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Technology and Health Care -1 (2015) 1–13 1
DOI 10.3233/THC-151039
IOS Press
Assessing unilateral spatial neglect using1
advanced technologies: The potentiality of2
mobile virtual reality3
Federica Pallavicinia,∗, Elisa Pedrolia, Silvia Serinoa, Andrea Dell’Isolab, Pietro Cipressoa,4
Carlo Cisariband Giuseppe Rivaa,c
5
aApplied Technology for Neuro-Psychology Laboratory, IRCCS Istituto Auxologico Italiano, Milan,6
Italy7
bPhysical and Rehabilitative Medicine, Department of Health Sciences, Università del Piemonte8
Orientale “A. Avogadro”, Novara, Italy9
cDepartment of Psychology, Catholic University of Milan, Milan, Italy10
Received 8 July 201511
Accepted 4 August 201512
Abstract.13
BACKGROUND: Unilateral Spatial Neglect, or neglect, is a common behavioral syndrome in patients following unilateral14
brain damage, such as stroke. In recent years, new technologies, such as computer-based tools and virtual reality have been15
used in order to solve some limitations of the traditional neglect evaluation. Within this perspective, also mobile devices such16
as tablets seems to be promising tools, being able to support interactive virtual environments and, at the same time, allowing to17
easily reproduce traditional paper-and-pencil test.18
OBJECTIVE: In this context, the aim of our study was to investigate the potentiality of a new mobile application (Neglect19
App) designed and developed for tablet (iPad) for screening neglect symptoms.20
METHODS: To address this objective, we divided a sample of 16 right-damaged patients according to the presence or absence21
of neglect and we administered assessment test in their traditional and Neglect App version.22
RESULTS: Results showed that the cancellation tests developed within Neglect App were equally effective to traditional paper-23
and-pencil tests (Line cancellation test and Star Cancellation test) in detecting neglect symptoms. Secondly, according to our24
results, the Neglect App Card Dealing task was more sensitive in detecting neglect symptoms than traditional functional task.25
CONCLUSIONS: Globally, results gives preliminary evidences supporting the feasibility of Neglect App for the screening of26
USN symptoms.27
Keywords: Neglect, neuropsychological assessment, tablet, virtual reality28
1. Introduction29
Unilateral Spatial Neglect (USN), or neglect, is a common behavioral syndrome in patients following30
unilateral brain damage, such as stroke. The reported incidence of USN can be identified in approxi-31
∗Corresponding author: Federica Pallavicini, Applied Technology for Neuro-Psychology Laboratory (IRCCS Istituto Auxo-
logico Italiano), Via Magnasco, 2, 20149 Milano, Italy. E-mail: f.pallavicini@auxologico.it.
0928-7329/15/$35.00 © 2015 – IOS Press and the authors. All rights reserved
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2F. Pallavicini et al. / Assessing unilateral spatial neglect using advanced technologies
mately 40–50% of the post-stroke patients [1,2]. This disorder is generally characterized by a difficulty32
or inability to pay attention, to detect, and to orient toward objects located in the hemi-space contralateral33
to the lesion of one of the cerebral hemispheres, even in the absence of sensory or motor deficit [3,4]. In34
particular, neglect symptoms are more both common and severe after damages in the right hemisphere,35
which consequently affect patients’ behaviors in the left part of the space [5,6]. USN is a complex syn-36
drome, difficult to assess and treat, characterized by heterogeneous symptoms [7–9].37
Traditionally, USN is evaluated with paper-and-pencil cancellation tests, where patients are asked to38
detect specific targets displayed in a sheet: distracters may be inserted to increase the difficulty of the39
task. These test include line [10], circle [11], letter [12], star [13] and symbol cancellation [14], among40
others.41
Although USN diagnosis based on traditional pencil-and-paper test is widely used by clinicians, it has42
been observed by a lot of studies that they are characterized by two main important limitations. First of43
all, previous research reported that this type of test lack of ecological validity [15,16] and inconsistencies44
have been reported between neglect patients’ performance in these test and important deficits occurring45
in their daily life activities [17–20]. As underlined by Tsirlin and colleagues [21], most of these tests46
don’t capture everyday problems occurring in natural environments of USN patients.47
However,given the complexity of patients’ daily life activities, it is extremely difficult to observe them,48
in term of time and resources [22]. Secondly, traditional paper-and-pencil cancellation test capture the49
spatial navigation deficit insufficiently, or even not at all, even if it seems to be an important characteristic50
in the domain of the neglect syndrome [23,24].51
In the last few decades, one of the major advances in neuropsychology has been represented by the52
use of new technologies, during both screening and rehabilitation [25–27]. Regarding USN, numerous53
efforts have been made to develop new tools that will enable a more complete assessment, trying to54
go beyond the limits of traditional paper-and-pencil test. In particular, there has been a wide interest in55
transferring paper-and-pencil cancellation tests to computer-based setting, resulting in a more detailed56
and precise recording of performance during the assessment, as well as an enhanced consistency in57
testing across setting [28,29]. Studies have been reported that computer-based assessment tool could be58
potentially more sensitive than paper-and-pencil tests in detecting a slower processing of contralesional59
hemispace [20,29–34]. In even more recent years, promising new methods using Virtual Reality (VR)60
technologies have emerged. In the domain of USN assessment, VR is a relatively new tool [35–40].61
However, this instrument, has proven effective in the assessment of neuropsychological functioning, in62
particular for evaluation of executive [41–43], spatial [38,44] and mental imagery processes [45,46].63
Preliminary studies have explored the use of VR for the assessment of USN symptoms, proposing both64
interesting virtual versions of the traditional pencil-and-paper cancellation tests and virtual tasks specific65
to the investigation of space exploration [21].66
