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Virtual reality as a tool for assessing episodic memory

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The principal attraction of virtual reality is its potential to create experiments close to daily life with perfect experimental control. We performed an experiment in a virtual town in order to develop a better episodic memory assessment. We tested all components of episodic memory. Young and elderly adults participated in the virtual test: they were either in an active exploration or in a passive exploration of the town. The results showed that older persons recalled the spatiotemporal context and the details of the events in a lower proportion compared to younger ones regardless of the active or passive condition. But no difference was found between active and passive exploration in measures of episodic memory. Finally, correlations mainly appeared between memory complaint and virtual scores, but not with a classical verbal episodic memory test. The virtual test seems to allow a better assessment of episodic memory compared to classical studies, especially because of its components of spatiotemporal memory assessment. In conclusion, virtual reality appears to offer the possibility of developing neuropsychological tools closer to the daily life of patients.
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Assessing Truly Episodic Memory with a Virtual Environment: Effect of
Aging, Encoding and Sensory-motor Implication
Plancher, G.
gaen.plancher@univ-paris5.fr
Nicolas, S.
serge.nicolas@univ-paris5.fr
Piolino, P.
pascale.piolino@univ-paris5.fr
Laboratory of Psychology and Cognitive Neurosciences, CNRS, University Paris Descartes.
Research group Memory and Learning
71 avenue Edouard Vaillant, 92774 Boulogne-Billancourt, France
Abstract
Episodic memory is rarely studied in a frame closed
to its complete definition. We studied episodic
memory for young and older adults in active and
passive exploration and in intentional versus
incidental encoding in a virtual environment. The
active participants drove a car through a virtual
town whereas passive participants were only
passengers. After the exploration, subjects performed
memory free recall test which assessed all
components of episodic memory; the verbal
components: the what, the when, the where, the
details; the visuo-spatial component; and they took a
recognition test. Our findings showed no difference
between age groups in incidental encoding
regardless of the components. By contrast, young
adults were better in intentional encoding for target,
verbal-spatial and for temporal information; but not
for the visuo-spatial score. Old adults showed better
recognitions than young. In addition, we found no
effect of enactment on episodic memory. Virtual
reality appears as an interesting tool for study
episodic memory.
1. Introduction
According to Tulving [11], episodic memory allows
conscious recollection of personal events, together
with their phenomenological and spatio-temporal
encoding contexts. The constructive memory
framework postulates that the features of an episode
are linked together at encoding to form a coherent
representation. The recollection of one element of the
episode allows the recollection of the other elements
[5]. Yet, the majority of episodic memory studies are
far from what we experience in daily life and far
from its definition [11]. In order to investigate all
components of episodic memory a context where we
can assess the memories of what, when, where and
details of an event is needed. Virtual reality (VR) can
provide a fully controlled experimental situation in a
rich context and it allows active interactions between
the subject and the stimuli.
Difficulties with episodic memory are among the
most frequent cognitive deficits in normal aging.
Aging deficit is more important for the memory of
the spatio-temporal context than for the memory of
factual information [8]. For example, older adults are
less likely to correctly remember contextual features
of events, such as their colour or location [3].
The capacity for retrieve an event can depend on
the quality and on the strength of associations created
between central information and contextual features
[7]. The motor activity and the intentional encoding
can reinforce association between features of an
event.
The fact to be active rather than passive in an
event enriched the context of episodic memory. It has
been shown that performance in episodic memory is
enhanced by this activity [12]. This effect is usually
attributed to the good item-specific information
provided by enactment. It was shown also for spatial
memory in virtual environment [23,24]. Moreover, it
was observed that older adults have a deficit for
spatial memory in virtual environments [6]. Active
compare to passive exploration in virtual
environment would enhance episodic memory of
participants.
Another factor which contributes to a richer
memory trace is the intentionality of learning.
Participants show better memory performance when
they learn intentionally the items, i.e. they try to
memorize it, than when they learn the items
incidentally, i.e. they are not informed that their
memory will be tested [9]. Intentionality should
enhance episodic memory.
In the present study we were interested on the
memory of different components of episodic memory
for young and older adults in a virtual environment.
We compared their performances in active and
passive exploration and in intentional versus
incidental encoding.
