Applied Neuropsychology: Adult

ISSN: 2327-9095 (Print) 2327-9109 (Online) Journal homepage: http://www.tandfonline.com/loi/hapn21

Use of virtual reality in improving poststroke
neglect: Promising neuropsychological and
neurophysiological findings from a case study
Rosaria De Luca, Viviana Lo Buono, Antonino Leo, Margherita Russo, Bianca
Aragona, Simona Leonardi, Antonio Buda, Antonino Naro & Rocco Salvatore
Calabrò
To cite this article: Rosaria De Luca, Viviana Lo Buono, Antonino Leo, Margherita Russo,
Bianca Aragona, Simona Leonardi, Antonio Buda, Antonino Naro & Rocco Salvatore Calabrò
(2017): Use of virtual reality in improving poststroke neglect: Promising neuropsychological
and neurophysiological findings from a case study, Applied Neuropsychology: Adult, DOI:
10.1080/23279095.2017.1363040
To link to this article: http://dx.doi.org/10.1080/23279095.2017.1363040

Published online: 22 Sep 2017.

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Date: 23 September 2017, At: 06:00

APPLIED NEUROPSYCHOLOGY: ADULT
https://doi.org/10.1080/23279095.2017.1363040

none defined

Use of virtual reality in improving poststroke neglect: Promising
neuropsychological and neurophysiological findings from a case study
Rosaria De Luca, Viviana Lo Buono, Antonino Leo, Margherita Russo, Bianca Aragona, Simona Leonardi,
Antonio Buda, Antonino Naro and Rocco Salvatore Calabrò

Downloaded by [University of Sussex Library] at 06:00 23 September 2017

IRCCS Centro Neurolesi “Bonino Pulejo” Messina, Messina, Italy
ABSTRACT

KEYWORDS

After experiencing a stroke in the right hemisphere, almost 50% of patients show unilateral spatial
neglect (USN). Virtual Reality technologies offer impressive opportunities for both the rehabilitation
and assessment of different cognitive deficits, including USN. A 57-year-old woman, affected by
subarachnoid hemorrhage presented a severe left hemiparesis with severe cognitive and
behavioral alterations, including temporal and spatial disorientation, reduction of attention and
memory process, slowing ideation, USN, and depression of mood. She underwent two different
rehabilitation trainings, including standard cognitive training (SCT) in addition to semi-immersive
virtual training with her shadow (S-IVT_s) and SCT in addition to a Semi- immersive virtual training,
without her shadow (S-IVT). The patient was assessed before and after each of the two different
trainings, by using a specific psychometric battery and the event related potential, P300. Only at
the end of the use of the S-IVT, we observed a significant improvement in the motor and cognitive
function, with regard to USN. SCT in addition to S-IVT with Bts-Nirvana System may be a promising
approach in improving attention process, spatial cognition, and mood in patients with post stroke
USN, as also demonstrated by the electrophysiological parameters.

BTS-Nirvana; cognitive
rehabilitation; motor
recovery; virtual reality

Introduction
Unilateral spatial neglect (USN) is a syndrome caused
by unilateral brain injury, mainly involving the right
hemisphere. There are several pathological processes
that may cause USN, such as neoplasia, trauma and
neurodegenerative disorders; however, stroke is the
most frequent cause of USN. As a matter of fact, in
the acute stage after right hemisphere stroke, USN
may emerge in up to 80% of the patients, but most
studies describe rates closer to 50%” (Li & Malhotra,
2015). Unilateral neglect is a complex syndrome that
is commonly defined as a disorder of perception,
attention and action in controlateral side of damage
(Azouvi, Jacquin-Courtois, & Luautè, 2017), with loss
of spatial awareness of the contralesional side (Rode,
Pagliari, Huchon, Rossetti, & Pisella, 2017). Stroke
patients with USN do not explore controlateral space
effectively and omit to detect stimuli located in that side
of space, even if they can move their head and eyes. It
has been shown that increasing the attentional demands
of the cancellation task aggravates neglect contralesionally (Bowen, Lincoln, & Dewey, 2002). This bias has
been interpreted as a consequence of the disruption of