Although the dramatic development in the field of computer-based test and VR, there are still some67
problems related to the use of these technologies, far from the research and clinical settings. First of68
all, from a technological point of view, both these tools are not so easy to be used, requiring a specific69
training for the clinician and the patient. Secondly, both computer-based test and VR system are tools70
developed to be used in the clinic, since they require a specific setting and staff able to use these type of71
technological devices. Finally, from a clinical perspective, these technologies are not easy to be moved at72
patients’ home, where an automatic assessment of USN symptoms may be useful to evaluate the severity73
of symptoms over time, especially when patients are provided with a rehabilitative training.74
Within this perspective, mobile devices such as tablets are promising tools that already meet the re-75
quirements needed to support interactive VR environments and, at the same time, allow to easily repro-76
duce traditional paper-and-pencil cancellation test. However, still very few experimental studies have77
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F. Pallavicini et al. / Assessing unilateral spatial neglect using advanced technologies 3
investigated the potential of the tablet in the assessment of USN [47–49]. So far, moreover, there have78
been few attempts to reproduce traditional paper-and-pencil cancellation tests on the tablet, with the79
aim to develop tool able to offer detailed visuo-spatial indexes in order to better understand the peculiar80
features of the syndrome and to develop a more customized rehabilitation [48,49].81
No study, however, has tried to build a tool for the assessment of USN exploiting the peculiar char-82
acteristics of tablets, such as the possibility to play interactive virtual environments and its graphics83
capabilities. The growing availability, low-cost and easy-to-use of “mobile virtual reality”, that is the84
integration of VR environments on mobile devices, represents a meaningful opportunity for neuropsy-85
chological assessment, although unfortunately not yet adequately explored.86
In this context, the aim of our study was to investigate the potentiality of a new mobile application87
(Neglect App) designed and developed for tablet (iPad) for screening USN symptoms. Accordingly, in88
this study we investigatedwhether our newly developed mobile application could screen USN symptoms89
through comparison to right hemispheric stroke patients with and without neglect.90
2. Materials and methods91
2.1. Participants92
A sample of 25 patients recruited at Ospedale Maggiore di Novara (Italy) were screened for interviews93
and neuropsychological assessmentfor admission to the study. Criteria for participation were the follow-94
ing: (1) Right vascular lesion (which was fully evaluated by the clinical staff of the Ospedale Maggiore95
di Novara); (2) age between 18 and 85 years; (3) no severe cognitive impairment, as assessed with the96
Mini Mental State Examination (MMSE) [50] (MMSE >24); (4) no difficulties in language compre-97
hension; (5) no history of psychosis, alcohol or drug dependence, as assessed by a clinical interview;98
(6) no motor deficit that would prevent the use of the tablet; (7) normal or corrected-to-normal vision.99
In particular, if patients present possible factors (e.g., hemianopsia), typically following some type of100
lesions (e.g., occipital cortex), that may prevent the possibility to take part in this study, were excluded.101
None of the recruited sample presented posterior cerebral artery or lesions in the occipital cortex.102
On the other hand, of the initial recruited sample, three patients were excluded due to important mo-103
tor deficits and six for severe cognitive impairment (MMSE <24). Of the initial recruited sample,104
three patients were excluded due to important motor deficits and six for severe cognitive impairment105
(MMSE <24) [50]. The final experimental sample included 16 participants with right-hemisphere dam-106
age caused by a cerebrovascular lesion, without hemianopia. Participants were 12 men (85.2%) and107
4 women (14.8%). The mean age was 66.1 ±11.9, with mean years of education of 8.56 ±3.5. All108
participants were right-handed.109
According to the score obtained at the Line Cancellation Test [10] and the Star Cancellation Test [53],110
participants were divided into two groups: patients with USN (Neglect Group), and patients without the111
USN (Non-neglect Group). Specifically, if the patient omitted more than 1 line or 3 stars in the left side112
and none in the right side of sheet was included in the Neglect Group. If patients omitted lines or stars113
in both sides of space, the examiner calculated a value (number of item omitted in left side/total items114
omitted); values equal or greater than 0.75 indicate USN. Eight participants (5 males, 3 females) were115
assigned to the Neglect Group, and the other 8 participants (7 males, 1 female) were assigned to the116
Non-neglect Group. Descriptive of the sample are reported in Table 1. Before participating in the study,117
each participant was given written information about the study and was asked to give written consent to118
be included. The study received ethical approval from the Ethical Committee of the Istituto Auxologico119
Italiano.120
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4F. Pallavicini et al. / Assessing unilateral spatial neglect using advanced technologies
Tab l e 1
Demographic and clinical characteristics of the sample
ID Gender Age Education Lesion site Onset Neglect Stroke type
(years) (years) (months)
1 M 53 8 Temporo-frontal 23 No Aneurysm
2 M 56 13 Fronto-parieto-temporal 26 No Ischemic
3 M 74 5 Semioval center 13 Yes Aneurysm
4 M 66 13 Parietal 18 Yes Hemorrhage
5 M 68 13 Fronto-parieto-temporal 18 Yes Ischemic
6 M 69 8 Fronto-parieto-temporal 13 Yes Ischemic
7 M 68 8 Fronto-parieto-temporal 57 No Ischemic
8 M 65 13 Temporo-parietal 21 No Hemorrhage
9 M 77 5 Frontal 31 Yes Subarachnoid hemorrhage
10 M 67 8 Basal ganglia +white matter 5 No Ischemic
11 F 74 5 Frontal-parietal 71 No Ischemic
12 M 67 5 Temporo-parietal 15 No Ischemic
13 F 73 13 Temporo-parietal 4 Yes Ischemic
14 M 59 8 Frontal-parietal 4 No Ischemic
15 F 74 2 Frontal-parietal Insular 3 Yes Ischemic
16 F 59 7 Frontal 3 Yes Subarachnoid hemorrhage
2.2. Instruments121
