Executive Dysfunctions in Schizophrenia: A Critical Review of Traditional, Ecological, and Virtual Reality Assessments
Executive Dysfunctions in Schizophrenia: A Critical Review of Traditional, Ecological, and Virtual Reality Assessments
Clinical Medicine
Review
Executive Dysfunctions in Schizophrenia: A Critical Review of
Traditional, Ecological, and Virtual Reality Assessments
Ernest Tyburski 1, * , Monika Mak 2 , Andrzej Sokołowski 3 , Anna Starkowska 4 , Ewa Karabanowicz 5 ,
Magdalena Kerestey 5 , Zofia Lebiecka 2 , Joanna Preś 2 , Leszek Sagan 6 , Jerzy Samochowiec 7
and Ashok S. Jansari 8
1 Institute of Psychology, SWPS University of Social Sciences and Humanities, 61-719 Poznań, Poland
2 Department of Health Psychology, Pomeranian Medical University in Szczecin, 71-457 Szczecin, Poland;
[email protected] (M.M.); [email protected] (Z.L.); [email protected] (J.P.)
3 Memory and Aging Center, Department of Neurology, UCSF Weill Institute for Neurosciences, University of
California, 675 Nelson Rising Lane, Suite 190, San Francisco, CA 94143, USA; [email protected]
4 Faculty of Psychology in Wrocław, SWPS University of Social Sciences and Humanities,
53-238 Wrocław, Poland; [email protected]
5 Institute of Psychology, University of Szczecin, 71-017 Szczecin, Poland; [email protected] (E.K.);
[email protected] (M.K.)
6 Department of Neurosurgery, Pomeranian Medical University in Szczecin, 71-252 Szczecin, Poland;
[email protected]
7 Department of Psychiatry, Pomeranian Medical University in Szczecin, 71-457 Szczecin, Poland;
[email protected]
Citation: Tyburski, E.; Mak, M.; 8 Department of Psychology, Goldsmiths, University of London, New Cross, London SE14 6NW, UK;
Sokołowski, A.; Starkowska, A.; [email protected]
Karabanowicz, E.; Kerestey, M.; * Correspondence: [email protected]; Tel.: +48-61-271-12-22
Lebiecka, Z.; Preś, J.; Sagan, L.;
Samochowiec, J.; et al. Executive Abstract: In recent years, interest has grown in measuring executive function in schizophrenia with
Dysfunctions in Schizophrenia: A ecological and virtual reality (VR) tools. However, there is a lack of critical analysis comparing those
Critical Review of Traditional, tools with traditional ones. This paper aims to characterize executive dysfunction in schizophrenia
Ecological, and Virtual Reality by comparing ecological and virtual reality assessments with traditional tools, and to describe the
Assessments. J. Clin. Med. 2021, 10,
neurobiological and psychopathological correlates. The analysis revealed that ecological and VR tests
2782. https://doi.org/10.3390/
have higher levels of verisimilitude and similar levels of veridicality compared to traditional tools. Both
jcm10132782
negative symptoms and disorganization correlate significantly with executive dysfunction as measured
by traditional tools, but their relationships with measures based on ecological and VR methods are still
Academic Editor: José
Gutiérrez-Maldonado
unclear. Although there is much research on brain correlates of executive impairments in schizophrenia
with traditional tools, it is uncertain if these results will be confirmed with the use of ecological and VR
Received: 10 May 2021 tools. In the diagnosis of executive dysfunction, it is important to use a variety of neuropsychological
Accepted: 18 June 2021 methods—especially those with confirmed ecological validity—to properly recognize the underlying
Published: 24 June 2021 characteristics of the observed deficits and to implement effective forms of therapy.
Publisher’s Note: MDPI stays neutral Keywords: virtual reality; schizophrenia; executive functions; cognitive functions; ecological validity;
with regard to jurisdictional claims in neuropsychology; psychopathological dimensions
published maps and institutional affil-
iations.
1. Introduction
Executive dysfunction, cognitive deficits, positive and negative symptoms, and disor-
Copyright: © 2021 by the authors. ganization are key psychopathological symptoms in schizophrenia; they are consequences
Licensee MDPI, Basel, Switzerland. of abnormalities in the structural and functional levels in the brain [1,2]. The cognitive
This article is an open access article deficits affect attention, verbal and episodic memory, and visuo-spatial processes [1,2]. It
distributed under the terms and
is worth noting that it has been claimed that executive dysfunction constitutes the most
conditions of the Creative Commons
specific set of neuropsychological symptoms in schizophrenia [3–5]. Although executive
Attribution (CC BY) license (https://
dysfunction is not included in the diagnostic criteria for schizophrenia in the Diagnostic
creativecommons.org/licenses/by/
and Statistical Manual of Mental Disorders-5th Edition (DSM-5) [6], the international group
4.0/).
of experts who authored the manual define them as separate domains of cognitive impair-
ments and indicate that they are important aspects of schizophrenia. Investigating the
nature of executive dysfunction is very important, especially due to the fact that they affect
as many as 1% of the general population, regardless of country or cultural background,
causing significant impairment in the social, professional, and family life of patients and
leading to profound disability [7–9].