2. Methods
2.1. Participants
113 undergraduate psychology students from Paris
Descartes University (67 female and 33 male; Mage =
21.57; SD = 2.99) and 45 older adults participated
voluntarily (Mage=59.42; SD=9.85). They were
randomly assigned to one of the four conditions
resulting of the crossing between active/passive
sensory-motor implication and intentional/incidental
encoding. Inclusion of subjects was based on absence
of neurological or psychiatric medical history and
signs of depression. No medication known to impair
memory was allowed. The groups did not differ on
verbal abilities according to the 44-item Mill Hill
test. Old adults shown a normal score at the MMSE
and had a socio-cultural level equal to young adults.
2.2. Materials
2.2.1. The Virtual Apparatus
The virtual apparatus was composed of a computer
generated 3-D model of a created environment. The
environment was built with Virtools Dev 3.0
software (www.virtools.com). The environment was
run on a PC laptop computer and explored using a
steering wheel, a gas pedal and a brake pedal. It was
projected with a video projector onto a screen (85 cm
high and 110 cm long).
2.2.2. The virtual environment (VE)
A town based on photos of Paris, France, was built.
In the town, there was one possible route composed
by nine turns. Nine specific areas with their context
composed the town’s elements. The interconnected
specific areas were, in this order: the area of tall
buildings, the shops, the roadblocks, the town hall,
the restaurants, the car accident, the train station, the
arcade buildings, the old red buildings and the park.
One of these areas is a car accident scene; in this
specific event, two cars crashed into one another, a
horn was heard and black smoke appeared. Buildings
connected each area with another. People, garbage
containers, barriers, trees, billboards and motionless
cars were the context of the town. Each area was
composed of some contextual elements. For example,
in front the train station: a car accident occurred, a
woman walked, a billboard and trees were presented
(see Figure 1.)
Figure 1. Example of a virtual town’s view
2.3. Procedure
Participants were tested individually. They were
seated on a comfortable chair. The VE was projected
on the wall, 150cm ahead of subjects. In order to
match the visual stimulation between active and
passive participants, we recorded the navigation of
all active participants. Each passive participant saw
the record of one active participant.
If the subjects were in an incidental encoding,
they were told to drive through the virtual town and
pay attention to the town. If the participants were in
an intentional encoding, we asked participants to try
to remember the most elements they saw in the town
and the itinerary of the driver in order to recall them
at the end of the presentation.
2.3.1 Exploration of the virtual environment
Active condition
The participants manipulated a steering wheel, a gas
pedal and a brake pedal to move around in the virtual
town. Before the immersion within the town, the
participants trained in an empty environment until
they were comfortable. We notified the subjects that
they did not have to drive too fast. Then, the active
participants were immerged in the virtual town. Only
one trip was possible, the participants could not stop
and could not turn back. Navigation stopped at the
end of the route, approximately two minutes after the
start.
Passive condition
The participants were immerged directly in the
virtual town. We told subjects they were sitting on
the passenger side. The passive participants saw the
recorded route of the active participants and in order
to control the attention in our experimental situations;
we told passive subjects to pay attention to the
driving and to the itinerary of the driver.
2.3.2 Memory tests
The free recall test
What recall
This recall was scored out of a possible 31 elements.
Participants had “to recall all the elements presented
in the town”. The maximum was 9 central elements
(e.g. “the train station”) and 22 minor elements (e.g.
“the girl”).
Where recall
This recall was divided in two different parts: the
verbal where recall (where 1) and the visuo-spatial
where recall (where 2). For the verbal where, the
subjects had to remember spatial information
concerning the element, if it was “in front of us”, “on
their left” or “on their right”. This recall was scored
out of a possible 31 verbal where. For the visuo-
spatial where, the subject had to draw the map of the
town and localise the elements on the map. The map
score was computed with the number of correct turns,
the maximum score was 9 turns. Participants had also
to recall the locations of elements on a correct map;
the maximum score was 31 correct locations. Thus,
the maximum of visuo-spatial where score was 40
correct recalls.
When recall
31 temporal recalls were possible. The participants
had to recall when the element occurred, if it was “at
the beginning”, “at the middle” or “at the end of the
town”.
Details recall
22 details recalls were possible. The subjects had to
recall the details of the element they remembered
(e.g. one of the cars was blue).
The recognition test
A recognition test was presented after the recall. The
subjects had to choose the item presented in the town
among three different items. It was composed of 10
questions concerning the elements and their locations
in the town. For example, “who was presented in
front of the accident?”