2.2.1. The neuropsychological evaluation122
A neuropsychological evaluation was conducted both to ensure that patients met the aforementioned123
study criteria and to collect data on the patients’ cognitive profiles. In particular, the Mini Mental State124
Evaluation (MMSE) [50] was used to assess individuals’ general cognitive level.125
2.2.2. Traditional assessment tests126
The following traditional neuropsychological test were used for screening for neglect symptoms:127
1. Traditional paper-and-pencil cancellation tests, which were used both to evaluate neglect symp-128
toms and consequently to divide the sample in two divided into two groups (i.e., patients with129
USN – Neglect Group. and patients without the USN – Non-neglect Group) and to collect data for130
the comparisons with their Neglect App version.131
In particular, we administered the two following paper-and-pencil cancellation tests:132
a) Line cancellations test [10]: the patient was given a sheet of paper with three rows of six lines on133
the left and the same on the right, and one row of four lines in the center. Individuals are asked134
to cross out all the lines on the page (size of 56.39 ×37.34 cm). The number of lines selected135
and non-selected (omissions) targets on the left side and on the right side were recorded (for a136
total of 18).137
b) Star cancellation test within the behavioural inattention test (BIT) [13]: patient was presented138
with 56 small stars mixed up with many large stars and capital letters (page size of 56.39 ×139
37.34 cm). Individual was asked to cross out all the small stars after the examiner had demon-140
strated this, crossing out two centrally positioned small stars. The number of selected and omit-141
ted small stars on the left side and on the right side were recorded (for a total of 28 stars).142
2. Traditional card dealing task, taken from Semi-structured Scales for the Functional Evaluation of143
Hemi-inattention [51,52], was used as a functional and ecological evaluation of USN symptoms,144
in order to collect data for the comparisons with its Neglect App version, During this task the145
examiners ask the patient to deal three cards for a game to himself/herself and to each one of the146
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F. Pallavicini et al. / Assessing unilateral spatial neglect using advanced technologies 5
three individuals seated at the same table (the examiner in the front of, one person at the right side147
and another one at the left side of the patient) and four in the middle of the table. The number of148
cards correctly given and the number of cards not deal in the left side and in the right side of the149
patient were recorded (for a total of 3 cards).150
2.2.3. Neglect App assessment tests151
Neglect App, the iPad application developed and used in this study, contains a series of test for the152
evaluation of the USN using interactive virtual environments. Specifically, the app includes two different153
categories of tasks:154
1. Neglect App cancellation tests, which are designed to recreate the traditional paper-and-pencil155
cancellation test, played within the application in a three-dimensional version. The two cancellation156
tests included in NeglectApp have been developedon the basis of the paper-and-pencil cancellation157
test described in the previous paragraph and in particular:158
a) Neglect App simple cancellation test, which corresponds to the Line Cancellations Test [10].159
Patients have to selected 30 hammers placed in a room (15 on the left and 15, on the right160
side). The number of hammers selected (correct targets) and the number of item non selected161
(omissions) on the left side and on the right side was recorded;162
b) Neglect App cancellation with distractors test built on the basis of the Star Cancellation163
Test [53]. Patients have to select 12 screwdrivers (6 in the right and 6 in the left) placed in164
a room with 22 other objects (hammers, wrench and others, 11 on the right and 11 on the left).165
The number of selected and omitted screwdrivers on the left side and on the right side were166
recorded (see Fig. 1).167
2. NeglectAppcarddealingtaskrecreates, in a virtual environment on the tablet, the Card Dealing168
Task [51,52] described in the previous paragraph. As in the traditional version of the test, the patient169
have to give three cards for a game to himself/herself and to each one of the three individuals seated170
and four in the middle of the table. The number of cards correctly given and the number of cards171
not deal in the left side and on the right side of the patient were recorded (for a total of 3 cards).172
Neglect App test were carried out with the aid of a stylus for touchscreen, on an iPad2 (Model173
A1397 with IOS ver. 7.1, screen size active area of 47.70 ×26.82 cm.174
2.2.4. Neglect App usability assessment175
The System Usability Scale (SUS) [54] was used to evaluate the Neglect App usability. The scale is176
composed of 10 statements that are scored on a 5-point scale of strength of agreement. For each item,177
the score may range from 0 to 4, and then the sum of score have to be multiplied for 2.5. Consequently,178
final scores for the SUS can range from 0 to 100, where higher scores indicate better usability.179
2.2.5. Technological skills assessment180
A self-assessment scale was used to evaluate patients’ technological abilities. The two-item question-181
naire was created to assess individuals’ perceived technological skills in the use of personal computers182
and tablet. The individual is asked to rate from 0 to 100 his/her perceived technological skills both in the183
use of personal computers and tablet, where higher scores indicate better perceived skills.184
2.3. Procedure test185
Participants were included in the study after a preliminary clinical interview and a neuropsychological186
evaluation using the Mini Mental State Evaluation (MMSE) [50]. According to this preliminary evalu-187
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6F. Pallavicini et al. / Assessing unilateral spatial neglect using advanced technologies
Fig. 1. Traditional cancellation test, line cancellation test [10]
and star cancellation test [13], compared with their Neglect
App version, respectively Neglect App simple cancellation test
and Neglect App with distractors cancellation test. (Colours are
visible in the online version of the article; http://dx.doi.org/10.