the selective spatial attentional processes (Ricci et al.,
2016). USN is characterized by different anatomicalclinical subtypes (auditory, visual, somatosensory,
motor, allocentric, egocentric, and representational
neglect) that may be associated or dissociated (Rode
et al., 2017). These clinical subtypes may occur in
association with primary sensory or motor deficits
(Li & Malhotra, 2015). Different treatment and rehabilitative approaches for USN has been described. There is
not a definite answer to whether there are USN treatments generally applicable to improve the functional
behavior, and only a few studies have employed functional-based outcomes (Bowen et al., 2002). Although
various rehabilitation interventions have been used in
treating USN, evidence of their benefit is lacking (Ricci
et al., 2016). In recent years, rehabilitation approaches
of neglect can be sorted into two types: top-down and
bottom-up methods. (Rode et al., 2017) Top-down
methods are based on stimulation of the contralesional
side through a voluntary effort by the patient following
therapist’s instructions. Specifically, these consist in
training the direction of the patient’s gaze using a
prompt to the left. (Rode et al., 2017). On the contrary,

CONTACT Rocco Salvatore Calabrò
salbro77@tiscali.it
IRCCS Centro Neurolesi “Bonino-Pulejo”, S.S. 113, Contrada Casazza, 98124 Messina, Italy.
Color versions of one or more of the figures in the article can be found online at www.tandfonline.com/hapn.
© 2017 Taylor & Francis Group, LLC

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R. DE LUCA ET AL.

bottom-up methods do not require the patient’s
awareness regarding his bias. These consist in the
manipulation of patient’s sensory environment, using
sensory stimulation, hemiblinding (or eyeblinding), or
prism adaptation (Rode et al., 2017). Rehabilitation after
stroke is imperative for patients with USN because it
may improve their behavioral, social, and cognitive outcomes, and therefore it can reduce the financial burden
on public health services (Bowen, Hazelton, Pollock, &
Lincoln, 2013). There is good evidence supporting the
use of pursuit intervention over traditional training that
is based on saccadic eye movements (Ogourtsova, Souza
Silva, Archambault, & Lamontagne, 2015). Recently,
there is limited evidence that virtual reality (VR) is more
effective than conventional therapy in improving USN
in patients with stroke, given that VR may provide
enhanced methods for USN assessment and treatment
(Fordell, Bodin, Eklund, & Malm, 2016; Laver, George,
Thomas, Deutsch, & Crotty, 2011; Pedroli, Serino,
Cipresso, Pallavicini, & Riva, 2015). In particular, it
has been shown that training with VR can improve
spatial attention and the use of such ability in activities
of daily living, even in chronic neglect (Saevarsson,
Kristjánsson, Bach, & Heinrich, 2012).
The aim of this study is to evaluate the neuropsychological and neurophysiological outcomes in a poststroke
individual after an intensive rehabilitative cycle with a
combined therapeutic approach, that is, standard
cognitive training (SCT) in addition to Semi-immersive
Virtual Training (S-IVT) with Bts-Nirvana System.

Material and methods
A 57-year-old woman, affected by subarachnoid
hemorrhage involving the right fronto-temporalparietal region, presented a left hemiparesis; she was
total dependent in the activity of daily life. She had
severe cognitive and behavioral abnormalities, including
temporal and spatial disorientation, reduction of
attention and memory process, slowing ideation, USN
in the left extracorporeal space and severe mood
depression. She underwent two different rehabilitation
trainings, including either standard cognitive training
(SCT) in addition to Semi-immersive virtual training
with her shadow (S-IVT_s) or SCT in addition to a
Semi- immersive virtual training, without her shadow
(S-IVT). Each rehabilitative session with BTS- Nirvana
lasted about 45 minutes. The initial intensive virtual
rehabilitative training (the patient performed the cognitive tasks in a virtual scenario with her shadow)
included 20 rehabilitation sessions, five times a week
for one month. After three weeks of no-treatment in
the virtual environment, the patient was submitted to

