An initial validation of the Virtual Reality Paced Auditory Serial

Journal of Neuroscience Methods 222 (2014) 15–23
Contents lists available at ScienceDirect
Journal of Neuroscience Methods
journal homepage: www.elsevier.com/locate/jneumeth
Clinical Neuroscience
An initial validation of the Virtual Reality Paced Auditory Serial
Addition Test in a college sample
Thomas D. Parsons a,∗ , Christopher G. Courtney b
a
b
Department of Psychology, University of North Texas, Denton, United States
Department of Psychology, University of Southern California, Los Angeles, United States
h i g h l i g h t s
•
•
•
•
We validate a Virtual Reality Paced Auditory Serial Addition Test (VR-PASAT).
The VR-PASAT requires sustained attention at an increasingly demanding rate.
The VR-PASAT is an attentional processing measure.
The VR-PASAT provides unique information not tapped by traditional attention tasks.
a r t i c l e
i n f o
Article history:
Received 26 August 2013
Received in revised form 6 October 2013
Accepted 9 October 2013
Keywords:
Neuropsychological assessment
Ecological validity
Paced Auditory Serial Addition Test
Virtual environment
a b s t r a c t
Background: Numerous studies have demonstrated that the Paced Auditory Serial Addition Test (PASAT)
has utility for the detection of cognitive processing deficits. While the PASAT has demonstrated high
levels of internal consistency and test–retest reliability, administration of the PASAT has been known
to create undue anxiety and frustration in participants. As a result, degradation of performance may be
found on the PASAT. The difficult nature of the PASAT may subsequently decrease the probability of their
return for follow up testing.
New method: This study is a preliminary attempt at assessing the potential of a PASAT embedded in a
virtual reality environment. The Virtual Reality PASAT (VR-PASAT) was compared with a paper-and-pencil
version of the PASAT as well as other standardized neuropsychological measures. The two modalities of
the PASAT were conducted with a sample of 50 healthy university students, between the ages of 19 and
34 years. Equivalent distributions were found for age, gender, education, and computer familiarity.
Results: Moderate relationships were found between VR-PASAT and other putative attentional processing
measures. The VR-PASAT was unrelated to indices of learning, memory, or visuospatial processing.
Comparison with existing method(s): Comparison of the VR-PASAT with the traditional paper-and-pencil
PASAT indicated that both versions require the examinee to sustain attention at an increasingly demanding, externally determined rate.
Conclusions: Results offer preliminary support for the construct validity (in a college sample) of the
VR-PASAT as an attentional processing measure and suggest that this task may provide some unique
information not tapped by traditional attentional processing tasks.
© 2013 Elsevier B.V. All rights reserved.
The Paced Auditory Serial Addition Test (PASAT) is a serial addition task developed as an aurally mediated alternative to visually
mediated assessments of attention processing (Sampson, 1958;
Sampson and MacNeilage, 1960). The PASAT has been found to have
robust correlations with tests of executive function (e.g., Stroop;
Trails B; Card Sorting; Spikman et al., 2001; Sherman et al., 1997).
∗ Corresponding author at: Clinical Neuropsychology and Simulation (CNS) Lab,
Department of Psychology, University of North Texas, 1155 Union Circle #311280,
Denton, TX 76203, United States. Tel.: +1 940 565 4329.
E-mail address: Thomas.Parsons@unt.edu (T.D. Parsons).
0165-0270/$ – see front matter © 2013 Elsevier B.V. All rights reserved.
http://dx.doi.org/10.1016/j.jneumeth.2013.10.006
Gronwall and Sampson (1974) extended the PASAT to clinical populations in the 1970s with emphasis upon the impact of traumatic
brain injury (TBI) on speed of information processing. The PASAT
also has been used to investigate the ways in which neurocognitive processing has been impacted by multifarious neurological
conditions (e.g., mild traumatic brain injury, multiple sclerosis,
chronic fatigue syndrome, lupus, hypoglycemia, renal transplant,
depression, and schizophrenia; see Tombaugh, 2006 for review).
The typical administration of the PASAT involves the presentation
of a series of single digit numbers where the two most recent digits
must be summed. For example, if the digits ‘5’, ‘3’ and ‘2’ were presented, the participant would respond with the correct sums, which
16
T.D. Parsons, C.G. Courtney / Journal of Neuroscience Methods 222 (2014) 15–23
are ‘8’ and then ‘5’. Participants are required to respond prior to
the presentation of the next digit for a response to be scored as
correct.
While studies have found evidence for the utility of the PASAT
for neuropsychological assessment of multiple sclerosis (Kujala
et al., 1995; Benedict et al., 2002), Parkinson’s disease (Dujardin
et al., 2007), epilepsy (Prevey et al., 1998), systemic lupus erythematosus (Shucard et al., 2004), attention deficit hyperactivity
disorder (Schweitzer et al., 2000), and traumatic brain injury (O’Jile
et al., 2006), a number of potential normative considerations have
emerged as possible confounds. Studies have found increasing age
to be negatively related to PASAT performance (Brittain et al., 1991;
Roman et al., 1991; Diehr et al., 1998, 2003; Wiens et al., 1997),
especially after age 50 (Roman et al., 1991). A general exception
to this trend can be found in studies that involve young adults
(Wingenfeld et al., 1999). Clinically meaningful sex differences in
the PASAT performance have not been found (Brittain et al., 1991;
Wiens et al., 1997; Wingenfeld et al., 1999; Diehr et al., 2003).