3233/THC-151039)
Fig. 2. Screenshot of the Neglect App card dealing task.
(Colours are visible in the online version of the article; http:
//dx.doi.org/10.3233/THC-151039)
ation and the inclusion/exclusion criteria described above, participants who were suitable for the study188
attended a single testing session at the Ospedale Maggiore di Novara, lasting about one hour. Upon189
arrival the procedure was explained to the individuals and informed consent was obtained. Then, indi-190
viduals were asked to fill out the technological skills assessment questionnaire. Participants were asked191
randomly to complete traditional and Neglect App test, following an established randomization schema192
obtained from http://www.randomizer.org/. The order of tests in both conditions of assessment was also193
randomized for each subject. Before completing Neglect App tasks, each participant had a training pe-194
riod of about ten minutes in an ad hoc virtual environment within the app, in order to become familiar195
with both the navigation and selection tasks. Moreover, at the end of the Neglect App tests, participants196
were asked to fill out the SUS.197
3. Results198
Data were entered into Microsoft Excel and analyzed using SPSS for Windows, version 18.0 (Statis-199
tical Package for the Social Sciences-SPSS for Windows, Chicago, IL, USA). Since outcomes were not200
approximately normally distributed, non parametric statistics were used. Specifically, the Mann-Whitney201
Test was used to compare the two independent groups. In particular the performance of the Neglect and202
Non-neglect Group in the traditional and Neglect App tests were compared using non parametric anal-203
ysis, in order to test whether the number of omitted targets in the traditional and Neglect App tasks204
changed depending on the neglect condition (Neglect vs. Non-neglect Group).205
An index of omission error score (one for the left side and one for the right side) has been computed206
[(number of omissions/number of targets) ×100] for each assessment tasks [55]. These scores were207
compared between the Neglect and Non-neglect Group using the Mann-Whitney Test. Nonparametric208
test was used also to test difference between groups in Neglect App usability score, assessed through the209
SUS. The level of significance was set at α=0.05.210
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F. Pallavicini et al. / Assessing unilateral spatial neglect using advanced technologies 7
Tab l e 2
Median values and Mann-Whitney U test results in the sample divided for group (Neglect and Non-Neglect Group) for age,
education, duration from onset, MMSE score and perceived skills in the use of PC and tablet
Neglect Group Non-neglect Group Ur p
Variables Median Median
Age 71 66 14 −0.475 0.06
Education (years) 70.5 80.5 29 −0.08 0.743
Duration from onset (months) 13 22 160.5 −0.407 0.103
MMSE score 26 260.8 25 −0.183 0.462
Perceived skills in the use of a PC 35 35 310.5 −0.013 0.957
Perceived skills in the use of a tablet 170.5 20 28 −0.111 0.656
Tab l e 3
Median values and Mann-Whitney U test results in the sample divided for Group (Neglect and Non-neglect Group) for tradi-
tional paper-and-pencil and Neglect App assessment test mean scores expressed in %) in the left side
Neglect Group Non-neglect Group Ur p
Variables Median Median
Line cancellation test 660.6 0.000 15 −0.496 0.047*
Neglect App simple cancellation test 930.3 60.66 80.5 −0.632 0.01**
Star cancellation test 900.7 70.4 2 −0.795 0.001***
Neglect App cancellation with distractors test 100 0.000 8 −0.66 0.008**
Traditional card dealing task 330.3 0.000 21 −0.116 0.755
Neglect App card dealing task 100 0.000 120.5 −0.622 0.02*
*P<0.05, **P<0.01, ***P<0.001.
3.1. General characteristics of Neglect and Non-neglect Group procedure test211
Results did not show any significant differences with regard to age, education, duration from onset,212
MMSE mean scores and perceived technological skills between the Neglect and Non-neglect Group213
(p>0.05) (see Table 2).214
3.2. Comparison of Neglect and Non-neglect Group performance in traditional and Neglect App215
assessment test216
Two individuals were excluded from the Neglect App Card Dealing analyses due to problems in the217
score recording; hence, the analyses were conducted with 14 participants: 8 Neglect and 6 Non-Neglect.218
Non-parametric analyses showed a significant difference in the number of omissions in the left side219
between Neglect and Non-neglect Group in the Line Cancellation Test (U=15; r=−0.496; p<220
0.05), Neglect App Simple Cancellation Test (U=8.5; p<0.01; r=−0.632), Star Cancellation221
Tes t ( U=2; p<0.001; r=−0.795;), Neglect App Cancellation with Distractors Test (U=8; p<222
0.01; r=−0.66;), and in the Neglect App Card Dealing Task (U=12.5; p<0.05; r=−0.622;).223
No difference between groups were found in the Traditional Card Dealing Task (U=21; p>0.05;224
r=−0.116) (see Table 3).225
Results on the number of omissions in the right side did not show any statistically significant difference226
between Neglect and Non-neglect Groups (p>0.05) (see Table 4).227
3.3. Neglect App usability228
The mean SUS score of the all sample was high (80.1 ±16.6), indicating a high usability of the229
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8F. Pallavicini et al. / Assessing unilateral spatial neglect using advanced technologies
Tab l e 4
Median values and Mann-Whitney U test results in the sample divided for group (Neglect and Non-neglect Group) for traditional