the Semi-immersive virtual training, without her
shadow (S-IVT) for other 20 rehabilitative sessions.
The use of the BTS NIRVANA System is different: in
the first combined treatment, there is the avatar of the
patient (i.e., her shadow), whereas in the second
treatment the patient does not see her shadow,
providing a better sensorial video-audio immersion
(See Table 1). Her cognitive and neurophysiological
profile were evaluated in two separate sessions, before
and after each of the two different trainings, by using
a proper psychometric battery: Mini Mental State
Examination (MMSE), Repeatable Battery for Neuropsychological Status (RBANS), Hamilton Rating Scale
for Depression (HRS-D), and Behavioral Inattention
Test (BIT) to assess visual neglect. The allocation of
attention in the patient was obtained by studying the
P300 component of the event-related potential (Sawaki
& Katayama, 2008). Furthermore, the patient’s control
of trunk was evaluated by using the Trunk Control Test
to better assess the motor recovery.
BTS NIRVANA is the first therapeutic system aiding
the rehabilitation process of the patients affected by
neuro-motor and cognitive diseases by multisensory
stimulation. BTS NIRVANA is particularly recommended in the rehabilitation therapy of patients with
movement and attentive dysfunctions caused by stroke.
Standard BTS NIRVANA equipment is composed by 1
or 2 markerless infrared sensors, workstation touch
screen, camera supports (different models available),
BTS NIRVANA software, and Webcam. The system is
connected to a projector or a big screen; it reproduces
an interactive series of exercises and, thanks to an
infrared video camera analyzing the patient’s
movements, it creates interactivity. BTS NIRVANA is
a movement-based system providing patients VR
scenarios to interact with: that is, audio–video stimuli
(musical sphere) presented in the left, in the right, or
in both the sides of interactive virtual scenarios; or
specific nature environment, where the patient can
change different visuo-spatial elements (see Figure 2).

Results
Our findings showed an improvement in motor
(Control of Trunk) and cognitive performances after
the VR rehabilitative training. In particular, after
S-IVT treatment (comparison T0-T3), in addition to
the standard cognitive approach, a nearly complete
resolution of the USN was observed, with a significant
increase in the attention, visual search, scanning, and
spatial cognition scores (Table 2), as shown by the
significant reliable change index (RCI) values. RCI is a
statistic tool that is used to determine whether a change

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APPLIED NEUROPSYCHOLOGY: ADULT

Table 1.

Virtual cognitive rehabilitative program with BTS-Nirvana system.

Cognitive
domain

Nirvana BTS
Semi-immersive virtual training with shadow
S-IVT_s

3

Nirvana BTS
Semi-immersive virtual training without shadow
S-IVT

spatial cognition To program some movements finalized to virtual touch, to move or To program some movements finalized to virtual touch, to move or
and ideomanipulate specific objects, in different directions (i.e.,, balls;
manipulate specific objects, in different directions (i.e.,, balls;
motor praxis
flowers; butterfly); or to realize specific associations (i.e.,, numberflowers; butterfly); or to realize specific associations (i.e.,,
color) with a dynamic interaction in virtual environment. When
number- color) with a dynamic interaction in virtual
the patient touches virtual objects determinate a video and audio
environment. When the patient touch virtual objects
feedback (using sprites task, observing her shadow reflected on
determinate a video and audio feedback (using sprites task,
the virtual scenarios). These rehabilitation exercises with audiointeracting directly with some virtual scenarios, without to
visual stimuli involve the visuo-spatial and praxis abilities of
observe her shadow). These rehabilitation exercises with audiopatients, resulting in a very motivational training.
visual stimuli involve the visuo-spatial and praxis abilities of
patients, resulting in a very motivational training.
In particular, the subject perform ideo-motor sequences (from
In particular, the subject perform ideo-motor sequences (from
simple to complex serious of actions), after the verbal consign by
simple to complex serious of actions), after the verbal consign by
therapist. The patient observes her shadow during the execution
therapist. The patient is immerse in virtual environment, without
of virtual tasks.
seeing her shadow, during the execution of virtual tasks.
The level of difficulty increases (from first to third level) with the
The level of difficulty increases (from first to third level) with the
increase of the complexity of virtual ideo-motor serious to realize.
increase of the complexity of virtual ideo-motor serious to realize.
Attention
To select, with an immediate and recall feedback (audio and video), To select, with an immediate and recall feedback (audio and video),
process
some various elements (colors; musical strings; geometric or not
some various elements (colors; musical strings; geometric or not
form; animals …) observed in the virtual environment. These
form; animals …) observed in the virtual environment. These
elements remain visible to the observer for a variable time,
elements remain visible to observer for a variable time, established
established by the interaction between the virtual system, therapist
by the interaction between the virtual system, therapist and
and patient. The patient touches the virtual target element, in a
patient. The patient touch the virtual target element, in a specific
specific time, and so, this action causes a visual change with a
time, and so, this action cause a visual change with a peculiar audio
peculiar audio feedback (positive reinforce); otherwise the element
feedback (positive reinforce); otherwise the element disappear
disappear (negative reinforce) (Hunt task). The patients observes
(negative reinforce) (Hunt task). The patient interacts directly with
her shadow during the execution of virtual tasks.
these virtual scenarios, without to observe her shadow. The
patients is immersive in virtual environment, without her shadow,
during the execution of virtual tasks.
The level of difficulty increases with the increase of the numbers of
The level of difficulty increases with the increase of the numbers of
distracters and reducing the usable time of execution.
distracters and reducing the usable time of execution.

