulving, E. (2002). Episodic memory: From mind to brain. Annual Review of Psychology, 53, 125.
Tulving, E., & Thomson, D. M. (1973). Encoding specicity and retrieval processes in
semantic memory. Psychological Review, 80, 352373.
Van Halteren-van Tilborg, I. A., Scherder, E. J., & Hulstijn, W. (2007). Motor-skill
learning in Alzheimers disease: A review with an eye to the clinical practice.
Neuropsychology Review, 3, 203212.
Wechsler, D. (2001). Wechsler Adult Intelligence Scale Third Edition (WAIS III). Paris
(French version): EAP.
Weniger, G., Ruhleder, M., Lange, C., Wolf, S., & Irle, E. (2011). Egocentric and allocentric memory as assessed by virtual reality in individuals with amnestic mild
cognitive impairment. Neuropsychologia, 49, 518527.
Westerberg, C. E., Paller, K. E., Holdstock, J. S., Mayes, A. R., & Reber, P. J. (2006).
When memory does not fail: Familiarity-based recognition in mild cognitive
impairment and Alzheimers disease. Neuropsychology, 20, 193205.
Widmann, C. N., Beinhoff, U., & Riepe, M. W. (2012). Everyday memory decits in
very mild Alzheimers disease. Neurobiology of Aging, 33, 297303.
Wojtasik, V., Olivier, C., Lekeu, F., Quittre, A., Adam, S., & Salmon, E. (2010). A grid
for a precise analysis of daily activities. Neuropsychological Rehabilitation, 20,
120136.
Wolf, H., Jelic, V., Gertz, H. J., Nordberg, A., Julin, P., & Wahlund, L. O. (2003). A critical discussion of the role of neuroimaging in mild cognitive impairment. Acta
Neurologica Scandinavica, 107, 5276.
Yesavage, J. A. (1988). Geriatric depression scale. Psychopharmacology Bulletin, 24,
709711.
Yonelinas, A. P. (2002). The nature of recollection and familiarity: A review of 30
years of research. Journal of Memory and Language, 46, 441517.
Yonelinas, A. P., Aly, M., Wang, W. C., & Koen, J. D. (2010). Recollection and familiarity: Examining controversial assumptions and new directions. Hippocampus,
20, 11781194.
Yonelinas, A. P., & Jacoby, L. L. (1995). The relation between remembering and knowing as bases for recognition: Effects of size congruency. Journal of Memory and
Language, 34, 622643.
Yonelinas, A. P., Kroll, N. E., Dobbins, I., Lazzara, M., & Knight, R. T. (1998). Recollection
and familiarity decits in amnesia: Convergence of remember-know, process
dissociation, and receiver operating characteristic data. Neuropsychology, 12,
323339.
Zakzanis, K. K., Quintin, G., Graham, S. J., & Mraz, R. (2009). Age and dementia related
differences in spatial navigation within an immersive virtual environment. Medical Science Monitor: International Medical Journal of Experimental and Clinical
Research, 15, 140150.
Zanetti, O., Zanieri, G., Di Giovanni, G., De Vreese, L. P., Pezzini, A., Metitieri, T., et al.
(2001). Effectiveness of procedural memory stimulation in mild Alzheimers disease patients: A controlled study. Neuropsychological Rehabilitation, 11, 263272.