3. Results
Analyses of variance (ANOVA) were conducted on
the data recorded from the different components of
the episodic memory: the what, verbal where, visuo-
spatial where, when and details and on the correct
recognitions. The encoding, the sensory-motor
implication and the age were included in the
ANOVA as between factors.
A main effect of the encoding was found, the
intentional encoding compared to the incidental
encoding leads to a better recall of what (F (1,152) =
8.04; p < 0.01), of verbal where (F (1,152) = 9.29; p
< 0.01), of visuo-spatial where (F (1,152) = 9.93; p<
0.001), of when (F (1,152) = 9.31; p < 0.01), of the
details (F (1,152) = 4.35; p < 0.05). Learning
information intentionally leads to better memory of
all components of episodic memory.
Second, the sensory-motor implication had no
effect neither on the what (F (1,152) < 1), the verbal
where (F (1,152) = 1.24; n.s.), the visuo-spatial
where (F (1,152) = 1.12; n.s.) the when (F (1,152) =
1.77, n.s.), the details (F (1,152) < 1) recall scores
nor on the recognition test (F (1,152) = 1, n.s.).
Activity did not enhance the different components of
episodic memory in a VE.
Moreover, we found a main effect of the age,
young adult were better than old adults on verbal
where recall (F (1,152) = 65.94, p < 0.001), on visuo-
spatial where recall (F (1,152) = 4.8, p < 0.05), on
when recall (F (1,152) = 14.6, p < 0.001), on details
recall (F (1,152) = 7.9, p < 0.01). No effect of the age
was found on the what recall (F (1,152) = 2.28, n.s.).
Though, old adults showed a higher score on the
recognition test (F (1,152) = 11.88, p < 0.001).
In addition, we found interactions between the
encoding and the age (See Figure 2.). The young
adults were better only in intentional encoding for the
what (F (1,112) = 6.81, p < 0.01), the verbal where (F
(1,112) = 13.59, p < 0.001), the when (F (1,112) =
13.08, p < 0.001). Moreover, old adults were better
than young only in incidental encoding for the
recognition score (F(1,112) = 4.91, p < 0.05). No
interaction was observed for the visuo-spatial where
score (F (1,112) = 2.65, n.s.) and for the details score
(F(1,112) < 1).
0
2
4
6
8
10
12
14
16
What Verbal Where Visuo-spatial
Where When Details Recognition
young adults intentional
young adults incidental
old adults intentional
old adults incidental
Figure 2. Recall of various episodic memory components according to the age and the encoding.
4. Discussion
It was the aim of the current study to examine
the effects of aging, encoding and sensory-motor
implication on various components of episodic
memory. The results clearly indicate age-related
decline on memory of the spatio-temporal context
and of details unlike factual recall. These findings are
in agreement with previous results showing that
contextual memory decline with aging [3,8].
However an interaction was found between the
age and the encoding: no difference appears between
ages in incidental encoding. By contrast young adults
were better in intentional encoding for target (what)
information, for verbal spatial information (where 1)
and for temporal information (when) than old adults.
In addition what was surprising is the superiority of
older adults compare to young in incidental encoding
for correct recognitions. An explanation for this
effect could be that this test was especially about the
accident and it is possible that older adults were more
attentive to this emotional event. Thus they
recognized stimuli better than young adults who were
more used to with video games and their emotional
stimulations. But old adults were better for
recognitions only in incidental encoding. The results
showing that older adults did not benefit from
intentional encoding suggest that age-related deficits
in memory may come from the incapacity for old
adult to develop encoding strategies. However, this
interaction was not observed for the visuo-spatial
score (where 2), i.e. the old adults benefit of
intentional encoding for this score. So this finding
leads to believe that intentional encoding is most
likely to be effective for older adults when
information is visuo-spatial rather than verbal.
Therefore, for young adults encoding was
advantageous for all scores even for visuo-spatial
score which is more implicit and automatic. These
data confirms previous studies showing that spatial
memory is function to intention to learn for young
and old adults [10]. Though, this result is evidence
against the total automaticity of the encoding of
spatial location information [4].