While some studies (Brittain et al., 1991; Wiens et al., 1997) have
found the effects of education to be marginal, Diehr et al. (1998)
found age, education, and ethnicity to be significant predictors
of PASAT performance. A further issue for the PASAT has been
the use of number lists and the resulting impact of math ability
(Chronicle and MacGregor, 1998; Gronwall and Wrightson, 1981;
Hiscock et al., 1998; Royan et al., 2004; Tombaugh et al., 2004).
Royan et al. (2004) and Tombaugh et al. (2004) found that scores
on a math test accounted for a greater amount of variance for
more difficult lists than for an easier list. A potential solution to
this issue is to reduce the complexity of the answers (Johnson
et al., 1988) and/or slow the inter-stimulus interval (ISI)s. For
example, a modified version of the PASAT has been incorporated
into multiple sclerosis (MS)test batteries which uses only the 2.0 s
and/or 3.0 s trials ( Rudick et al., 1997; Rao, 1990;Benedict et al.,
2002).
In addition to the potential demographic effects, a number of
neuropsychologists have criticized the PASAT’s tendency to elevate levels of stress in participants (Aupperle et al., 2002; Deary
et al., 1994; Diehr et al., 2003; Holdwick and Wingenfeld, 1999;
Hugenholtz et al., 1988; Iverson et al., 2000; Kinsella, 1998; Roman
et al., 1991). The negative impact of the PASAT on mood and affect
has led neuropsychologists to advise that the PASAT generally
should not be administered until the end of a neuropsychology battery (Holdwick and Wingenfeld, 1999; Hugenholtz et al.,
1988) and should not be administered to participants who are
highly anxious or experiencing post-traumatic stress symptoms
specifically (Kinsella, 1998; Roman et al., 1991). The robust stress
response elicited by the PASAT has even led to its use as a laboratory inducer of psychological stress and fatigue (Johnson et al.,
1997). For example, Lejuez et al. (2003) developed a modified computer version of the PASAT (PASAT-C) that used three presentation
rates (i.e., 3.0 s, 1.5 s and 1.0 s) to elicit graded levels of psychological stress. Stress was measured using (1) subjective ratings
on a visual analog scale (0–100); and (2) objective psychophysiological measurements of skin conductance response. Results
revealed elevations over baseline for both subjective and objective
measures.
Given the above, modified versions of the traditional PASAT
have emerged. Promise has been found in the use of short
forms and Adjusting-Paced Serial Addition Test (Adjusting-PSAT,
Tombaugh, 1999) versions for reducing discomfort and stress
effects by shortening the task. Another option that may reduce
psychological stress is the use of virtual gaming environments
that offer an advanced computer interface that allows participants
to become immersed within a computer-generated simulation.
Potential virtual gaming environment use in assessment and rehabilitation of human cognitive processes is becoming recognized as
technology advances. Virtual gaming environments that are
absorbing and interesting have been found to have a valuable
effect on mood, health, and recovery (Prins et al., 2011). According
to Gamberini et al. (2008) virtual gaming environments provide
alternative realities in which users’ stress levels may be reduced
as they step back from the real world. In fact, virtual gaming
environments have been found to be helpful for psychotherapeutic assessment and treatment of stress reactions due to specific
phobias and post-traumatic stress disorder (Parsons and Rizzo,
2008a). Research has shown that virtual gaming environments
have the potential to lowering cortisol levels (Dandeneau et al.,
2007).
Since virtual gaming environments allow for precise presentation and control of dynamic perceptual stimuli, they may have
promise for providing ecologically valid assessments that combine the veridical control and rigor of laboratory measures with
a verisimilitude that reflects real life situations (McGeorge et al.,
2001; Renison et al., 2012). Additionally, the enhanced computation power allows for a range of the accurate recording of
neurobehavioral responses in a perceptual environmental that systematically presents complex stimuli. Such simulation technology
appears to be distinctively suited for the development of ecologically valid assessments, in which stimuli are presented in a
consistent and precise manner. As a result, participants are able
to manipulate three dimensional objects in a virtual environment
that proffers a range of potential task demands (Schultheis et al.,
2002).
A number of virtual environment-based neuropsychological
assessments have been developed and validated. Examples of virtual reality-based cognitive assessments include: attention (Law
et al., 2006; Parsons et al., 2007) spatial abilities (Beck et al.,
2010; Moffat, 2009), episodic memory (Plancher et al., 2012),
retrospective memory (Parsons and Rizzo, 2008b), prospective
memory (Knight and Titov, 2009), spatial memory (Astur et al.,
2004; Goodrich-Hunsaker and Hopkins, 2010); and executive functions (Armstrong et al., 2013; Henry et al., 2012; Jovanovski
et al., 2012). The Virtual Reality PASAT (VR-PASAT) joins these
projects and focuses on refined analysis of neurocognitive testing
using a virtual gaming environment to assess attention processing
in the context of traversing a virtual city. Specifically, the primary aim of the present study was an initial examination of
the convergent and divergent validity of the VR-PASAT using
the methodology provided by the multitrait–multimethod matrix
(Campbell and Fiske, 1959). The use of this matrix approach
with multiple neurocognitive measures allows for the simultaneous investigation of convergent validity (i.e., extent to which
different neurocognitive measures of attentional processing are
related) and discriminant validity (i.e., extent to which neurocognitive measures of domains other than attentional processing are
unrelated). The use of the multitrait–multimethod matrix gave
us the advantage of being able to examine method variance (i.e.,
degree to which scales are correlated because they use the same
method of measurement rather than because they share valid trait
variance).