Currently, there is ongoing debate as to whether distinct types of schizophrenia can
be linked with specific executive disorders [10,11]. Numerous authors point out the need
to analyze particular subtypes of the disorder separately (e.g., those with predominantly
positive or negative symptoms [12]). Due to the heterogeneity of schizophrenia symptoms,
it seems valid to distinguish more homogeneous groups of patients within this one condi-
tion (such as negative and positive syndromes). Carpenter, Heinrichs, and Wagman [13]
propose the category of Deficit Schizophrenia (DS)—a subtype of the disorder with pre-
dominantly primary negative symptoms, which are stable over time. Negative symptoms
include poverty of speech, social withdrawal, limited speech content, restricted affect, and
apathy [14]. Numerous reports have demonstrated the validity of the diagnosis of DS,
due to, among other things, variations in genotype distribution [15], functional and struc-
tural differences in the brain [16], and cognitive and executive function differences [17,18].
However, research on the occurrence of executive dysfunction in DS has yielded inconsis-
tent results. Some studies suggest that, compared to non-deficit patients (NDS; patients
without deficit psychopathological symptoms), those with DS manifest difficulties with
regards to cognitive inhibition, problem-solving, and verbal and non-verbal cognitive
flexibility [19,20]; however, other studies have failed to confirm these results (for a detailed
overview see: [21]).
One of the most important challenges in contemporary neuropsychology is the use
of innovative technological methods to diagnose and treat schizophrenia patients [22].
Moreover, it is of utmost importance to develop tools that contribute to understanding
and predicting patients’ behavior in real-life situations [23]. There are several systematic
reviews [24,25], several selective reviews, and one meta-analysis [26] about assessment
and treatment using VR in different clinical populations. Other papers explore VR in the
schizophrenia spectrum in the broad context of different cognitive functions [27–29]. How-
ever, none of these seem to offer an extensive analysis of executive dysfunction measured
by VR in schizophrenia. To our knowledge, no previous papers detail the complex charac-
teristics of and compare traditional, ecological, and VR tools. Despite the well-established
links between executive impairments measured by traditional tools and psychopathologi-
cal dimensions e.g., [30], links between measurement by ecological and VR tools and the
aforementioned dimensions have been severely neglected in systematic reviews. This is
all the more surprising as knowing these relationships helps us understand the nature
of schizophrenia and to organize interdisciplinary diagnostic and support systems for
patients [31]. Moreover, systematic reviews lack information about the relationships of
white matter integrity or functional changes in the brain with executive functions measured
by ecological and VR tools. Successfully finding biological markers would enable faster
diagnosis, earlier implementation of effective treatment, and improved quality of life [32].
Given these limitations and the paucity of comprehensive analyses in the available review
papers, we formulated the following objectives. The primary aim of this review was to
characterize executive dysfunction in schizophrenia in conditions resembling everyday
situations by comparing traditional, ecological, and VR tools in terms of the ecological
dimensions of verisimilitude and veridicality. Our secondary goal was to describe the
neurobiological and psychopathological correlates of that dysfunction.
approach [33]. It is commonly accepted, however, that they mediate between cognition
(information processing systems) and action (i.e., the performance of activities) [34]. The
theoretical background of executive functions can be traced back to Luria’s research [35].
He distinguished three functional systems in the human brain: (a) an arousal and attention
unit (limbic and reticular activation system); (b) a unit that receives, stores, and analyzes in-
formation (posterior neocortex); and (c) a unit that plans, organizes, and regulates behavior
and cognition (frontal lobes). In his approach, regulation is defined as the ability to change
one’s actions during the execution of a particular task, which often takes place with the
involvement of linguistic processes [36]. The capacity to contrast the outcomes of a given
behavior with its initial purpose is defined as control. Finding a solution to a problem
involves analyzing initial conditions, developing a specific plan (strategy), implementing
the relevant operations, and comparing the result with the initial data [37].