Moreover, we observed no effect of the sensory-
motor implication on the recall of elements and on
their spatio-temporal context. These results are
paradoxical with studies using the enactment
paradigm showing that action enhances memory
[1,2]. But in previous studies, the motor activity was
composed of more movements than in our study. In
our study, visuo-motor interaction and motor control
were not that such as important. We can conclude
that memory of these components do not require
visuo-motor coupling in a VE, passive exploration is
sufficient to this cognitive ability. We propose that
no effect of active exploration on episodic memory
occurred on episodic verbal scores because the
subject verbalized what he perceived and then
recalled verbal information he inferred from
perception rather than the perceived information. In
addition, we supposed that no effect was observed on
visuo-spatial score because our motor activity is very
weak, no comparable with previous studies showing
a sensory-motor effect. It should be interesting to
study the effect of enaction on episodic memory with
a bigger action. Last, VE appears to be an appropriate
tool to study evolution of truly episodic memory for
young and older adults.
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Full-text available
Chez l'homme, la mémoire épisodique est l'aptitude cognitive qui lui permet de récupérer une expérience passée vécue, ou épisode, selon un état de conscience spécifique. La particularité de ce système de mémoire est la construction de liens entre les dimensions contextuelles constitutif de l'épisode mnésique : l'évènement « Quoi ? », le moment « Quand ? », et l'endroit « Où ? ». Les études classiques de la mémoire épisodique indiquent que ces dimensions sont traitées et intégrées dans les structures corticales comprenant principalement le lobe temporal médian et le cortex préfrontal. Des études récentes de la mémoire en IRMf faisant usage de matériaux expérimentaux plus naturelles et écologiques ont ouvert la perspective de réseaux corticaux sous-jacents de la mémoire épisodique s'étendant au-delà de ces structures. En effet, ces études suggèrent l'idée que le lobe pariétal joue un rôle important dans la constitution d'un épisode mnésique au contexte enrichi. Cependant les mécanismes et structures relatives aux traitements des caractéristiques contextuelles d'un évènement restent débattues, et les interactions induites entre les différentes dimensions contextuelles d'un épisode mnésique, lors de son rappel, sont mal compris. Cette thèse présente 3 objectifs principaux : 1) développer de nouveaux protocoles expérimentaux pour étudier la mémoire des épisodes mnésiques encodés dans des situations comprenant un contexte riche et écologique ; 2) évaluer l'influence du contexte temporel et spatial sur la performance de rappel des épisodes encodés dans ces situations hautement écologiques ; et 3) élucider les structures corticales sous-jacentes aux traitements de ces dimensions contextuelles. Avec ces objectifs en vue, j'ai développé des protocoles d'études faisant usage de films, de réalité virtuelle et d'une application mobile géolocalisée lors de la phase d'encodage. J'ai étudié les performances de rappel comportementale, et sous IRMf, par le moyen de 2 tâches : une tâche hybride Rappel/Familier et de Mémoire source ; et une tâche de jugement de l'ordre temporel. Mes résultats comportementaux de la première tâche démontrent que le rappel correct et confiant de l'endroit « Où ? » et du moment « Quand ? » prédit la probabilité du choix rappel, et non familier, du « Quoi ? » ; et cela, dans l'ensemble des modalités d'encodage. L'étude IRMf a mis en évidence une activité accrue du Précuneus concomitante. Dans la tâche de jugement de l'ordre temporel j'ai observé une modulation des temps de réaction et de l'activité du Précuneus en fonction de la distance temporelle entre les épisodes pendant la phase l'encodage. Plus important, à travers les études, j'ai constaté que ces effets comportementaux et d'imagerie sont modulés en fonction d'autres facteurs contextuels associés aux épisodes écologiques (p. ex. facteurs spatiaux, contenu sémantique, modalité d'encodage), ce qui démontre que l'information épisodique traitée par le Précuneus dépasse les dimensions classiques "quoi, où, quand". Ces résultats mettent en avant l'implication du lobe pariétal médian pour le rappel des épisodes mnésiques écologiques et suggérant son implication dans le rappel conscient et subjectif d'un épisode. J'interprète ces résultats à la lumière des théories reconstructives de la mémoire épisodique et je propose que le Précuneus soit impliqué dans l'intégration multidimensionnelle des épisodes mnésiques enrichis selon une perspective subjective/personnelle accrue. Plus généralement, mes études appuient l'importance d'étudier la cognition humaine dans son milieu écologique, en démontrant ici le rôle crucial du Précuneus, qui est une structure éloignée du réseau classique temporo-frontale de la mémoire épisodique
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