Lack of Evidence That Neural Empathic Responses Are Blunted in Excessive Users of Violent Video Games: An fMRI Study

Abstract

The use of violent video games has been often linked to increase of aggressive behavior. According to the General Aggression Model, one of the central mechanisms for this aggressiveness inducing impact is an emotional desensitization process resulting from long lasting repeated violent game playing. This desensitization should evidence itself in a lack of empathy. Recent research has focused primarily on acute, short term impact of violent media use but only little is known about long term effects. In this study 15 excessive users of violent games and control subjects matched for age and education viewed pictures depicting emotional and neutral situations with and without social interaction while fMRI activations were obtained. While the typical pattern of activations for empathy and theory of mind networks was seen, both groups showed no differences in brain responses. We interpret our results as evidence against the desensitization hypothesis and suggest that the impact of violent media on emotional processing may be rather acute and short-lived.

Full text

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ORIGINAL RESEARCH
published: 08 March 2017
doi: 10.3389/fpsyg.2017.00174
Edited by:
Matthias Brand,
University of Duisburg-Essen,
Germany
Reviewed by:
Matt R. Judah,
Old Dominion University, USA
Adriano Schimmenti,
Kore University of Enna, Italy
*Correspondence:
Gregor R. Szycik
szycik.gregor@mh-hannover.de
Specialty section:
This article was submitted to
Psychopathology,
a section of the journal
Frontiers in Psychology
Received: 24 November 2016
Accepted: 25 January 2017
Published: 08 March 2017
Citation:
Szycik GR, Mohammadi B, Münte TF
and te Wildt BT (2017) Lack
of Evidence That Neural Empathic
Responses Are Blunted in Excessive
Users of Violent Video Games: An
fMRI Study. Front. Psychol. 8:174.
doi: 10.3389/fpsyg.2017.00174
Lack of Evidence That Neural
Empathic Responses Are Blunted in
Excessive Users of Violent Video
Games: An fMRI Study
Gregor R. Szycik1*, Bahram Mohammadi2,3 , Thomas F. Münte2,4 and Bert T. te Wildt5
1Department of Psychiatry, Social Psychiatry and Psychotherapy, Hannover Medical School, Hanover, Germany,
2Department of Neurology, University of Lübeck, Lübeck, Germany, 3Clinical Neuroscience Lab, International Neuroscience
Institute, Hanover, Germany, 4Institute of Psychology II, University of Lübeck, Lübeck, Germany, 5Department of
Psychosomatic Medicine and Psychotherapy, LWL University Hospitals of the Ruhr-University, Bochum, Germany
The use of violent video games has been often linked to increase of aggressive behavior.
According to the General Aggression Model, one of the central mechanisms for this
aggressiveness inducing impact is an emotional desensitization process resulting from
long lasting repeated violent game playing. This desensitization should evidence itself in
a lack of empathy. Recent research has focused primarily on acute, short term impact
of violent media use but only little is known about long term effects. In this study 15
excessive users of violent games and control subjects matched for age and education
viewed pictures depicting emotional and neutral situations with and without social
interaction while fMRI activations were obtained. While the typical pattern of activations
for empathy and theory of mind networks was seen, both groups showed no differences
in brain responses. We interpret our results as evidence against the desensitization
hypothesis and suggest that the impact of violent media on emotional processing may
be rather acute and short-lived.
Keywords: video games, violence, desensitization, General Aggression Model, Catalyst Model
INTRODUCTION
The possible influence of violent video games (VVG) on human aggressive behaviour is hotly
debated. According to research done in the context of the General Aggression Model (GAM)
a direct and causal relationship between the use of VVG and aggressiveness (Anderson and
Bushman, 2002) is postulated: aggressive or impulsive behavior is a short term result of both
personal and situational variables like exposure to VVG. Therefore, an increase of aggression after
exposure to VVG is hypothesized to appear as a result of cognitive cuing effects (Anderson and
Dill, 2000). Long-term exposure to VVG on aggressive behavior according to the GAM leads to an
increase in aggressive personality traits by learning, rehearsal and reinforcement of aggression-
related knowledge structures. Also, a desensitization against violent content and a decrease of
empathy and prosocial behavior has been postulated (Sparks and Sparks, 2002;Anderson et al.,
2003;Huesmann et al., 2003).