In our assessment of convergent validity, we hypothesized
(1) that the performance on the VR-PASAT would correlate significantly with performance on traditional neuropsychological
measures of attentional processing. Given the addition of being
immersed in a virtual gaming environment, we hypothesized (2)
that the correlations would be moderate rather than high; and (3)
participants would endorse less discomfort and stress on the VRPASAT when compared to the PASAT 200 (see Diehr et al., 1998). In
our assessment of discriminant validity, we hypothesized (4) that
correlations between the VR-PASAT and traditional neuropsychological measure of domains other than attentional processing would
not be statistically significant.
T.D. Parsons, C.G. Courtney / Journal of Neuroscience Methods 222 (2014) 15–23
1. Methods
We acquired data on the implementation of a VR-based PASAT
(i.e., VR-PASAT) in a college aged sample that also received a
traditional (paper-and-pencil; computerized) neuropsychological
battery. We aimed to assess the psychometric properties of the
VR and paper-and-pencil measures. Hence, scores were correlated
with demographic and other performance measures administered.
Standard correlational analyses using a brief demographic survey
and standardized (paper-and-pencil; computerized) neurocognitive tests aided our initial assessment of both the concurrent and
divergent validity properties of this form of assessment. This study
with college students expands considerably upon a previously published initial validation with active duty military (Parsons et al.,
2012).
1.1. Participants
The University of Southern California’s Institutional Review
Board approved the study. A total of 50 college-aged subjects participated in the study. Given that some research has shown age and
education to be significant predictors of PASAT performance (Diehr
et al., 1998), the age range of participants was 19–34 years of age
(age: M = 25.58; SD = 4.25) and the education range of participants
was 12–19 years (education: M = 13.82; SD = 1.93). Participants
were 75% male. No significant differences were found for age, gender, education, self-reported symptoms of depression, or computer
familiarity. After informed consent was obtained, basic demographic information, participants responded to questions designed
to measure computer experience and usage activities: how frequently participants use a computer (e.g., “How many hours per
week do you spend on the computer?”); their perceived level of
computer skill on a Likert scale (1 – not at all to 5 – very skilled); e.g.,
“How many hours per week do you spend playing video games?”;
and what type of games they play (e.g., role-playing, strategy,
sports, etc.). Participants were also given a medical health history
form to assess the presence of any mental or physical disorders that
may have hindered their performance. All subjects were free of histories of neurologic disease or injury, psychiatric illness including
substance abuse or dependence, or self-reported specific developmental disorders. No participants were excluded for responses
given on this form.
1.2. Design and measures
Experimental sessions took place over a 2-hour period. Participants completed the VR PASAT as part of a neuropsychological
battery administered under standard conditions. In addition to a
standardized traditional (paper-and-pencil; computerized) neuropsychological battery, participants completed two versions of
the PASAT: (a) the PASAT 200 digitally recorded auditory presentation of the PASAT (Diehr et al., 1998); and (b) the VR PASAT.
Testing occurred in a quiet, climate controlled environment in a
university-owned computer lab. The order in which the various
PASAT tests were administered was counterbalanced across subjects. Participants completed the simulator sickness questionnaire,
which includes a pre- and post-VR exposure symptom checklist
(Kennedy et al., 1992). Participants were asked to rate their preference for assessment: “From the following options, please place a
check mark next to your most preferred mode of assessment: (1)
audio recording where you had to add numbers together; (2) the
computerized assessments where you watched stimuli on a monitor; or (3) the virtual reality assessment where you added numbers
together while traveling through the virtual city.”
17
1.2.1. Traditional paper-and-pencil measures
Paced Auditory Serial Addition Test (PASAT-200): Each participant completed the PASAT-200 (Diehr et al., 1998) in the following
manner: a digital recording presenting auditory stimuli (i.e., numbers) of four sequences of 50 digits was used (maximum possible
score for each sequence was 49). The four sequences had presentation rates of 3.0, 2.4, 2.0, and 1.6 s per digit, respectively. Each
sequence of 50 digits was unique. The digital recording had approximately a 15-s delay between each sequence. The PASAT-200 (Levin
et al., 1982; Diehr et al., 1998) was chosen over the original version PASAT-244 version (Gronwall, 1977; Gronwall and Sampson,
1974). The “PASAT-200” is a revised 200-item version that was
introduced by Levin et al. (1982) and extended by Diehr et al. (1998).
While both versions follow the typical administration (four series
of numbers presented at increasing speed), during the PASAT-244
the same series of 61 pseudo-random numbers is presented four
times. Brittain et al. (1991) suggested that this increases practice
effects decreases the usability of the PASAT-244 for repeat testing.
Contrariwise, the PASAT-200 uses four series of 50 digits and each
series is unique.
D-KEFS (Color–Word Interference Test): Each participant was presented with the following stimuli from the D-KEFS Color–Word
Interference Test (Delis et al., 1997): (a) “color naming” card with
50 colored blocks; (b) “word reading” stimulus card with 50 color
words printed in black ink; (c) “color–word inhibition” card with 50
color names printed in a discrepant ink color; and (d) “color–word
inhibition/switching” card, in which the subject performed the
interference task if and only if the words (50 total words) did not
have a box drawn around them. We followed the D-KEFS manual’s
prescribed approach to administration and the D-KEFS’s “Scoring
Assistant” software for scoring of the Color–Word Interference Test.