On the other hand, Lezak, Howieson, and Loring [38] propose that executive functions
form a comprehensive set of processes or mental abilities used in the execution of purposeful
actions, enabling one to adapt to new situations. Lezak [38] clinically describes executive
functions in terms of four main domains: volition, purposive action, effective performance,
and planning. The first stage involves a conscious, future-oriented decision or intention
to carry out a deliberate action. The next stage, planning, happens once the goal has been
set: a sequence of steps necessary to solve the problem or achieve the goal is identified.
Purposive action is the process of turning intentions and plans into a specific behavioral
act; this requires the monitoring and correction of one’s course of action as well as the
modulation of the tempo and intensity of one’s own reactions. Another important element
of executive functions is working memory, introduced by Baddeley [39], which consists of a
central executive, phonological loop, and visual-spatial sketchpad. Working memory is also
considered an aspect of executive functions in the model proposed by Diamond [40].
Following these important formulations, researchers currently understand executive
functions as the mental abilities responsible for, inter alia: (a) planning and organization,
(b) anticipation and focus of attention, (c) initiation of activity, (d) self-monitoring and
impulse control, (e) working memory, (f) mental flexibility and the ability to make use of
feedback, and (g) choosing effective strategies for problem-solving [41]. These functions
also constitute an executive process that designates mental resources and monitors, inhibits,
and controls other mental processes and behavioral reactions, thereby reinforcing better
adaptation to the external environment [42]. Depending on the dynamics of a situation,
they facilitate the adjustment of behavior and tailoring of reactions [34]. Cognitive and
behavioral control constitute two especially important executive domains [43,44]. Studies
have shown a factorial structure of executive functions in healthy individuals by ana-
lyzing multiple measures of executive performance. For instance, Testa, Bennett, and
Ponsford [45] performed a factor analysis of 19 neuropsychological tests on 200 healthy
people and differentiated six largely independent factors: set-shifting and interference man-
agement, prospective working memory, task analysis, strategy generation and regulation,
response inhibition, and self-monitoring and set-maintenance. However, Miyake et al. [46]
distinguished only three central executive domains (shifting, inhibition, and updating).
The authors suggested the relative independence of these functions but noted that they
share certain common characteristics.
It is uncertain whether the same factor structure would be found using different
ecological and VR tools, and more research on this topic is needed. Additionally, the
factor structure of executive functions identified in healthy populations may differ from
that of clinical populations (e.g., for schizophrenia patients, see: [19]). Despite different
theoretical models of executive functions and repeated factor analyses, there are still
inconsistencies in their definitions and number of components; hence, “executive functions”
can be considered as an umbrella term indicating a “wide range of cognitive processes and
behavioral competencies” [33].
J. Clin. Med. 2021, 10, 2782 4 of 26
integrity of the nerve fibers connecting these areas [62]. Other reports show that structural
abnormalities are present also in the cortical areas [63] and connections [64] of the DMN.
Finally, there are reports of structural abnormalities in the anterior cingulate and insula [65]
and the integrity of nerve fibers connecting the brain areas [66] that constitute the SN.
Reduced volume of the DLPFC and the ACC as well as reduced integrity of the cingu-
lum bundles (CB) in schizophrenia patients is linked to impaired ability to generate rules
and problems with abstract thinking [67–71]. Furthermore, reduced integrity of the frontal
portion of the CB [64,72] and the anterior limb of the internal capsule (ALIC) [62] has been
found to be linked to deficits in cognitive inhibition of dominant verbal responses. Other
reports have also shown that reduced integrity of the ALIC [73] and fornix [74] correlate
with impaired cognitive flexibility. However, some studies did not find a relationship
in patients with schizophrenia between executive functions and white matter integrity
in the superior longitudinal fasciculus, corpus callosum, anterior cingulum, and forceps
minor [75,76].
Figure 1. Tools for assessing executive functions in terms of their ecological validity level (verisimil-
itude and veridicality). Verisimilitude as a continuous dimension: stimuli and activities without
features of real-life—stimuli and activities with features of real-life. Veridicality as a continuous
dimension: lack of correlation of functional outcome and behavioral observation—correlation of
functional outcome and behavioral observation. CMPT = Computerized Meeting Preparation Task;
CST = Computerized Shopping Task; DS = Digit Span; DST = Digit Sequencing Test; EFPT = Ex-
ecutive Function Performance Test; LNST = Letter Number Sequencing Test; MET = Multiple Er-
rands Test; PDT = Plan-a-Day Test; SCWT = Stroop Color Word Test; SET = Six Elements Test;
SS = Spatial Span; TMT = Trail Making Test; TOL = Tower of London; VAP-S = Virtual Action
Plan—Supermarket; VCFMT = Virtual Cognitive Flexibility Measurement Task; VEP = Virtual Egyp-
tian Pyramids; VFT = Verbal Fluency Test; VMT = Virtual Maze Task; VRPMT = Virtual Reality
Prospective Memory Test; VSST = Virtual Supermarket Shopping Task; WCST = Wisconsin Card
Sorting Test; ZMT = Zoo Map Test.