paper-and-pencil and Neglect App assessment test mean scores (expressed in %) in the right side
Neglect Group Non-neglect Group Urp
Variables Median Median
Line cancellation test 20.77 0.000 180.5 −0.43 0.084
Neglect App simple cancellation test 30 10 150.5 −0.438 0.079
Star cancellation test 330.3 50.55 210.5 −0.279 0.263
Neglect App cancellation with distractors test 25 0.000 16 −0.465 0.063
Traditional card dealing task 0.000 0.000 20 −0.307 0.248
Neglect App card dealing task 0.000 0.000 310.5 −0.024 0.927
Fig. 3. Whitney U test results in the sample divided for group (neglect and Non-neglect) for line cancellation test star cancel-
lation test, Neglect App simple cancellation test, and Neglect App with distractors cancellation test, in the left-space. (Colours
are visible in the online version of the article; http://dx.doi.org/10.3233/THC-151039)
Neglect App. Non-parametric analyses did not show significant difference in the SUS total score between230
Neglect (Median =78.7) and Non-neglect Group (Median =86.2) (U=18.5; p=0.154; r=−0.356).231
4. Discussion232
This study provides preliminary evidence supporting the feasibility of Neglect App for the screening of233
USN symptoms. In particular, results showed that the cancellation tests developed within Neglect App234
were equally effective to the traditional paper-and-pencil tests in the screening of symptoms between235
patients with and without neglect. Moreover, according to our results, the Neglect App Card Dealing236
task was more sensitive in detecting neglect symptoms than traditional functional task.237
Firstly, regarding cancellation tests, results showed that the percentage of omissions in the left side238
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F. Pallavicini et al. / Assessing unilateral spatial neglect using advanced technologies 9
Fig. 4. Whitney U test results in the sample divided for group (neglect and Non-neglect) for traditional and Neglect App card
dealing task in the left side. (Colours are visible in the online version of the article; http://dx.doi.org/10.3233/THC-151039)
(but not in the right side) was significantly different between Neglect and Non-neglect Group both in239
the traditional paper-and-pencil test, (i.e., Line Cancellation Test [10] and Star Cancellation Test [13])240
than in the Neglect App versions of these tests, respectively Neglect App Simple Cancellation test and241
Neglect App with Distractors Cancellation test. Similarly to our results, a recent previous study [49]242
reported differences in cancellation test between patients with and without neglect in a tablet version of243
these test. Our results, moreover, seems in accordance to what has been observed in a previous study [56]244
in which patients with neglect showed aberrant search performance in a virtual reality cancellation task.245
Secondly, regarding the Card Dealing task, results showed significantly differences in the percent-246
age of omissions between Neglect and Non-neglect Group in the Neglect App version of Card Dealing247
task but not in the traditional one. This result could be explained thorugh different assumptions. Firstly,248
results obtained may be related to a specific feature of Neglect App. It is argued that there is a disso-249
ciation between a spared strategy-driven attention opposed to a loss of stimuli-related attention [57].250
Apparently, in real-life, the external cues orient and guide the preserved attentional strategies, while in251
a virtual environments experienced on a tablet there are only standardized stimuli and this condition252
may aggravates USN symptoms. Secondly, our results can be interpreted according to the “pre-motor253
model” that suggests the presence in the brain of multiple and dissociable frames of spatial reference254
(personal, peri-personal and extra-personal) [58,59]. In particular the difference we observed could be255
related to the fact that while Neglect App version of Card Dealing task assess hemispatial neglect in the256
near extra-personal space, the traditional version involved a more extensive extra-personal space.257
Finally, it’s interesting to note that in our study, participants, even if they were characterized by low258
knowledge in the use of PCs and tablets and by a high mean age (about 65 years old), reported excellent259
user-friendliness of Neglect App, as shown by the analyses on the SUS questionnaire. Moreover, we260
did not observe difference in Neglect App usability between patient with and without USN. This seems261
important to exclude that, because of USN patients motor limitations, there are difficulties in the use of262
the app and its ease of learning.263
5. Conclusion264
Even if our results are interesting for their possible applications in the assessment and rehabilitation265
of the USN, our study have some limitations, which could affect the generalizability of the results,266
or that may have influenced the findings. The main one is related to the small sample included in the267
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10 F. Pallavicini et al. / Assessing unilateral spatial neglect using advanced technologies
study. However, it’s important to acknowledge that patients with right hemisphere damage caused by a268
cerebrovascular lesion is really difficult to be recruited. For the same reason, a number of studies in this269
field have often included an even more limited number of subjects (e.g. [4,56,60]. Moreover, differently270