1.2.2. Automated Neuropsychological Assessment Metrics
(ANAM4)
The ANAM4 is a library of tests that have been recently normed
from over 107,500 participants ranging from 17 to 65 years of age
(Vincent et al., 2012). The ANAM4 TBI provides automated measures of fundamental neurocognitive functions including response
speed, attention/concentration, immediate and delayed memory,
spatial processing, and decision-processing speed and efficiency
(ANAM, 2007). We followed the ANAM (2007) manual’s approach
to administration and scoring of the ANAM tests. Brief descriptions
of each test follow (see also Vincent et al., 2012):
Code Substitution—Learning Phase: This measure assesses learning and immediate memory of symbol-digit pairs. The participant
presses designated buttons to indicate whether the pair in question represents a correct or an incorrect mapping. In the “Learning
Phase”, the defined pairs are presented on the screen simultaneously with the symbol-digit stimulus in question.
Code Substitution—Delayed Memory: This measure assesses
memory for symbol-digit pairs from the set of previously memorized (Code Substitution—Learning Phase) symbol-digit pairs. The
participant presses designated buttons to indicate whether they
remember the pair from the “Learning Phase”. The same comparison stimuli used in the Code Substitution-Learning phase are again
presented individually but without the target cue.
Procedural Reaction Time: This task measures attention
and reaction time by presented a number (e.g., 2, 3, 4,
or 5) on the monitor display using a large dot matrix.
The participant is required to press designated buttons to
indicate whether the number presented is a “low” number (2 or
3) or a “high” number (4 or 5).
Mathematical Processing: This measure assesses working memory and the participant’s ability to solve arithmetic problems
that involve three single-digit numbers and two operators (e.g.,
“4 − 1 + 2 =”). The participant presses designated buttons to
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T.D. Parsons, C.G. Courtney / Journal of Neuroscience Methods 222 (2014) 15–23
indicate whether the answer to the problem is “less than 5” or
“greater than 5”.
Matching to Sample: This test assesses visuo-spatial abilities. The
participant views a pattern produced by eight shaded cells in a 4 × 4
sample grid. The sample is then removed and 2 comparison patterns are displayed side by side. One grid is identical to the sample
grid and the other grid differs by one shaded cell. The participant is
required to press a designated button to select the grid that matches
the sample.
Stroop Task: This task requires the subject to press a computer
key labeled red, green, or blue to identify each color stimulus presented. There are three possible blocks of 50 trials for this test. In
the first block, the words RED, GREEN, and BLUE are presented individually in black type on the display. The participant is instructed
to read each word aloud and to press a corresponding key for each
word (“red” = 1; “green” = 2; and “blue” = 3). In the second block, a
series of XXXXs is presented on the display in one of three colors (red XXXXs, green XXXXs, or blue XXXXs). The participant is
instructed to say the color of the XXXXs aloud and to press the
corresponding key based on color. In the third block, a series of
individual words (“RED,” “GREEN,” or “BLUE”) are presented in a
color that does not match the name of the color depicted by the
word. The participant is instructed to say the color of the word aloud
rather than reading the actual word and to press the response key
assigned to that color.
1.2.3. Virtual Reality Paced Auditory Serial Addition Test
The VR-PASAT is a measure of cognitive function that aims
specifically to assess auditory information processing speed and
flexibility, as well as calculation ability. Two monitors were used:
(a) one for displaying the Launcher application, which is used
by the examiner administering the test; and (b) another for displaying the participant’s view of the virtual environment in the
head-mounted display (HMD; eMagin Z800 with an InterSense
InteriaCube 2+ attached for tracking). To increase the potential
for sensory immersion, a tactile transducer was built using a
three-foot-square platform with six Aura bass shaker speakers
(AST-2B-04, 50W Bass Shaker) attached. The tactile transducer was
powered by a Sherwood RX-4105 amplifier with 100 watts per
channel × 2 in stereo mode.
Animation software was utilized for development of the virtual city environment. The environments were rendered in real
time using a graphics engine with a fully customizable rendering pipeline, including vertex and pixel shaders, shadows, bump
maps, and screen space geometric primitives. A MATLAB scoring
program (Wu et al., 2010) and human–computer interface (Clinical
Neuropsychology and Simulation Interface; CNS-I) was employed
for data acquisition (Wu et al., 2013). The CNS-I also allowed for
key events in the environment to be logged and time stamped with
millisecond temporal accuracy.
The VR-PASAT is presented in a Virtual City. Single digits are
first aurally presented every 3 s (3 PASAT) and then every 2 s (2
PASAT). The participant must add each new digit to the one immediately prior to it. The test result is the number of correct sums given
(out of 49 possible). The participant follows a guide through the 5
zones of the city and does not stop at any point during the walkthrough scenario. Navigation through the scenario uses a common
USB Logitech game pad device. While the participant is following
the guide, s/he hears background chatter and a number presented
at varying intervals. Instructions for the VR PASAT task can be found
in Appendix A. Each section of the VR-PASAT has a maximum of 49
correct answers (i.e., 50 digits are presented for each part). Participant responses are recorded via the computer’s sound board and
by the examiner. Metrics include: the number of correct responses
per presentation rate; number of non-responses; number of errors;
number of suppression failures (i.e., adding to the sum of the last
addition rather than to the last number heard); number of consecutive correct responses; longest series of correct responses; and
reaction time data.