The alternative Catalyst Model postulates only little or no effects of VVG use on human
aggressive behavior (Ferguson et al., 2008). Following this model, aggressive behavior results
primarily from biological factors and VVG only shape the style of aggressive expression. This view
criticizes the GAM because of the discrepancy between its predictions and the recent violence
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Szycik et al. Emotional Desensitization and Violent Video Games
statistics (Ferguson, 2010), small effect sizes or poor quality meta-
analyses (Kutner and Olson, 2008;Ferguson, 2015a), and the
publication bias or selective reporting of only significant data
(Elson and Ferguson, 2014;Ferguson, 2015b).
The literature regarding short term desensitization effects of
VVG has been inconsistent. Some short term desensitization
effects could be shown regarding physiological reactivity, i.e.,
reduction in heart rate or galvanic skin reactions to violent
stimuli (Carnagey et al., 2007a,b;Staude-Muller et al., 2008). The
P300 component of the event-related potential has also been
found to be reduced after VVG use (Bartholow et al., 2006;
Engelhardt et al., 2011). Other studies using violent and non-
violent versions of the same game could not find differences
in physiological markers like heart rate or skin conductance
(Ballard et al., 2012;Chittaro and Sioni, 2012). A recent meta-
analysis suggests a relationship between VVG use and decrease
in empathy (and more desensitization) but only for short term
effects (Anderson et al., 2010). Long term effects were not
analyzed in this meta-analysis because of a lack of pertinent
studies. To our knowledge only two studies focussed on long
term desensitization effects of VVG use by the means of fMRI.
In the first study small effects were shown but the results were
not adequately corrected for multiple comparisons (Montag et al.,
2012) which raise the possibility that the reported differences
would not have survived adequate correction. Our group studied
28 male excessive VVG users and a matched control group
with two experiments using emotional picture stimuli from the
IAPS data base (Szycik et al., 2016). The user group had at
least 3 h of VVG abstinence prior to experiment making the
design more suitable for analyzing long term effects. VVG users
showed similar brain responses as control subjects for emotional
material indicating no specific desensitization effect of excessive
long lasting VVG use.
As Montag et al. (2012) and Szycik et al. (2016) the current
study focused on the long-term desensitization effects of VVG
use but this time with an emphasis on empathy. For this reason
we used a picture set, patterned after the materials of the
Adult Attachment Projective Picture System (AAP; George and
West, 2001), designed to elicit empathic / emotional reactions
in situations with and without social interaction (Krämer et al.,
2010;Beyer et al., 2014a,b). According to the Perception-
Action-Model (PAM) of empathy (Preston and de Waal, 2002)
and in keeping with previous results using the same stimulus
set we hypothesized that pictures depicting another person’s
emotional state should elicit empathic reactions and concomitant
neural activations. Furthermore, according to the desensitization
hypothesis derived from the GAM that excessive VVG users
should show decreased brain activity in the empathy network
(Bzdok et al., 2012).
MATERIALS AND METHODS
All subjects gave written informed consent in accordance with
the Declaration of Helsinki. The protocol was approved by the
ethic committee of the Medical School Hannover. All participants
were also provided with short briefing prior to the experiment.
First possible contradictions for MRI measurements were cleared
by standard questionnaire and then all necessary information
regarding the study was given (e.g., experimental task). The
subjects had also the possibility to ask questions before the
experiment. After the experiment all subjects were provided with
standard debriefing containing additional information regarding
the study.
