In the last decade, embodiment has dramatically influenced our conception of cognition.
In this new frame, episodic memory, and particularly memory decline have been reinterpreted.
Interventions supporting memory in the aging population address the connection between
mind and body. Here, we discuss the use of Virtual Reality (VR) as an innovative tool
to support episodic memory in older adults.
The embodied nature of episodic memory and its implications for aging
Traditional cognitive models of human mind describe it as processing abstract symbols
and following predefined formal rules (Fodor, 1975, 1983).
An alternative view, the embodied cognition approach, claims however that the mind
is inherently embodied: this is to say that perceptual and motor systems influence
the way we construct concepts, make inferences, and use language (Barsalou, 2008;
Shapiro, 2011). Empirical evidence supports this claim in different cognitive domains:
in language comprehension (Hauk et al., 2004; Tettamanti et al., 2005; Repetto et
al., 2013, 2015b; Repetto, 2014), second language learning (Macedonia et al., 2011;
Repetto et al., 2015a; Macedonia and Repetto, 2016), and also in memory (Pezzulo et
al., 2010; van Dam et al., 2013; Downing-Doucet and Guérard, 2014; Bochynska and Laeng,
2015; Lagacé and Guérard, 2015). Specifically, it has been argued that the ability
to encode and retrieve information is constrained by the actions we can perform upon
it and by the limitations/opportunities provided by our bodies (Glenberg, 1997). The
embodied nature of memory appears particularly evident for episodic memories. They
consist of past events with reference to the individuals themselves as participants
of those events (Tulving, 2001, 2002) and linked to a place and a particular time.
According to Tulving (2001), the essence of episodic retrieval is the “autonoetic
consciousness,” namely the subjective and conscious experience of mentally reliving
a personal past event. This includes “all the attendant visual, kinesthetic, and spatial
impressions” (Wilson, 2002 p.633).
It has been argued that the ontogeny of episodic memory is strictly connected with
the onset of locomotion during infancy, and related to the maturation of the hippocampus
(Glenberg and Hayes, 2016). This brain structure, together with the entorhinal cortex,
contains different kinds of cells dedicated to different tasks. Hippocampal place
cells code location (Ekstrom et al., 2003). Head-direction cells provide a viewing
direction on the retrieved contents (Taube, 1998) and allow the generation of an egocentrically
coherent representation in medial parietal areas. Grid cells in the entorhinal cortex
support the process of updating a viewpoint in relation to self-motion signals (Boccara
et al., 2010). Glenberg and Hayes (2016) specifically proposed that the alignment
of hippocampal place cells and grid cells related to environmental cues triggers the
encoding of space in which personal events are experienced. Embodied navigation and
memory are thus strictly connected (Leutgeb et al., 2005; Buzsáki and Moser, 2013).
Miller et al. (2013) developed an hybrid memory test assessing both spatial and episodic
memory for a group of epileptic patients implanted with depth electrodes. The test
was implemented in a virtual reality environment. In the encoding phase, patients
were asked to drive in a virtual city and to deliver different items to stores; in
the retrieval phase, patients were prompted to verbally recall the items delivered
during navigation. Miller and colleagues found that place cells that fired at a specific
location during virtual navigation were also activated during subsequent recall of
the item associated to that location. This indicates that activity was reinstated
during retrieval in episodic memory.
The embodied approach of memory also accounts for the decline of episodic memory described
during aging (Koen and Yonelinas, 2014). Here, the critical element is the reduction
of locomotion observed in older individuals. The decrease of locomotion results in
the reduction of the opportunities for the hippocampal place cells and grid cells
to be tuned with the environment (Glenberg and Hayes, 2016). It stands to reason that,
in order to enhance episodic memory in older adults, trainings procedures should target
self-locomotion and navigation tasks. To this extent, Virtual Reality systems (VR)
could be employed as training tool.
Virtual reality as a tool to improve episodic memory in the aging population
Virtual reality allows users to create, explore and interact within environments that
are perceived as near to reality. Typically, users entering a VR lab feel as being
a part of this world and behave as if they were in the real world (Riva and Mantovani,
2012; Riva et al., 2014). Specifically, even if users do not always move their bodies
in the real space, users have the subjective perception of being “in action.” The
effect of a virtual action on cognitive processing has been demonstrated by Repetto
et al. (2015b) who have found that performing a virtual movement with a limb (i.e.,
virtual run—performed with the legs/feet) speeds up the comprehension of verbs that
describe actions performed with the same limb (to kick, performed with legs/feet).
On this base, VR can be used to support episodic memory, in particular in elderly
(Morganti et al., 2013).
Three main features that VR implements may have an impact on episodic memory in elderly:
First VR allows to experience from an egocentric point of view. This feature places
VR in an intermediate position between mere action observation (such as in a video)
and real action execution (Serino et al., 2015), with an important rebound on brain
activity (Serino et al., 2014). In a fMRI study, Strafella and Paus (2000) have demonstrated
that cortical excitability is modified by the observation of movements performed by
others. Futhermore, this modulation can be enhanced if the orientation of the movement
is egocentric (Maeda et al., 2002). In a recent experiment, Bergouignan et al. (2014)
tested the egocentric point of view in relation to encoding and retrieving real-life
events. Participants seating in front of a “professor” had a social interaction with
him. They saw a real scene filmed and projected through a head-mounted display (HMD)
connected to cameras in different locations. The first camera was located exactly
over the participants' head, so that participants looked at the scene from the same
perspective as without the HMDs. The second camera was located 2 m in front of the
participants and rotated 180° to face them. This experimental manipulation yielded
two different subjective frames of reference. In the former, the sense of bodily self
was located inside of the physical body (in-body condition). In the latter the sense
of bodily self was located outside the physical body (out-of-body condition). To induce
the illusion of being in one of these two locations, they received a visuo-tactile
stimulation on their chest with a rod, synchronous with the scene projected to HMD.