J. Clin. Med. 2021, 10, 2782 7 of 26
Table 1. Characteristics of and evidence for diagnostic validity and two dimensions of ecological validity (verisimilitude and veridicality) of traditional, ecological, and VR tools that
measure executive functions in schizophrenia.
Ecological Validity
Diagnostic Validity
Type Tool Verisimilitude Veridicality
Examined Confirmed Developed Construct Technological Demands Examined Confirmed
Yes: significant difference Yes: significant correlation
between patients with Laboratory task: Computer version as between results on SCWT and
Traditional SCWT [85,86] Yes schizophrenia and healthy No paper-pencil or non-immersive Yes scales of community
controls [1,87,88]; several computerized task technology functioning [89–91]; several
meta-analyses meta-analyses
Yes: significant correlation
Yes: significant difference between results on TOL and
between patients with Laboratory task: Computer version as scales of community functioning,
Traditional TOL [85,92] Yes schizophrenia and healthy No paper-pencil or non-immersive Yes scales of social behavior in the
controls [93–95]; several computerized task technology milieu, scales of social
meta-analyses problem-solving, scales of social
skills [7]; one meta-analysis
Yes: significant difference Yes: significant correlation
between patients with Laboratory task: Computer version as between results on TMT and
Traditional TMT [85] Yes schizophrenia and healthy No paper-pencil or non-immersive Yes scales of community
controls [1,87,88]; several computerized task technology functioning [89,91]; two
meta-analyses meta-analyses
Yes: significant correlation
Yes: significant difference between results on WCST and
between patients with Laboratory task: Computer version as scales of community functioning,
Traditional WCST [85,96] Yes schizophrenia and healthy No paper-pencil or non-immersive Yes scales of social behavior in the
controls [1,2,87,88]; several computerized task technology milieu, scales of social
meta-analyses problem-solving, scales of social
skills [7]; one meta-analysis
Yes: significant difference Yes: significant correlation
between patients with Laboratory task: between results on VFT and
Traditional VFT [85,97] Yes schizophrenia and healthy No paper-pencil or Lack of computer version Yes scales of community
controls [1,87,88]; several computerized task functioning [7]; one
meta-analyses meta-analysis
J. Clin. Med. 2021, 10, 2782 8 of 26
Table 1. Cont.
Ecological Validity
Diagnostic Validity
Type Tool Verisimilitude Veridicality
Examined Confirmed Developed Construct Technological Demands Examined Confirmed
Yes: significant difference Yes: significant correlation
between patients with Laboratory task: Computer version as between results on DS and
Traditional DS [85,98] Yes schizophrenia and healthy No verbal or non-immersive Yes scales of community
controls [1,87,99,100]; several computerized task technology functioning [7,89–91]; several
meta-analyses meta-analyses
Yes: significant difference Yes: significant correlation
between patients with Laboratory task: between results on DST and
Traditional DST [101] schizophrenia and healthy No verbal or Lack of computer version Yes scales of community
controls [10]; one computerized task functioning [7]; one
meta-analysis meta-analysis
Yes: significant difference Yes: significant correlation
between patients with Laboratory task: Computer version as between results on LNST and
Traditional LNST [102] Yes schizophrenia and healthy No verbal or non-immersive Yes scales of community
controls [1]; one computerized task technology functioning [91]; one
meta-analysis meta-analysis
Yes: significant difference Yes: significant correlation
between patients with Laboratory task: Computer version as between results on SS and scales
Traditional SS [85,103] schizophrenia and healthy No manual or non-immersive Yes of community
controls [99,100]; two computerized task technology functioning [89–91]; several
meta-analyses meta-analyses
Independent living
as manual task:
Yes: significant difference
simple cooking, Computer version as
between patients with
Ecological EFPT [104,105] Yes Yes telephone use, non-immersive No No information
schizophrenia and healthy
medication technology
controls [104]; single study
management, and
bill payment
J. Clin. Med. 2021, 10, 2782 9 of 26
Table 1. Cont.