Participants
As use of VVG and aggressive behavior is more prevalent in
men, only male participants were recruited. Inclusion criterion
for the VVG user group was consumption of violent games
of the first-person shooter category (e.g., Counterstrike, Call
of Duty or Battlefield) for at least 4 years and for at least
2 h daily. First-person shooter games are centered on combat
situations seen from the first-person perspective, involving virtual
weapons (mostly automatic rifles). Control subjects did not have
any experience with VVG (self-report). We also excluded all
control subjects that reported a daily use of any video games. All
participants were free of psychiatric and neurological disorders
as assessed clinically by the senior author, a board-certified
psychiatrist. One participant of the VVG group was excluded
from the analysis due to taking antidepressant medication. All
of the subjects had normal or corrected to normal vision.
Experimental and control groups were matched for school
education and age.
For the experiment 15 VVG users (mean age 22.8 ±4.3 years)
and 15 control subjects (mean age 22.1 ±3.0 years) were
recruited (difference n.s.). The VVG users had played violent
games since 13.1 ±4.4 years for about 4.0 ±1.3 h daily.
To avoid possible immediate effects of violent games all
participants refrained from playing for at least 3 h prior to
the experiment during which time they were informed about
the experiment and were prepared for data acquisition. The
actual time without playing VVG before the experiment was
considerably longer in most subjects.
Stimuli and Design
The experimental stimulation in this study is based on a
previous publication and uses black- line drawings on a gray
background (Krämer et al., 2010;Beyer et al., 2014a,b). The
drawings were assigned to four conditions: emotionally negative
social situations involving two interaction partners (EMOT-
TWO), emotionally neutral social situations also involving
two interaction partners (NEUT-TWO), emotionally negative
situations involving one person (EMOT-ONE), and emotionally
neutral situations involving one person (NEUT-ONE). Negative
emotional stimuli depicted emotions like anger, sadness, pain or
anxiety (Figure 1). The stimuli had been previously rated for their
emotional content with consistent results across the individual
subjects and significant differences for the specific categories
(Krämer et al., 2010).
The stimuli were presented for 4 s in pseudorandom order
each with varying interstimulus interval (ISI). For each of the four
experimental categories 24 different stimuli were used. Between
the stimuli a black central fixation cross was presented on gray
background. ISI varied pseudo-randomly within each category
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FIGURE 1 | Example stimuli. Depicted are examples of the drawings used
in this study: (A) emotionally negative social situations involving two interaction
partners (EMOT-TWO), (B) emotionally neutral social situations also involving
two interaction partners (NEUT-TWO), (C) emotionally negative situations
involving one person (EMOT-ONE), and (D) emotionally neutral situations
involving one person (NEUT-ONE).
with 15 intervals of 6 s duration, 5 intervals of 8 s duration and 2
intervals each of 10 s and 12 s duration. During fMRI scanning
participants were instructed to watch the pictures carefully
and imagine how they would feel in the depicted situation.
Presentation software (Neurobehavioral Systems, Inc.) was used
to deliver stimuli. Stimuli were presented via an MRI-compatible
video display mounted into prepared glasses (CinemaVision,
Resonance Technology Inc., USA). Prior to fMRI scanning a test
picture was presented to ensure good visibility of stimuli for each
participant.
Image Acquisition
Magnetic-resonance images were acquired on a 3-T Siemens
Magnetom Scanner (Erlangen, Germany) equipped with a
standard head coil. A total of 545 T2∗-weighted volumes of the
whole brain (EPI-sequence; TR 2000 ms, TE 30 ms, flip angle
80◦, FOV 192 mm, matrix 642, 34 slices, slice thickness 3 mm,
interslice gap 0.75 mm) near to standard bicommisural (AC-
PC) orientation were collected. After the functional measurement
a 3D high resolution T1-weighted volume for anatomical
information (MPRAGE-sequence; matrix 192 ×2562, 1 mm
isovoxel) was recorded. The subject’s head was fixed during the
entire measurement to avoid head movements.