1.3. Data analytic considerations
After completion of each assessment, examiners compiled
scores of the number of correct responses for each trial (e.g., maximum = 49); and the total number of correct responses summed
over all trials (composite score). In addition to these scores, the
examiner calculated the average time per correct response (dividing total trial time by number correct for each trial and averaging
the results). Further, each trial duration was calculated by multiplying the duration of the ISI by 60 (e.g., 2.0 × 60 s = 120 s).
In addition to the aforementioned PASAT scoring procedures,
examiners also looked at percent correct, and latency of responding.
The calculation of the percentage of correct responses provides an
alternate approach that may be helpful for cross-study comparison.
An important development in PASAT administration (included in
the VR-PASAT) is computer-automation that permits measurement
of the speed at which a participant responds as well as recording the
number of correct responses (Tombaugh, 1999; Wingenfeld et al.,
1999).
Feature extraction and optimal response classification for the
VR-PASAT responses were examined using a MATLAB scoring program (i.e., CNS-I) adapted specifically for this study (Wu et al.,
2013). This allowed for assessment of performance validity (suboptimal effort) and screening for outliers to establish data integrity:
(a) identification of outliers as observations exceeding three
standard deviations from the median reaction time; (b) exclusion
of observations that are in both the top 1% in speed and simultaneously in the bottom 1% of accuracy; and (c) filtering and pattern
recognition assessment for establishing feature sets using support
vector machine classifiers.
2. Results
2.1. Comparison of PASAT modalities
Table 1 presents the descriptives for VR-PASAT and PASAT 200
response times, and percentage correct for performance during
3.0 s trials, 2.0 s trials, and composite scores. Given that all variables
were found to be normally distributed, parametric Pearson r correlations were utilized for relational analyses, with attendant results
for comparison between PASAT modalities depicted in Table 2. As
indicated, there is a significant relationship among all PASAT scores
for VR-PASAT and PASAT 200 modalities. All participants stated that
they preferred the VR-PASAT modality over that of the PASAT 200.
2.2. Comparison of VR-PASAT to traditional neuropsychological
measures
Table 3 presents descriptives for standardized neuropsychological tests. Again, given that all variables were found to be
normally distributed, parametric Pearson r correlations were utilized for relational analyses, with attendant results for comparison
of VR-RASAT with traditional neuropsychological measures found
in Table 4. There is not a significant relationship between age or
education and VR-PASAT scores. Convergent validity was evident
via modest correlations noted among comparisons of VR-PASAT
performance: (1) paper-and-pencil stroop (DKEFS Stroop) Inhibition was correlated with both VR-PASAT 2.0 s and 3.0 s; (2)
DKEFS Stroop Inhibition\Switching scores were correlated with
VR-PASAT 3.0 s, but not VR-PASAT 2.0 s; (3) ANAM computerautomated Stroop scores, Mathematical Processing, and Procedural
T.D. Parsons, C.G. Courtney / Journal of Neuroscience Methods 222 (2014) 15–23
19
Table 1
Descriptives for PASAT modalities.
3s
VR-PASAT
# Correct
RT
%
PASAT 200
# Correct
RT
%
2s
Composite
Mean
SD
SE
Var
Mean
SD
SE
Var
Mean
SD
SE
Var
39.62
4.91
.66
10.44
1.48
.17
1.48
.21
.02
108.89
2.18
.03
32.96
4.12
.55
10.79
1.64
.18
1.53
.23
.03
116.49
2.69
.03
72.58
4.46
.60
18.95
1.33
.16
2.68
.19
.02
359.27
1.77
.02
39.22
4.13
.78
10.05
1.23
.20
1.42
.17
.03
100.99
1.52
.04
33.56
3.36
.67
10.36
1.38
.21
1.47
.20
.03
107.31
1.91
.04
72.78
3.71
.73
18.58
1.14
.19
2.63
.16
.03
345.07
1.29
.03
Note: For all analyses, N = 50. SE = Standard Error; SD = Standard Deviation; Var = Variance.
Table 2
Pearson’s r correlation coefficients between VR PASAT Scores and PASAT 200.
VR-PASAT 3.0 s
PASAT 200 3.0 s
RT
%
PASAT 200 2.0 s
RT
%
PASAT 200 composite
RT
%
VR-PASAT 2.0 s
VR-PASAT composite
RT
%
RT
%
RT
%
.970**
−.952**
−.936**
.967**
.571**
−.577**
−.579**
.605**
.860**
−.856**
−.845**
.877**
.594**
−.622**
−.591**
.633**
.911**
−.858**
−.811**
.923**
.852**
−.852**
−.788**
.874**
.849**
−.862**
−.831**
.876**
.822**
−.791**
−.786**
.842**
.948**
−.938**
−.905**
.961**
Note: For all analyses, N = 50. RT = response time; % = percentage; 3.0 s = 3 s; and 2.0 = 2 s.
* Correlation is significant at the 0.05 level (2-tailed).
**
Correlation is significant at the 0.01 level (2-tailed).
Table 3
Descriptives for neuropsychological tests.