Ecological Validity
Diagnostic Validity
Type Tool Verisimilitude Veridicality
Examined Confirmed Developed Construct Technological Demands Examined Confirmed
Yes: significant correlation
between results on MET and
Yes: significant difference
two scales of real-world
between patients with Computer version as
Manual task: functioning [106]; single study
Ecological MET [106,107] Yes schizophrenia and healthy Yes non-immersive Yes
shopping center No: no significant correlation
controls [106,108]; two technology
between results in MET and two
studies
scales of real-world
functioning [108]; single study
Yes: significant correlation
between MSET and scale of
Yes: significant difference real-world functioning [111];
between patients with single study
Manual tasks: six
Ecological MSET [109] Yes schizophrenia and healthy Yes Lack of computer version Yes No: no significant correlation
realistic problems
controls [110]; one between results on MSET and
meta-analysis questionnaire ratings of
executive impairment [112];
single study
Yes: significant correlation
Yes: significant difference
between ZMT and questionnaire
between patients with
Manual task: map of ratings of executive impairment
Ecological ZMT [113,114] Yes schizophrenia and healthy Yes Lack of computer version Yes
zoo and scale of real-world
controls [110]; one
functioning [111,112];
meta-analysis
two studies
Virtual reality task: Computer non-immersive
Yes: significant correlation
Yes: significant difference supermarket with technology, scenario,
between results on VAP-S and
Virtual between patients with aisles displaying participants’ activities in
VAP-S [115] Yes Yes Yes results of naturalistic behavioral
reality schizophrenia and healthy items and static the environment, graphic
observations of real-life
controls [116]; single study virtual people representations of
tasks [117]; single study
(avatars) real items
J. Clin. Med. 2021, 10, 2782 10 of 26
Table 1. Cont.
Ecological Validity
Diagnostic Validity
Type Tool Verisimilitude Veridicality
Examined Confirmed Developed Construct Technological Demands Examined Confirmed
Computer non-immersive
Yes: significant difference Virtual reality task: technology, scenario,
Virtual between patients with city, station, bus and participants’ activities in
VCFMT [118] Yes Yes No No information
reality schizophrenia and healthy virtual people the environment, graphic
controls [118]; single study (avatars) representations of
real items
Computer non-immersive
Yes: significant difference Virtual reality task: technology, scenario, Yes: significant correlation
Virtual a between patients with office in a company participants’ activities in between results on CMPT and
CMPT [119] Yes Yes Yes
reality schizophrenia and healthy and virtual people the environment, graphic two scales of real-world
controls [119]; single study (avatars) representations of functioning [119]; single study
real items
Computer non-immersive
Yes: significant difference Virtual reality task: technology, scenario, No: no significant between
Virtual b between patients with office in a company participants’ activities in results on CMPT and two scales
CMPT [120] Yes Yes Yes
reality schizophrenia and healthy and virtual people the environment, graphic of real-world functioning [120];
controls [120]; single study (avatars) representations of single study
real items
Computer non-immersive
Yes: significant difference technology, scenario, Yes: significant correlation
Virtual reality task:
Virtual between patients with participants’ activities in between results on CST and
CST [121] Yes Yes grocery and virtual Yes
reality schizophrenia and healthy the environment, graphic scale of real-world
people (avatars)
controls [121]; single study representations of functioning [121]; single study
real items
Computer non-immersive
Yes: significant difference Yes: significant correlation
technology, scenario,
between patients with Virtual reality task: between results on PDT and
Virtual participants’ activities in
PDT [122] Yes schizophrenia and healthy Yes workplace Yes scale of real-world
reality the environment, graphic
controls [123,124]; environment functioning [123,124];
representations of
two studies two studies
real items
J. Clin. Med. 2021, 10, 2782 11 of 26
Table 1. Cont.