from the majority of other studies, we did not include a control group of healthy participants, focusing271
only on a clinical sample, more complex to be found but more informative. The second limit is related to272
the fact that, the Neglect App version adopted in the study, did not offer visuospatial data (e.g. latency,273
distance, search speed) about patients’ performance during the different tasks. To record also this type274
of data, that could be obtained creating an interface between tablet and software for the recording of275
visual movements (e.g. eye-tracking software), would give an important additional value to the app.276
Future studies will investigate deeply this aspect. Finally, future studies are needed also to increase the277
generalizability of the results found regarding Neglect App and the possibility to use tablets and mobile278
virtual reality to replace existing traditional USN test (e.g. increasing the number of participants of the279
study, and conducting a follow-up study repeated administration of the test).280
As regards to the differences between the existing applications on the app store that attempts to repli-281
cate the conventional pencil and paper test and Neglect App, the main ones could be summarized as282
following:283
–Neglect App is the only one that contains a functional task that replicate on the tablet an ecological284
activity (dealing cards), thanks to the adoption of interactive virtual environments. This is relevant285
since, despite the evidence supporting the possible use of virtual reality in neuropsychological eval-286
uation and the increased interest in its use in cognitive training, this technology is still little explored287
and exploited [61].288
–The tests included in Neglect App (including those of barrage) unlike other app such as iNeglect289
(©Yonsey Severance Hospital), neglectTest (©Why not Zoidberg UG), and Visual Attention Ther-290
apy Lite (©Tactus Therapy Solutions Ltd), are not simple reproductions of classical tests (also291
from the point of view of graphics and interaction). Neglect App tasks, in fact, have been devel-292
oped specifically to exploit the specific characteristics of the tablet, such as the possibility to play293
interactive virtual environments and its graphics features.294
–Neglect App is available in the app store for free, unlike other app such as neglectTest (©Why not295
Zoidberg UG, 19.99C) and CABPad (©Cognisoft ApS; 449.99 C). This appears relevant since cost296
remains an important factor that can limit access to computerized testing and new technologies in297
general [61].298
In the future, it would be interesting to develop tasks that exploit the full potential of tablets and mobile299
virtual reality, using their features of navigation, realism and interactivity. In particular, if these results300
will be confirmed by future studies, it would be possible to develop mobile virtual reality scenarios to301
evaluate patients on important activities of daily living (such as for example, driving and cooking). This302
could enable neuropsychologists to save time and costs compared to those of tests administered in the303
real environment. Moreover, it could be interesting to study the possibility offered by mobile virtual304
reality and tablets in USN rehabilitation programs. Such technologies, in fact, could make patients’305
homework and tasks more engaging, and consequently more effective, than traditional ones. Potentially,306
moreover, data collected about exercises made on tablet (scores at each task, frequency of use, etc.) could307
be tracked over time and integrated with other patient information, providing important information to308
the clinician.309
Acknowledgments310
This study was supported by the Italian funded project “VRehab. Virtual Reality in the Assessment311
Galley Proof 14/08/2015; 8:53 File: THC1039.tex; BOKCTP/xhs p. 11
F. Pallavicini et al. / Assessing unilateral spatial neglect using advanced technologies 11
and TeleRehabilitation of Parkinson’s Disease and Post-Stroke Disabilities” – RF-2009-1472190. The312
authors are grateful to Fabio Ferrara and Valentina Virginia Zoffoli for their technical support in the313
development of Neglect App.314
Conflict of interest315
The authors declare that they have no competing interests.316
References317
[1] Appelros P, Karlsson GM, Seiger A, Nydevik I. Neglect and anosognosia after first-ever stroke: incidence and relation-318
ship to disability. Journal of Rehabilitation Medicine. 2002; 34(5): 215-20.319
[2] Ringman JM, Saver JL, Woolson RF, Clarke WR, Adams HP. Frequency, risk factors, anatomy, and course of unilateral320
neglect in an acute stroke cohort. Neurology. 2004; 63(3): 468-74.321
[3] Heilman KM, Bowers D, Valenstein E, Watson RT. Hemispace and hemispatial neglect. Advances in Psychology. 1987;322
45: 115-50.323
[4] Buxbaum LJ, Ferraro MK, Veramonti T, Farne A, Whyte J, Ladavas E, et al. Hemispatial neglect: subtypes, neu-324
roanatomy, and disability. Neurology. 2004; 62: 749-56.325
[5] Azouvi P, Samuel C, Louis-Dreyfus A, Bernati T, Bartolomeo P, Beis JM, et al. Sensitivity of clinical and behavioural326
tests of spatial neglect after right hemisphere stroke. J ournal of Neurology, Neurosurgery & Psychiatry. 2002; 73: 160-6.327
[6] Bisiach E, Perani D, Vallar G, Berti A. Unilateral neglect: personal and extra-personal. Neuropsychologia. 1986; 24(6):328
759-67.329
[7] Heilman KM, Valenstein E, Watson RT. The what and the how of neglect. In: Halligan PW, Marshall JC, editors. Spatial330