in an individual’s score (e.g., before and after some
intervention) is statistically significant or not (based
on how reliable the measure is). If the RCI is >1.96,
then the difference is statistically significant (1.96
equates to the 95% confidence interval). The patient also
showed an improvement in mood alteration (Table 2).
P300 amplitude in the 300–800 ms time window at
the Pz electrode was lower for frequent (nontargets)
than for infrequent (target) stimuli when stimulating
the left hemifield (Figure 1), as confirmed by RCI values

(with α of 0.05, Bonferroni corrected) (nontarget vs. left
target, RCI ¼ 1.2; nontarget vs. right target RCI ¼ 3.1;
left target vs. right target, RCI ¼ 3.3). Peak times did
not show clear effects. Following the first training
(S-IVT_s), a mild improvement in P300 amplitude
was observed when stimulating the left hemifield
(RCI ¼ 2.8), whereas a greater improvement was found
after the S-IVT training (RCI ¼ 3.52).

Discussion

Figure 1. Illustrates the P300 amplitudes to target (t) and
nontarget (nt) stimuli provided to the left and right hemifield
at baseline and after Semi-immersive Virtual Training with
(S-IVT_S) and without shadow (S-IVT). Vertical bars refer to SD.

USN is a complex disorder of spatial representation,
spatio-motor programming, and spatial attention. The
rehabilitative approach could be difficult and, to
date, there is not a gold standard method for the
rehabilitation of neglect (Pierce & Buxbaum, 2002). It
is strictly recommended to use a combination of
multiple approaches to develop a personalized rehabilitation process (Kerkhoff & Schenk, 2012), given that a
combination of different treatments seem to be more
effective than a traditional cognitive rehabilitation
program (Arai, Ohi, Sasaki, Nobuto, & Tanaka, 1997).
Paper-and-pencil methods are used in traditional
rehabilitative training. A typical session consists in
repetitive exercises with static, two-dimensional, and
geometrical targets that generally require a simple visual

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R. DE LUCA ET AL.

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Figure 2. Semi-immersive virtual training with (2a) and without (2b) shadow (S-IVT_s) in BTS NIRVANA system.