Ecological Validity
Diagnostic Validity
Type Tool Verisimilitude Veridicality
Examined Confirmed Developed Construct Technological Demands Examined Confirmed
Computer immersive
Yes: significant difference Virtual reality task: technology, scenario,
Virtual between patients with rooms with three participants’ activities in
VEP [125] Yes Yes No No information
reality schizophrenia and healthy doors in each and the environment, graphic
controls [125]; single study corridors representations of
real items
Yes: significant difference Computer immersive
Virtual reality task:
Virtual between patients with technology, scenario,
VMT [126] Yes Yes maze with walls and No No information
reality schizophrenia and healthy participants’ activities in
green grass
controls [126]; single study the environment
Virtual reality task: Computer non-immersive
Yes: significant difference shopping center with technology, scenario,
Virtual VRPMT [127, between patients with aisles displaying participants’ activities in
Yes Yes No No information
reality 128] schizophrenia and healthy items and static the environment, graphic
controls [128]; single study virtual people representations of
(avatars) real items
Virtual reality task: Computer non-immersive
Yes: significant difference supermarket with technology, scenario, No: no significant correlation
Virtual between patients with aisles displaying participants’ activities in between results on VSST and
VSST [129] Yes Yes Yes
reality schizophrenia and healthy items and static the environment, graphic scale of real-world
controls [129]; single study virtual people representations of functioning [129]
(avatars) real items
aCMPT without interruptions or unexpected outcomes and prospective memory instructions; b CMPT with interruptions or unexpected outcomes and prospective memory instructions. CMPT = Computerized
Meeting Preparation Task; CST = Computerized Shopping Task; DS = Digit Span; DST = Digit Sequencing Test; EFPT = Executive Function Performance Test; LNST = Letter Number Sequencing Test;
MET = Multiple Errands Test; PDT = Plan-a-Day Test; SCWT = Stroop Color Word Test; SET = Six Elements Test; SS = Spatial Span; TMT = Trail Making Test; TOL = Tower of London; VAP-S = Virtual Action
Plan—Supermarket; VCFMT = Virtual Cognitive Flexibility Measurement Task; VEP = Virtual Egyptian Pyramids; VFT = Verbal Fluency Test; VMT = Virtual Maze Task; VRPMT = Virtual-Reality Prospective
Memory Test; VSST = Virtual Supermarket Shopping Task; WCST = Wisconsin Card Sorting Test; ZMT = Zoo Map Test.
J. Clin. Med. 2021, 10, 2782 12 of 26
Unfortunately, these tools typically have a similar structure and methodology to the
first methods used in the early twentieth century, (e.g., the Stanford-Binet Intelligence Scale)
and do not reflect patients’ difficulties in real life; in effect, these tests are characterized by
low levels of veridicality, confirmed by correlations on the level of 0.20–0.30 with functional
outcome scales (see: Table 1 and Figure 1) [85]. Additionally, these tools lack verisimili-
tude, as they were not originally designed for their current purpose—to assess executive
functions in patients with psychiatric disorders—because they were either constructed as
experimental investigations of basic cognitive systems in healthy persons (e.g., WCST) or
for testing frontal lobe functions in patients with anterior lesions (e.g., TOL). Therefore, it
might not be appropriate to draw conclusions concerning different aspects of executive
dysfunction in schizophrenia based on performance on such tests. Besides, since traditional
tools neglect the influence of emotional and social processes by diverging from the real-life
situations with which patients may have problems, it is impossible to assess the practical
effects of executive functions. Another limitation is that during standard psychological
testing, patients usually perform only one task, while, in real life, situations usually require
multitasking—carrying out a number of tasks simultaneously, which often compete with
each other at the same time [110,133]. Unlike in the laboratory, real-life problems are mostly
open-ended in nature, which is not reflected in the fixed goals and defined structure of
traditional tools [107]. Many patients with schizophrenia who achieve satisfactory results
on traditional tests can be impulsive, easily distracted, and have problems with using
J. Clin. Med. 2021, 10, 2782 13 of 26
feedback, which may be reflected in problems with real-life situations. These limitations
can be more adequately captured by more ecological tools [113]. Despite these limitations,
traditional tools are often used because of: familiarity, long tradition, availability, price,
short assessment time, and satisfactory diagnostic validity (see: Table 1).
Table 3. Description of traditional neuropsychological tools used to assess executive functions in schizophrenia.
ing, and prospective memory (which, together, are necessary for completing operations
in conditions resembling true-to-life situations) in their poor performance on ecological
tests such as the Executive Function Performance Test (EFPT) [104], the Multiple Errands
Test (MET) [106,108], the Modified Six Elements Task (MSET) [110], and the Zoo Map
Test (ZMT) [110]. Descriptions of these ecological neuropsychological tools used to assess
executive functions in schizophrenia are given in Table 4.
Ecological tools have particularly good verisimilitude and veridicality (see: Table 1
and Figure 1); that is, performance in the task situation is predictive of performance in
situations outside it and the context and form of these tools corresponds to situations
encountered in real life—an important factor for clinical diagnosis. Ecological tools are
more useful for identifying executive dysfunction in patients with schizophrenia due to
the fact they measure executive skills in a more integrated way, through tasks that are
closer to real-life situations, instead of separated theoretical components (e.g., planning or
shifting) [107].
Table 4. Descriptions of the ecological neuropsychological tools used for measuring executive functions in schizophrenia.