Mean
D-KEFS Color–Word Interference Test
Inhibition
Inhibition/Switching
Automated Neuropsychological Assessment Metrics
Procedural Reaction Time
Code Substitution—Learning
Code Substitution—Delayed Memory
Mathematical Processing
Matching to Sample
Stroop
SD
SE
49.60
60.52
12.96
13.77
1.83
1.95
571.62
1038.76
1208.82
2778.60
1590.04
831.19
73.14
215.02
344.42
568.69
418.29
206.80
10.34
30.41
48.71
80.43
59.16
29.25
Var
168.08
189.64
5349.63
46,233.90
118,627.86
323,409.88
174,965.71
42,767.12
Note: For all analyses, N = 50. SE = Standard Error; SD = Standard Deviation; Var = Variance.
Table 4
Pearson’s r correlation coefficients between VR PASAT Scores and Neuropsychology Tests.
VR-PASAT 3 s
RT
Demographics
Age
Education
D-KEFS Color–Word Interference Test
Inhibition
Inhibition/Switching
Automated Neuropsychological Assessment Metrics
Stroop
Mathematical Processing
Procedural Reaction Time
Code Substitution—Learning
Code Substitution—Delayed Memory
Matching to Sample
−.158
−.223
VR-PASAT 2 s
%
.151
.218
VR-PASAT composite
RT
%
RT
−.229
.022
.210
−.139
−.201
−.101
%
.203
.041
.431*
.356*
−.421**
−.332*
.530**
.241
−.492**
−.266
.566**
.367**
−.512**
−.334*
.345*
.406**
.432**
−.071
.037
.128
−.347*
−.440**
−.387**
.082
−.060
−.138
.386**
.526**
.278
.041
.098
.146
−.412**
−.516**
−.362**
−.074
−.183
−.136
.436**
.541**
.420**
.003
.082
.184
−.426**
−.536**
−.419**
.003
−.137
−.153
Note: For all analyses, N = 50. RT = response time; % = percentage.
*
Correlation is significant at the 0.05 level (2-tailed).
**
Correlation is significant at the 0.01 level (2-tailed).
20
T.D. Parsons, C.G. Courtney / Journal of Neuroscience Methods 222 (2014) 15–23
Reaction time were correlated with VR-PASAT at all levels. Divergent validity was evident via a lack of significant correlation
among levels (2.0 s and 3.0 s) of VR-PASAT and measures of
learning (Code Substitution—Learning Phase) and memory (Code
Substitution—Recall Phase). Further, there was no correlation
among VR-PASAT levels (2.0 s and 3.0 s trials) and a measure of
visuo-spatial abilities (Matching to Sample).
2.3. Predictive relations between VR-PASAT and traditional
measures of attentional processing
In order to further clarify the relationships between VR-PASAT
and the attentional processing measures, two step-wise multiple regression analyses were conducted with five attentional
processing measures (the DKEFS Stroop inhibition and inhibition/switching, and the ANAM Stroop, Mathematical Processing,
and Procedural Reaction Time) and education serving as predictor
variables and VR-PASAT 3.0 s Trial (first stepwise) and VR-PASAT
2.0 s Trial (second stepwise)serving as the criterion variables.
Results of the first stepwise yielded a significant regression equation that accounted for 25.5% of the variance in VR-PASAT 3.0 s
Trial scores (R2 = 0.255), F (2,47) = 9.37, P < 0.001. ANAM Procedural
Reaction Time was the first variable to enter the equation, accounting for approximately 19% of the variance in VR-PASAT 3.0 s Trial
scores (R2 = 0.186), followed by Mathematical Processing which
accounted for an additional 10% of the variance in VR-PASAT 3.0 s
scores (R2 change = 0.099). Results of the second stepwise yielded a
significant regression equation that accounted for 41% of the variance in VR-PASAT 2.0 s Trial scores (R2 = 0.408), F (2,47) = 16.16,
P < 0.001. DKEFS Stroop Inhibition was the first variable to enter
the equation, accounting for approximately 28% of the variance in
VR-PASAT 2.0 s Trial scores (R2 = 0.280), followed by Mathematical
Processing which accounted for an additional 13% of the variance
in VR-PASAT 2.0 s scores (R2 change = 0.127). The assumptions of
multiple regression were met as indicated by observation of standardized residual plots and by results of a Durbin–Watson test that
indicated independence of errors.
3. Discussion
This study provides preliminary information on the VR-PASAT’s
convergent and divergent validity for a college age population.
Comparisons among scores for traditional approaches to PASAT
assessment (PASAT 200) and a virtual reality instantiation (VRPASAT) revealed moderate to large correlations for all comparisons.
Further, self-report of “likability” revealed a unanimous preference for the virtual reality-based PASAT. In addition to findings
relative to direct comparisons of VR-PASAT to traditional the
PASAT modality, convergent and discriminant validity were evaluated using neuropsychological tests chosen a priori, according
to the multitrait–multimethod matrix approach. The VR-PASAT
was significantly related to measures of attentional processing
and executive functioning. Further, following expectation, VRPASAT scores did not correlate with measures of learning, memory,
and visuospatial processing drawn from the traditional neuropsychological test battery. Together, these findings suggest that the
VR-PASAT assesses a construct that is similar to those measured by
the other attentional processing tests (e.g., Stroop tasks; Spikman
et al., 2001; Sherman et al., 1997) in this study.