search in the near space, repeated several times a week
(Newport & Schenk, 2012). Contrarily, for USN
rehabilitation, the use of moving stimuli seem to be
crucial to modulate visual attention and drive attention
to the left side of the space, thereby improving target
detection in a specific area (Cipresso, Serino, Pedroli,
Gaggioli, & Riva, 2014; Kerkhoff, 2003).
VR for USN rehabilitation provides an advanced
human-computer interface that allows the patients to
interact with, and become immersed in, a computergenerated environment similar to the real-life
experience (Tsirlin, Dupierrix, Chokron, Coquillart, &
Ohlmann, 2009). VR rehabilitation of USN seem be
more engaging and consequently more effective than
traditional methods. Using advanced technology,
patients are trained through simulations that are
relevant for everyday life. BTS NIRVANA is a VR
platform that uses immersive reality and multisensory
stimulation to improve cognitive performances. It uses
a movement-based system providing patients virtual
reality scenarios to interact with. This study describes
the use of a combined rehabilitative program based on
a traditional approach and VR, in order to better
improve the neurocognitive functioning, with regard
to USN. Few studies explored the benefits of VR and
computer training in treating neglect. In a single
blinded RCT by Kim, Chun, Yun, Song, and Young
(2011), VR training led to significantly fewer errors on
a cancellation test, with notable improvement also in
daily life. Similarly, in a single case study, Mainetti,
Sedda, Ronchetti, Bottini, and Borghese (2013) found
significant improvement in two neglect tests when the
patient played a video game consisting of reaching for
different targets within the virtual space. Fordell et al.
(2016) developed a new training method, RehAtt,
consisting of a computer with monitor, 3D glasses,
and a force feedback interface (Robotic pen), to stimulate the motor activation to the contralesional arm. This

software, by combining visual scanning training with
multi-sensory stimulation in a 3D VR environment,
led to a significant improvement in chronic USN
(Saevarsson et al., 2012).

This study is in agreement with such previous
studies supporting the hypothesis that VR might
be useful in treating USN
In this study, we used event-related potentials (ERPs) to
more objectively explore brain function in patients with
poststroke neglect. The P300 is a positive ERP component that is most commonly recorded in an oddball
stimulus paradigm, where a series of trials with frequent
stimuli is interspersed trials with rare stimuli of a
Table 2. Unilateral spatial neglect improvement after neurorehabilitation in the virtual environment.
T0
Conventional subtest
Line crossing
Letter cancellation
Star cancellation
Figure and shape copying
Line bisection
Representational drawing
Behavioral subtest
Prescanning
Phone dialing
Menu reading
Article reading
Telling and setting
the time
Coin sorting
Address and sentence
copying
Map navigation
Card sorting
MMSE
HRS-D
TCT

T1

T2

T3

S-IVT_s S-IVT_s RCI S-IVT RCI S-IVT
25
6
14
0
0
1
T0
0
4
0
0
7

29
17
17
0
0
1
T1
0
6
0
0
7

5,3
2,9

29
17
17
0
0
1
T2
2
6
1
1
7

5,3
2,9

2
0

3
2

3
2

5
4

0
1
13
20
37

1
2
15
18
62

1
2
15
16
62

6
6
20
9
74

3,8

32
29
25
1
6
1
T3
5
8
6
5
9

RCI
7
4,2
2

5,9

Note. MMSE ¼ mini mental state examination; HRS-D ¼ Hamilton rating
scale for depression; BIT ¼ behavioral inattention test; TCT ¼ Trunk
control test.
RCI is >1.96 is significant.

APPLIED NEUROPSYCHOLOGY: ADULT

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different type (Saevarsson et al., 2012; Sutton, Braren,
Zubin, & John, 1965). The P300 is known to be modulated by attention in stroke patients with USN (Becker
& Shapiro, 1980), and its assessment further corroborates
our clinical findings. Indeed, S-VIT recovered the
reduced amplitude of the P300 to contralesional targets,
(that refer to the ipsilesional targets), while P300 amplitude increase correlated with the improvement in cognitive function scores and time in the standard neglect
tests. These results suggest a link between a recovery of
attentional dysfunction and the improvement in stimulus
processing, which was strengthened by using S-VIT.

Conclusion
Virtual Reality technologies offer impressive
opportunities for both the rehabilitation and assessment
of different cognitive deficits, including USN. In particular, the combined rehabilitative treatment of SCT
with S-IVT by using the BTS-NIRVANA System may
be a promising approach in improving attention process
and spatial cognition, which was as also demonstrated
by the neurophysiological data. However, future studies
are needed to examine the persisting effects of such
treatment.

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