Research based on VR methods has confirmed the presence of specific executive diffi-
culties in patients with schizophrenia, hindering their performance of complex everyday
activities, such as shopping, using public transport, or preparing a staff meeting in a busi-
ness office [24,25,137]. Although, like traditional tools, some VR tests were not developed
for patients with schizophrenia, evidence shows that they have good diagnostic validity
(see: Table 1). Using VR tools, it has been shown that schizophrenia patients have impaired
integration of visual and auditory stimuli. Moreover, Ku et al. [125] suggested that pa-
tients with schizophrenia have impaired multimodal integration and working memory
integration based on asking them to react to and interpret multimodal stimuli that had to
be memorized for a certain time period. Jeonghun Ku, Kim, and Kim [138] showed that
patients with schizophrenia cannot properly systematize or integrate the integrated stimuli
that occur in actual situations. A VR system was developed to administer multimodal
stimuli such as integrated visual and auditory stimuli. Patients were assessed and com-
pared in terms of their cognitive flexibility and working memory abilities by making them
experience and react to multimodal stimuli. Sorkin, Weinshall, Modai, and Peled [139]
examined sensory integration within schizophrenia patients’ working memory by means
of a virtual maze. Participants navigated through a series of rooms, repeatedly having to
choose from three doors. Each door had three characteristics (color, shape, and sound) and
only one combination of characteristics would open the door. Participants had to discover
the rule and implement it. When the task was over, each participant was given a perfor-
mance profile which included response time, error scores, strategy, and navigation ability.
Based on these profiles, a classification procedure was able to correctly identify 85% of the
schizophrenic patients. Furthermore, the patients did not exhibit any exceptional repetition
of responses regardless of the cessation of stimuli (traditionally known as “perseveration”),
as often happens in such patients. This only occurred when the task was not properly
explained to the participants.
Other specific executive difficulties in patients with schizophrenia have been demon-
strated in their poor performance on, inter alia, the Virtual-Action Planning Supermarket
(VAPS) [116], the Virtual Cognitive Flexibility Measurement Task (VCFMT) [118], the
Computerized Meeting Preparation Task (CMPT; see: Figure 2) [119,120], Computerized
Shopping Task (CST) [121], Plan-a-Day Test (PDT) [123,124], Virtual Egyptian Pyramids
(VEP) [125], Virtual Maze Task (VMT) [126], Virtual Reality Prospective Memory Test
(VRPMT) [128], and Virtual Supermarket Shopping Task (VSST; see: Figure 3) [129]. The
VR neuropsychological tools used to assess executive functions in schizophrenia are shown
in Table 5.
Table 5. Descriptions of virtual reality tools for measuring executive functions in schizophrenia.
Table 5. Cont.
Figure 2. Sample pictures presenting the main room, person-avatar, and office material area from the Computerized Meeting
Preparation Task (CMPT) [119]. Reprinted with permission from [119]. Copyright 2014 Elsevier. Participant‘s first person
view: (A) in the main room where the meeting takes place, (B) in the kitchen, and (C) in the office material area.
In his recent work, Parsons [142] presented a list of potential risks of using VR in clini-
cal conditions, including: (a) simulator sickness, (b) high fidelity stimulus presentations,
experience intensification, and information overload, (c) depersonalization, derealization,
and dysfunctional re-entry into the real, (d) virtual environments with vulnerable pop-
ulations, and (e) therapeutic misconceptions. Additionally, VR tools tend to be costly,
especially highly immersive methods (e.g., head-mounted displays). Patients have to
learn how to use often complicated human-computer interfaces, which may be difficult
for individuals with severe perception and memory impairments. For older patients,
computer anxiety may also be part of the problem [143]. For the welfare of patients, it
is essential that technology support clinicians in their therapeutic efforts, not substitute
for them. The therapeutic relationship is exceedingly important for both diagnosis and
neuropsychological interventions.
Figure 3. Sample pictures presenting the participant’s first-person view while collecting items on the Virtual Supermarket
Shopping Task (VSST) [129]. The names of the products are visible when pointed at. Reprinted with permission from [129].
Copyright 2021 Czech Academy of Sciences. Participant‘s first person view: (A) while collecting an item from the shelf,
(B) while collecting fruits and vegetables, and (C) while collecting products from the fridge.
SCWT, and WCST than with the VFT and working memory tasks. Patients who had stable
clinical profiles exhibited significantly stronger correlations with executive impairment
than did those with remitting or relapsing illnesses. Additionally, negative symptoms and
disorganization both correlated with general intellectual function (current IQ).
According to Thai et al. [110], only two studies have looked into the relationship
between psychopathological symptoms and executive dysfunction using ecological tests.
There were no significant correlations of subtests from the Behavioral Assessment of the
Dysexecutive Syndrome (BADS) battery with negative, positive, or disorganized symp-
toms [111,149]. In contrast, as assessed with Activities of Daily Living, negative symptoms
were linked to omissions during the choice of menu and greater delays between the first
and the last dishes, as well as the number of planning and repetition errors when cooking
the meal [150].