neglect: position papers on theory and practice Hove, UK: Erlbaum; 1994. p. 133-41.331
[8] Robertson IH, Halligan JC. Spatial neglect: A clinical handbook for diagnosis and treatment. Hove, UK: Psychology332
Press; 2000.333
[9] Stone SP, Wilson B, Wroot A, Halligan PW, Lange LS, Marshall JC, et al. The assessment of visuo-spatial neglect after334
acute stroke. Journal of Neurology, Neurosurgery, and Psychiatry. 1991; 54.335
[10] Albert ML. A simple test of visual neglect. Neurology. 1973.336
[11] Vallar G, Perani D. The anatomy of unilateral neglect after right-hemisphere stroke lesions. A clinical/CT-scan correlation337
study in man. Neuropsychologia. 1986; 24(5): 609-22.338
[12] Diller L, Weinberg J. Hemi-inattention in rehabilitation. The evolution of a rational remediation program. In: Weinstein339
EA, Friedland RP-, editors. Hemi-inattention and hemisphere specialization. New York: Raven Press; 1977. p. 62-82.340
[13] Wilson B, Cockburn J, Halligan P. Behavioural inattention test. Titchfield, Hampshire, UK: Thames Valley Test Com-341
pany; 1987.342
[14] Weintraub S, Mesulam MM. Visual hemispatial inattention: stimulus parameters and exploratory strategies. Journal of343
Neurology, Neurosurgery, and Psychiatry. 1988; 51(12): 1481-8.344
[15] Perez-Garcia M, Godoy-Garcia JF, Vera-Guerrero N, Laserna-Triguero JA, Ouente AE. Neuropsychological evaluation345
of everyday memory. Neuropsychology Review. 1998; 8: 203-27.346
[16] Levick WR. Observer rating of memory in children: a review. Brain Impairment. 2010(11): 144-51.347
[17] Eslinger PJ, Grattan LM, Damasio H, Damasio AR. Developmental consequences of childhood frontal lobe damage.348
Archives of Neurology. 1992; 49: 764-9.349
[18] Eslinger PJ, Flaherty-Craig CV, Benton AL. Developmental outcomes after early prefrontal cortex damage. Brain and350
Cognition. 2004; 55: 84-103.351
[19] Vriezen ER, Pigott SD, Pelletier PM. Developmental implications of early frontal-lobe damage: a case study. Brain and352
Cognition. 2001; 47: 222-5.353
[20] Bonato M. Neglect and extinction depend greatly on task demands: a review. Frontiers in Human Neuroscience. 2012;354
6: 195.355
[21] Tsirlin I, Dupierrix E, Chokron S, Coquillart S, Ohlmann T. Uses of virtual reality for diagnosis, rehabilitation and study356
of unilateral spatial neglect: review and analysis. Cyberpsychology & behavior. 2009; 12(2): 175-81.357
[22] Chevignardi MP, Soo C, Galvin J, Catroppa C, Eren S. Ecological assessment of cognitive functions in children with358
acquired brain injury: a systematic review. Brain Injury. 2012; 26(9): 1033-57.359
[23] Guariglia C, Piccardi L. Environmental orientation and navigation in different types of unilateral neglect. Experimental360
Brain Research. 2010; 206: 163-9.361
Galley Proof 14/08/2015; 8:53 File: THC1039.tex; BOKCTP/xhs p. 12
12 F. Pallavicini et al. / Assessing unilateral spatial neglect using advanced technologies
[24] Buxbaum LJ, Palermo MA, Mastrogiovanni D, Schmidt Read M, Rosenberg-Pitonyak E, Rizzo AA, et al. Assessment of
362
spatial attention and neglect with a virtual wheelchair navigation task. Journal of Clinical and Experimental Neuropsy-363
chology. 2006; 30: 650-60.364
[25] Bohil CJ, Alicea B, Biocca FA. Virtual reality in neuroscience research and therapy. Nature Reviews Neuroscience. 2011;365
12(12): 752-62.366
[26] Rose FD, Brooks BM, Rizzo AA. Virtual reality in brain damage rehabilitation: review. CyberPsychology & Behavior.367
2005; 8(3): 241-62.368
[27] Gaggioli A, Riva G. Psychological treatments: smart tools boost mental-health care. Nature. 2014; 512(7512): 28-.369
[28] Deouell LY, Sacher Y, Soroker N. Assessment of spatial attention after brain damage with a dynamic reaction time test.370
Journal of the International Neuropsychological Society. 2005; 11: 697-707.371
[29] Schendel KL, Robertson LC. Using reaction times to assess patients with unilateral neglect and extinction. Journal of372
Clinical and Experimental Neuropsychology. 2002; 24: 942-50.373
[30] List A, Brooks JL, Esterman M, Fle-varis AV, Landau AN, Bowman G, et al. Visual hemispatial neglect, re-assessed.374
Journal of the International Neuropsychological Society. 2008; 14: 243-56.375
[31] Posner MI, Walker JA, Friedrich FJ, Rafal RD. Effects of parietal injury on covert orienting of attention. Journal of376
Neuroscience. 1984; 4: 1863-74.377
[32] Smania N, Martini MC, Gambina G, Tomelleri G, Palamara A, Natale E, et al. The spatial distribution of visual attention378
in hemineglect and extinction patient. Brain. 1998; 121: 1759-70.379
[33] Losier BJW, Klein RM. A review of the evidence for a disengage deficit following parietal lobe damage. Neuroscience380
& Biobehavioral Reviews. 2001; 25: 1-13.381
[34] Marzi CA, Natale E, Anderson B. Mapping spatial attention with reaction time in neglect patients. In: Karnath H-O,382
Milner AD, Vallar G, editors. The Cognitive and Neural Basis of Spatial Neglect. Oxford: University Press; 2002. p.383
275-88.384
[35] Tsirlin I, Dupierrix E, Chokron S, Coquillart S, Ohlmann T. Uses of virtual reality for diagnosis, rehabilitation and study385
of unilateral spatial neglect: review and analysis. Cyberpsychology & Behavior. 2009; 12(2): 2009.386
[36] Kim DY, Ku J, Chang WH, Park TH, Lim JY, Han K, et al. Assessment of post-stroke extrapersonal neglect using a387
three-dimensional immersive virtual street crossing program. Acta Neurologica Scandinavica. 2010; 121(3): 171-7.388