After a week, participants' episodic memory of these life events was assessed. Results
revealed a poorer recollection for life events encoded in the out-of-body condition.
Furthermore, findings indicated that the retrieval of these life events was associated
with activity changes in the hippocampus. Considering these findings, VR allowing
an egocentric encoding and retrieval, could be a valid training tool for episodic
memory.
Second, VR allows active navigation while the user actively explores the environment
by manipulating keyboards, joysticks, or controllers. Within a virtual world, the
user can choose directions and get the impression of walking or running simply by
regulating the motion speed. Being the self-locomotion the base of embodiment and
grounding consequently episodic memory (Glenberg and Hayes, 2016) virtual promenades
could compensate for the decrease of the spontaneous motion in elderly. Jebara et
al. (2014) investigated the effect of different types of virtual navigation on episodic
memory in young and older adults. In a virtual environment designed as a city to be
explored from inside a car, participants were asked to retrieve the events occurred
with questions on “what,” “where,” and “when.” Participants were assigned to four
experimental conditions: (1) in the passive condition participants were the passengers,
with no possibility to interact with the environment; (2) in the itinerary control,
participants chose the road but did not drive the car; (3) in the low navigation control,
participants displayed the car on rails they could control with pedals without choosing
the directions; (4) in the high navigation control, participants drove as in real
life choosing also directions. As expected, the low navigation and the itinerary control
conditions enhanced episodic memory in both young and older adults. A study by Sauzéon
et al. (2016) report similar findings and suggest that active navigation in episodic
memory by means of VR benefits memory. In this study, younger and older adults explored
two versions (A and B) of a virtual apartment either actively by choosing directions
or passively (through a computer-guided tour of the apartment). The participants were
instructed to memorize all the objects located in the different rooms for future recall.
Performance was measured with different memory tests. The results underlined that
active navigation increased object recognition in both groups, but did not influence
other memory tasks (free recall, proactive interference, and semantic clustering).
The authors discussed this finding as analogy between active navigation and the enactment
effect (Engelkamp et al., 1994). Thereafter recall and recognition of items of verbal
items are enhanced if participants previously execute semantically related actions
to the words. The similarity between active virtual navigation and enactment is given
because both procedures selectively impact item-specific processing as recognition,
but not relational processing (for example semantic clustering of concepts). Following
this perspective, active navigation in VR, can tap into item-specific processing (Pedroli
et al., 2015), known to be more defective in older adults compared to relational processing
(Dennis et al., 2007). Third, VR provides environmental enrichment by using flexible
scenarios. They can in turn be implemented with different degrees of complexity. From
bi-dimensional (2D) to tri-dimensional perspectives (3D), the amount of spatial information
can increase the degree of enrichment. A beneficial effect of environmental enrichment
toward hippocampal function in mice (in terms of neurogenesis and hippocampus-dependent
learning and memory tasks) has been reported by Kempermann et al. (1997). Specifically,
it has been proven that VR place cells can be activated by means of virtual navigation
(Harvey et al., 2009). In humans, Clemenson and Stark (2015) have demonstrated that
3D in virtual environments improves memory in tasks known to be related to hippocampal
activity. In their study, the authors trained naïve video gamers for 2 weeks on two
different videogames. One was based on simple 2D graphics, and one was based on 3D
complex graphics. The control group received no training. Visual and memory performance
were tested: visual accuracy and visual processing speed in an enumeration task, memory
discrimination between highly similar lure items from repeated items, and a spatial
memory score. Participants trained with the 3D videogame outperformed both, the 2D
gamers and the control group in the discrimination task and in the spatial memory
task, but not in the visual task. Being the discrimination task associated with the
activity of the hippocampus (Lacy et al., 2010), authors inferred that 3D enriched
VR presumably impacts also the hippocampal activity. Taken together, these findings
support the view that episodic memory can be enhanced in older adults by means of
enriched 3D scenarios. They can stimulate hippocampal activity which in turn supports
episodic memory.
However, the use of VR with elderly might have some limitations per se: the first
affects the usability of different devices such as HMD, joypad or other controllers
(Castilla et al., 2013). Elder persons are reluctant toward technology and not used
to handle (Manera et al., 2016). The second limitation has to do with the cognitive
load of the task. If the task is too demanding, this can have detrimental effects
on the memory performance if attentional resources might split between complex motor
tasks and memory task (Jebara et al., 2014).
Despite these caveats, these studies pave the way for a new concept of trainings for
episodic memory: proposing VR as an effective tool for active navigation in 3D enriched
worlds.
Author contributions
CR, GR conceived the paper. CR, SS wrote the paper. MM, GR revised the paper.
Conflict of interest statement
The authors declare that the research was conducted in the absence of any commercial
or financial relationships that could be construed as a potential conflict of interest.
The reviewer NP and the handling Editor declared their shared affiliation, and the
handling Editor states that the process nevertheless met the standards of a fair and
objective review.