Acquisition of Psychometric Data
Prior to fMRI scanning data from different psychological
questionnaires was collected. We used the German adaptation
(“Der Saarbrücker Persönlichkeitsfragebogen zur Messung
von Empathie”) of the Interpersonal Reactivity Index (IRI)
with its four subscales: PT- perspective-taking, FS- fantasy
scale, EC- empathic concern, and PD- personal distress
(Davis, 1980). To analyze potential group differences in
aggressiveness we collected the data from the short version of
the German questionnaire for aggressiveness factors K-FAF:
“Kurzfragebogen zur Erfassung von Aggressivitätsfaktoren”
(Heubrock and Petermann, 2008). To analyze the ability
in emotional understanding, processing, or description the
German adaptation of the Toronto Alexithymia Scale (Bagby
et al., 1994) was used. To assess relevant personality traits
we used the German adaptation of the Temperament and
Character Inventory TCI (Cloninger, 1994) and The Inventory
of Clinical Personality Accentuations (“Inventar Klinischer
Persönlichkeitsakzentuierungen”) to screen clinical personality
aspects (Andresen, 2006).
fMRI Data Analysis
Analysis and visualization of the data were performed using
Brain Voyager QX (Brain Innovation BV, Maastricht, The
Netherlands) software (Goebel et al., 2006). First, a correction for
the temporal offset between the slices acquired in one scan was
applied. For this purpose the data was cubic spline interpolated.
After this slice scan time correction a 3D motion correction
was performed by realignment of the entire measured volume
set to the first volume by means of trilinear interpolation.
Thereafter, linear trends were removed and a high pass filter
was applied resulting in filtering out signals occurring less than
2 cycles in the whole time course. Structural and functional
data were spatially transformed into the Talairach standard
space (Talairach et al., 1988) using a 12-parameter affine
transformation. Functional EPI volumes were spatially smoothed
with an 8 mm full-width half-maximum isotropic Gaussian
kernel to accommodate residual anatomical differences across
volunteers.
For the statistical model a design matrix including all
conditions of interest was specified using a hemodynamic
response function. This function was created by convolving the
rectangle function with the model of Boynton et al. (1996) using
1=2.5, τ=1.25 and n=3. Thereafter, a multi-subject random
effects (RFX) analysis of variance model (ANOVA) with two
main within-subject factors and one between-subject factor was
used for identification of significant differences in hemodynamic
responses. The first within subject factor was emotional content
(EMOT vs. NEUT), the second within subject factor was social
relation (TWO vs. ONE). The between-subject factor was group
(VVG users vs. control subjects). Additional as regressors of
no interest we used overall six translation and rotation vectors
derived for each dataset during the 3D motion correction.
Main effects of all factors and their interaction were
considered. The false discovery rate threshold of q(FDR) <0.01
(Genovese et al., 2002) was chosen for identification of the
activated voxels. Voxels fulfilling these criteria are reported. The
centers of mass of suprathreshold regions were localized using
Talairach coordinates and the Talairach Daemon tool (Lancaster
et al., 2000).
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RESULTS
Questionnaire Data
Group differences were obtained only for the factor Novelty
Seeking of the Temperament and Character Inventory
[t(28) =2.126, p<0.042] and the scale Antisocial Personality
of The Inventory of Clinical Personality Accentuations
[t(28) =3.255, p<0.003]. VVG users showed higher
scores for Novelty Seeking (M=25.27, SD =4.59 vs.
M=20.47, SD =7.44) and for Antisocial Personality
(M=22.13, SD =5.89 vs. M=16.13, SD =4.03) in
comparison to controls. No further group differences were
apparent in the questionnaires, in particular no differences
were seen for empathy and aggression measures (for
FIGURE 2 | Results of the fMRI data analysis. (A) Brain sites identified for the main factor emotional content responding for stimuli with emotional negative and
neutral valence. (B) Brain sites identified for the main factor social relation, responding for stimuli depicting one person or two persons in social interaction. (C) Brain
sites identified for the interaction of the main factor emotional content and social interaction. The factor group revealed no significant brain sites, also all other
interactions resulted in no significant results. L, leftt; R, right; XZtal, Talairach coordinates.