Only a few studies simultaneously focus on the link between psychopathological
symptoms and executive functions measured by VR tools in patients with schizophrenia.
For example, on the Computerized Shopping Task, Larøi et al. [121] showed that positive,
negative, and general symptoms were negatively correlated with the total times participants
consulted the list and the number of correct articles. Moreover, Josman et al. [116] showed
that negative symptoms correlated with all indices of the Virtual Action Plan—Supermarket
(VAP-S): trajectory duration, distance covered, purchases, correct actions, number of stops,
and total duration of stops. However, Laloyaux et al. [119] found no correlations between
psychopathological symptoms and different aspects of executive function as measured
by the Computerized Meeting Preparation Task (CMPT). A recent meta-analysis of the
Positive and Negative Syndrome Scale suggests five main psychopathological symptoms
in schizophrenia: negative symptoms, positive symptoms, disorganization, resistance,
and affect [151]. However, to the best of knowledge, this approach lacks data on the
relationship between psychopathological dimensions and results on VR tools that assess
executive functions in patients with schizophrenia.
The literature analysis described in this paper reveals important issues that should be
considered in future research. One idea for measuring the verisimilitude of VR is to use a
panel of experts containing, in addition to clinicians, individuals who actually work in a
given environment (e.g., shop workers and regular customers in the case of supermarket
environments). As self-description questionnaires and clinical ratings do not provide a full
picture of a patient’s behavior outside the clinic, we suggest that veridicality should be as-
sessed in a more precise way, preferably by naturalistic observation in appropriately chosen
situations [117]. In addition to ecological validity, ecological tools, especially VR methods,
should be investigated in terms of the classical psychometric measures of different types
of reliability and validity, including diagnostic validity, in terms of sensitivity, specificity,
positive predictive power, and negative predictive power. In assessing test-retest reliability
for executive functions measures, it is important to control for the practice effect and to use
adequate statistical methods (e.g., the Reliable Change Index [159]). Similarly, Parsons [24]
highlighted the need for correspondence, representativeness, expedience, and relevance
in VR research. Future research should better control for social factors (e.g., interaction
with avatars) in VR research on executive functions. Concerning VR training of executive
functions, it is important to include follow-ups in the design of the research, in order to
understand the long term effects of such training. It is important to adopt an interdisci-
plinary approach, with more comprehensive behavior analysis, for research on executive
functions and rehabilitation of dysfunction thereof in schizophrenia patients. This should
be based on VR tools with complex real-life situation scripts combined with physiological
measurements (heart rate variability, galvanic skin response, and blood pressure) and brain
activity measurement carried out with different methods [158]. Augmented reality, which
allows the projection of items and avatars onto actual scenes, is another interesting new
direction for research.
Some clinical implications need to be discussed. Firstly, for both diagnosis and therapy,
it is important to find the right balance between maximizing patient benefit and avoiding
harm. Secondly, due to the lack of standardized VR tools for executive function assessment
in schizophrenia, which includes guidelines on development, norming, psychometric
validation, and administration, they should be used in combination with traditional tools
of proven psychometric value [26,142]. Similarly, due to the lack of empirically verified
and standardized therapeutic methods, VR tools should be used in combination with
traditional, empirically verified methods and cognitive-behavioral therapy. The American
Academy of Clinical Neuropsychology and the National Academy of Neuropsychology
advises that innovative computer diagnostic and therapeutic methods should always be
precisely described to provide comprehensive information on the product and thus to
allow clinicians to make informed decisions with patient welfare in mind [160].
10. Conclusions
Executive dysfunction in schizophrenia is an important clinical and social problem. Im-
pairments in monitoring, attention shifting, planning, inhibition, rule generation, abstract
thinking, and working memory, as well as the loss of skills required for the performance
of complex tasks, can negatively impact patients’ social and professional functioning as
well as their quality of life. When diagnosing executive dysfunction, an array of neu-
ropsychological methods must be used—not only traditional tools, but also those with
proven ecological validity (i.e., ecological and VR tools)—to accurately understand the
underlying nature of the deficits observed. However, due to the many potential risks of
using VR in clinical conditions and the lack of standardized VR tools for executive function
assessment in schizophrenia, they should be used in combination with traditional tools of
proven psychometric value. Future research should be based on paradigms that allow the
use of VR assessment of executive functioning with methods of functional neuroimaging.
Moreover, it would be interesting to investigate the influence of psychiatric medications on
executive functioning measured by VR techniques in schizophrenia.
J. Clin. Med. 2021, 10, 2782 20 of 26
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