Although the VR-PASAT shares common variance with other
attentional processing tests, it appears to also measure a component of attentional processing not measured, or measured to
a lesser extent, by more traditional tasks. Such an hypothesis is
supported by the rather modest relationships observed between
VR-PASAT and the attentional processing tests utilized in the
present study. When we used traditional attentional processing
measures and education as predictors of the 3.0 s VR-PASAT Trial,
we found that only the ANAM Procedural Reaction Time and Mathematical Processings cores were significant predictors. On the more
difficult 2.0 s VR-PASAT Trial, DKEFS Stroop Inhibition was the
most predictive, whereas Mathematical Processing accounted for
a smaller portion of variance in VR-PASAT 2.0 s Trial scores not
tapped by DKEFS Stroop Inhibition.
Some researchers consider the PASAT to be multifactorial
because it requires the successful completion of multiple neurocognitive functions. For example, Gronwall and Sampson (1974)
stated that the various speeded presentations of the PASAT reflect
Broadbent (1958) “channel capacity,” which refers to the rate at
which information transmission occurs in the nervous system.
According to Cicerone (1997), the PASAT appears to have two components: (1) attentional processing required to complete the PASAT
tasks; and (2) speed of information processing. The different findings for the 3.0 s VR-PASAT and 2.0 s VR-PASAT trials may reflect
findings from studies that have characterized the PASAT as tapping into different types of cognitive processes. Performance on the
VR-PASAT 3.0 s trials appears to reflect findings that (1) performance on the PASAT is affected by math ability (Chronicle and
MacGregor, 1998; Gronwall and Wrightson, 1981; Hiscock et al.,
1998; Royan et al., 2004; Sherman et al., 1997; Tombaugh et al.,
2004); and (2) processing speed (Demaree et al., 1999; Madigan
et al., 2000; Ponsford and Kinsella, 1992). Performance on the VRPASAT 2.0 seems to reflect attentional processing and executive
functioning. This comports well with factor analytic studies that
have found that the 2.0 s presentation of the PASAT loaded on
attention/concentration factors variously referred to as “attention
switching” (Bate et al., 2001).
These findings are important to keep in mind when considering the VR-PASAT as an exclusive test for assessing attentional
processing. In certain populations (e.g., multiple sclerosis patients),
the 3.0 s ISI may be preferred rather than the 2.0 s ISIs. This affirms
the choice to employ the 3.0 s and 2.0 s in the Brief Repeatable Battery of Neuropsychological Tests for multiple sclerosis (Rao, 1990)
and the addition of a 3.0 s ISI after omitting the 1.2 s trial in studying the neuropsychological effects of HIV infection (Heaton et al.,
1995). Further, the finding that Mathematical Processing was predictive in both the 3.0 s and 2.0 s VR-PASAT trials reflects a need to
make judicious decisions relative to the participant’s mathematical
abilities (Strauss et al., 1994).
The use of the multitrait–multimethod analyses allowed us
to examine the extent of convergent and divergent validity.
Accordingly, we concluded that the VR-PASAT had appropriate
levels of convergent and divergent validity in that the degree
to which convergent validity coefficients (assessing attentional
processing domain) derived from the VR-PASAT 3.0 s and 2.0 s
trial scores and the traditional neuropsychological measures of
attentional processing were larger than correlations of different
measures assessing domains other than attentional processing
within the same array of measures. Evidence for discriminant validity was indicated in that correlations of different scales assessed
using different measures were lower than the convergent validity
coefficients. The presence of significant relations among VR-PASAT
scores and attentional processing measures, as well as the lack
of association between VR-PASAT and the learning, memory, and
visuospatial processing measures offers further support to the purported sensitivity of the VR-PASAT as an attentional processing
measure.
Recent research indicates that nonclinical, undergraduate
research participants in a “neuropsychological experiment” may
put forth suboptimal effort (An et al., 2012). For the VR-PASAT, we
examine performance using scoring algorithms to screen for outliers and assess data integrity (Wu et al., 2013). It is important to
T.D. Parsons, C.G. Courtney / Journal of Neuroscience Methods 222 (2014) 15–23
note that the data are not free of potential confounds due to poor
effort. Screening was done at the time of testing and also during
the data analysis process to eliminate obvious poor effort, but data
may still contain some individuals who provided less than optimal
effort. This situation is true for most normative neuropsychological data and particularly true for computerized testing given the
reduced interaction with the examiner.
Our findings should be understood in the context of some limitations. These findings are based on a fairly small sample size of
college aged participants. As a necessary next step, the reliability
and validity of the test needs to be established using a larger sample
of participants across the lifespan to ensure that the current findings are not an anomaly due to sample size or age cohort. While
self-report of “likability” revealed a unanimous preference for the
virtual reality-based PASAT, future studies should incorporate a
more fully developed questionnaire that taps into multiple aspects
of participant experience and preference for paper-and-pencil,
two-dimensional computer automations of traditional measures;
and three-dimensional virtual gaming environment adaptations.
Given the fact that the study sample was made up of college age
students, the novelty of the high tech atmosphere may account for
the preference.
Additionally, as indicated previously, the diagnostic utility of
this VR-PASAT assessment tool must be determined. The ability of
the VR-PASAT to accurately classify participants into attentional
processing impaired and nonimpaired groups based on carefully
established critical values must be evaluated. This will involve
the generation of specific cut-off points for classifying a positive
(attentional processing impaired likely) or negative (attentional
processing impaired unlikely) finding. The VR-PASAT’s prediction
of attentional processing impairment must be evaluated by the
performance indices of sensitivity, specificity, predictive value of
a positive test, and predictive value of a negative test. Even though
reliability is considered to be a unique asset of testing in computergenerated VEs, issues of test–retest reliability must be addressed.