[37] Mesa-Gresa P, Lozano JA, Llórens R, Alcañiz M, Navarro MD, Noé E, editors. Clinical validation of a virtual environ-389
ment test for safe street crossing in the assessment of acquired brain injury patients with and without neglect. 13th IFIP390
TC 13 International Conference on Human-Computer Interaction 2011; Lisbon, Portugal.391
[38] Fordell H, Bodin K, Bucht G, Malm J. A virtual reality test battery for assessment and screening of spatial neglect. Acta392
Neurologica Scandinavica. 2011; 123(3): 167-74.393
[39] Peskine A, Rosso C, Box N, Galland A, Caron E, Rautureau G, et al. Virtual reality assessment for visuospatial neglect:394
importance of a dynamic task. Journal of Neurology, Neurosurgery & Psychiatry. 2011; 11(12): 1407-9.395
[40] Sugarman H, Weisel-Eichler A, Burstin A, Brown R, editors. Use of novel virtual reality system for the assessment and396
treatment of unilateral spatial neglect: a feasibility study. Virtual Rehabilitation (ICVR), 2011 International Conference397
on; 2011: IEEE.398
[41] Cipresso P, Albani G, Serino S, Pedroli E, Pallavicini F, Mauro A, et al. Virtual multiple errands test (VMET): a virtual399
reality-based tool to detect early executive functions deficit in Parkinson’s disease. Frontiers in Behavioral Neuroscience.400
2014; 8: 405.401
[42] Rand D, Rukan SBA, Weiss PL, Katz N. Validation of the virtual MET as an assessment tool for executive functions.402
Neuropsychological Rehabilitation. 2009; 19(4): 583-602.403
[43] Raspelli S, Pallavicini F, Carelli L, Morganti F, Pedroli E, Cipresso P, et al. Validating the neuro vr-based virtual version404
of the multiple errands test: preliminary results. Presence. 2012; 21(1): 31-42.405
[44] Weniger G, Ruhleder M, Lange C, Wolf S, Irle E. Egocentric and allocentric memory as assessed by virtual reality in406
individuals with amnestic mild cognitive impairment. Neuropsychologia. 2011; 49(3): 518-27.407
[45] Cánovas R, León I, Serrano P, Roldán M, Cimadevilla JM. Spatial navigation impairment in patients with refractory408
temporal lobe epilepsy: evidence from a new virtual reality-based task. Epilepsy & Behavior. 2011; 22(2): 364-9.409
[46] Morganti F, Stefanini S, Riva G. From allo-to egocentric spatial ability in early Alzheimer’s disease: a study with virtual410
reality spatial tasks. Cognitive Neuroscience. 2013; 4(3-4): 171-80.411
[47] Rabuffetti M, Ferrarin M, Spadone R, Pellegatta D, Gentileschi V, Vallar G, et al. Touch-screen system for assessing412
visuo-motor exploratory skills in neuropsychological disorders of spatial cognition. Medical and Biological Engineering413
and Computing. 2002; 40(6): 675-86.414
[48] Rabuffetti M, Farina E, Alberoni M, Pellegatta D, Appollonio I, Affanni P, et al. Spatio-temporal features of visual415
exploration in unilaterally brain-damaged subjects with or without neglect: results from a touchscreen test. PLoS One.416
2012.417
[49] Vaes N, Lafosse C, Nys G, Schevernels H, Dereymaeker L, Oostra K, et al. Capturing peripersonal spatial neglect: an418
electronic method to quantify visuospatial processes. Behavior Research Methods. 2014; 47(1): 27-44.419
Galley Proof 14/08/2015; 8:53 File: THC1039.tex; BOKCTP/xhs p. 13
F. Pallavicini et al. / Assessing unilateral spatial neglect using advanced technologies 13
[50] Folstein MF, Robins LN, Helzer JE. The mini-mental state examination. Archives of General Psychiatry. 1983; 40(7):
420
812-22.421
[51] Zoccolotti P, Antonucci G, Judica A. Psychometric characteristics of two semi-structured scales for the functional eval-422
uation of hemi-inattention in extrapersonal and personal space. Neuropsychological Rehabilitation. 1992; 2(3): 179-91.423
[52] Zoccolotti P, Judica A. Functional evaluation of hemineglect by means of a semistructured scale: personal extrapersonal424
differentiation. Neuropsychological Rehabilitation. 1991; 1(1): 33-44.425
[53] Wilson BA. Ecological validity of neuropsychological assessment: Do neuropsychological indexes predict performance426
in everyday activities? Applied and Preventive Psychology. 1993; 2(4): 209-15.427
[54] Brooke J. SUS-A quick and dirty usability scale. Usability evaluation in industry. 1996; 189: 194.428
[55] Ronchi R, Posteraro L, Fortis P, Bricolo E, Vallar G. Perseveration in left spatial neglect: drawing and cancellation tasks.429
Cortex. 2009; 45(3): 300-12.430
[56] Broeren J, Samuelsson H, Stibrant-Sunnerhagen K, Blomstrand C, Rydmark M. Neglect assessment as an application of431
virtual reality. Acta Neurologica Scandinavica. 2007; 116(3): 157-63.432
[57] Eskes GA, Butler B. Using limb movements to improve spatial neglect: the role of functional electrical stimulation.433
Restorative Neurology and Neuroscience. 2006; 24: 385-98.434
[58] Reddon JR, Gill DM, Gauk SE, Marez ND. Purdue pegboard: test-retest estimates. Perceptual and Motor Skills. 1988;435
66: 503-6.436
[59] Tanaka T, Ifukube T, Sugihara S, Izumi T. A case study of new assessment and training of unilateral spatial neglect in437
stroke patients: effect of visual image transformation and visual stimulation by using a head mounted display system438
(HMD). Journal of Neuroengineering and Rehabilitation. 2010; 7(20).439
[60] Bartolomeo P, Chokron S. Orienting of attention in left unilateral neglect. Neuroscience & Biobehavioral Reviews. 2002;440
26(2): 217-34.441
[61] Zygouris S, & Tsolaki M. Computerized cognitive testing for older adults a review. American Journal of Alzheimer’s442
Disease and Other Dementias. 2015; 30(1): 13-28.443