Our goal was to conduct an initial pilot study to validate the
VR-PASAT through the use of a standard neuropsychological battery for the assessment of nonclinical college age participants. We
believe that this goal was met. We recognize, however, that the
current findings are only a first step in the development of this
tool. Many more steps are necessary to continue the process of
test development and to fully establish the VR-PASAT as a measure
that contributes to existing assessment procedures for the diagnosis of attentional processing decline across the lifespan. Although
the VR-PASAT as a measure must be fully validated, current findings
provide preliminary data regarding the convergent and divergent validity of the VE as an attentional processing measure.
The VR-PASAT was correlated with widely accepted assessment
tools. Nevertheless, the fairly small sample size in a college age
cohort requires that the reliability and validity of the VR-PASAT
be established using a larger sample of well-matched participants
across the lifespan. This will ensure that current findings are not
a sample size or cohort-related anomaly. Finally, the ability of
the VR-PASAT to accurately classify participants not involved in
the initial validation study must be examined for cross-validation
purposes.
Appendix A. VR-PASAT
The Virtual Reality Paced Auditory Serial Addition Test (VRPASAT) is a measure of cognitive function that specifically assesses
auditory information processing speed and flexibility, as well
as calculation ability. The VR-PASAT is presented in a Virtual
City. The participant follows a guide through 5 zones of the Virtual City. Navigation through the scenario uses a common USB
21
Logitech game pad device. While the participant is following
the guide, s/he will hear background chatter and a number presented at varying intervals. Single digits are presented either every
3.0 s (3 PASAT) or every 2.0 s (2 PASAT) and the participant
must add each new digit to the one immediately prior to it.
The test result is the number of correct sums given (out of 49
possible).
ADMINISTRATION
Examiners are to verify that they have the correct Record Form
(Form A) before they start reading the instructions for the 3
Practice Trial to the participant.
PASAT-3 Practice Trials
For Part 1 (stimuli every 3 ) the examinee states,
“In the following scenario, as you follow the sergeant through the
city, you are going to hear radio chatter and a series of single digit
numbers that will be presented at the rate of one every 3 seconds.
Listen for the first two numbers, add them up, and tell me your
answer. When you hear the next number, add it to the one you
heard on the radio right before it. Continue to add the next number
to each preceding one. Remember, you are not being asked to give
me a running total, but rather the sum of the last two numbers that
were heard from the radio.”
Then the examinee gives the following example:
“For example, if the first two numbers were ‘5’ and ‘7,’ you would
say ‘12.’ If the next number were ‘3,’ you would say ‘10.’ Then if the
next number were ‘2,’ you would say ‘5.”’
If the participant is having difficulty understanding these
instructions, the examiner writes 5, 7, 3, and 2 on a sheet of paper
and repeat the instructions, demonstrating how the task is done.
The examiner then says,
“This is a challenging task. If you lose your place, just jump right
back in – listen for two numbers in a row and add them up and
keep going. There are some practice items. Let’s try those first.”
The examiner then says the sample items, stopping after the
last practice item. The examiner repeats the practice items, if necessary, until the participant understands the instructions (up to
three times). The examiner always administers at least one practice
trial before administering the actual test. If the participant begins
to give a running total, the examiner stops the practice immediately and explain the task again, emphasizing that he/she is not to
give a running total. The examiner then starts the practice items
again from the beginning. If the participant begins adding each
number to the number two previous to it, the examiner stops the
practice immediately—explaining the correct way to do the task,
and starts the practice items from the beginning. If the participant merely makes a math error, the computer continues with the
practice items. After two consecutive ‘no responses,’ the examiner
prompts him/her to resume by saying, “Jump back in with the next
two numbers you hear.”
The examiner administers the practice sequence a maximum of
three times. Record answers in the space provided on the back of
the PASAT Record Form.
PASAT-3
Once it is clear that the subject possesses sufficient understanding of the task, the examiner begins Part 1. Before starting Part 1,
the examiner reminds him/her:
“Remember, if you get lost, just jump back in because I can’t stop
the test once it has begun.”
The examiner discourages talking and oral calculations during the test; only the participant’s answers should be spoken out
loud. The participant may need prompting to continue the test if
she/he gets lost. After five consecutive ‘no responses’ the examiner
22
T.D. Parsons, C.G. Courtney / Journal of Neuroscience Methods 222 (2014) 15–23
redirects the participant quickly by saying, “Jump back in,” but do
not stop the scenario.
PASAT-2
Before Part 2 (stimuli every 2 ) the examiner says,
“Okay there is a second part to this exercise, identical to the first,
except that the numbers will come a little faster, one every 2
seconds.”
The examiner proceeds directly with the 2 administration.
Completing the PASAT Record Form
The examiner places a check next to all correct answers and
writes in any incorrect responses in the space provided. The examiner places a dash when no response was given. If the subject
corrects him/herself after giving a response, count the amended
answer as the response. The amended response is the one that will
be used in determining total correct, regardless of whether it was
the correct or incorrect response. The examiner slashes through the
old response and writes in ‘SC’ with a circle around it to indicate
that the participant self-corrected.
Each section of the VR-PASAT has a maximum of 49 correct
answers (i.e., 50 digits are presented for each part). Count the total
number correct (number of circled answers) for VR-PASAT-3 and
record on the VR-PASAT Record Form. Repeat the same scoring
procedure for VR-PASAT-2 .
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