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the overview of all questionnaire data see Supplementary
Material).
fMRI
The analysis of fMRI data revealed at q(FDR) <0.01 strong
effects for the main factor emotional content (Figure 2A). At a
less strict level of q(FDR) <0.05 additional typical activations
often seen for the processing of emotionally relevant material
were found, such as bilateral limbic structures including both
amygdalae. The main effect of social interaction was significant
for several brain areas at q(FDR) <0.01 (Figure 2B) similar to
earlier studies (Krämer et al., 2010;Beyer et al., 2014a,b). There
were no significant differences between VVG users and controls
at the level of q(FDR) <0.01. To check for weak effects, this
analysis was repeated at a very liberal threshold of p=0.01,
uncorrected, but again no reliable activation differences between
groups were seen. We also analyzed all possible interaction effects
at the q(FDR) <0.01 significance level. Only the interaction of
emotional content by social relation resulted in reliable brain
activations related primarily to bilateral parahippocampal gyrus
(Figure 2C). All other interactions including the factor group
were not significant at this level. Table 1 gives an overview about
the identified brain sites for the main factors and interaction of
the ANOVA analysis.
DISCUSSION
A central claim of the GAM regarding the effects of VVG
is desensitization toward emotional stimuli. Although some
evidence has been provided for short term effects of VVG in the
sense of a decreased empathy and increased of aggressiveness
(Carnagey et al., 2007a,b;Staude-Muller et al., 2008), long term
effects have not been intensively investigated. Long term effects
were the focus of the present study, which assessed neural
responses to stimuli designed to elicit empathic reactions. To
rule out short term effects of VVG, users had ben abstinent
for at least 3 h prior to the measurements. Contrary to our
initial hypothesis of a reduced activity in empathy related brain
regions in VVG users, the fMRI data did not provide evidence
for a neural desensitization in the processing emotionally salient
stimuli. In fact, the responses of both groups were very similar
and no group differences were observed even at relaxed statistical
thresholds. This lack of a group main effect and of interaction
effects involving the group factor is not due to a general
lack of emotional reactivity in our participants. Indeed, we
found robust activations for the factor emotional content in
our dataset (Figure 2A) similar to those found previously in
studies using the same materials (Krämer et al., 2010;Beyer
et al., 2014a,b). These activations included areas already known
as involved in processing of emotional content (limbic structures,
ventromedial and ventrolateral prefrontal cortex) and areas
involved in mentalizing or theory-of-mind process (e.g., regions
around superior temporal sulcus) (Bzdok et al., 2012, 2013;
Mutschler et al., 2013;Mitchell and Phillips, 2015;Morelli
et al., 2015). Our paradigm clearly is sensitive to differences
in emotional content. Also, aspects of social relation could
be reliable observed in our data and were in line with the
previous research (Adolphs, 2003;Krämer et al., 2010;Beyer et al.,
2014a,b).
Thus, the lack of group differences in our fMRI data dues not
suggests, that excessive VVG use leads to long term emotional
desensitization and a blunting of neural responses related to
empathy. This is corroborated by the questionnaire data which
TABLE 1 | Brain areas identified for the ANOVA.
Brain structure Hemisphere Talairach center of mass Cluster size (mm3)
x y z
Main Factor: emotional content
Inferior Frontal Gyrus, BA13 R 44 26 3 1242
Inferior Frontal Gyrus, BA9 R 41 10 28 1458
Superior Temporal Gyrus, BA39 R 50 −52 14 4401
Lingual Gyrus, BA18 R 6 −75 3 648
Medial Frontal Gyrus, BA9 L −1 47 30 918
Precentral Gyrus, BA44 L−42 18 8 3645
Middle Frontal Gyrus, BA6 L −39 −2 44 945
Middle Temporal Gyrus, BA39 L−48 −57 9 9180
Main Factor: social relation
Postcentral Gyrus, BA2 R 58 −19 33 837
Superior Temporal Gyrus, BA22 R 48 −53 16 6480
Cuneus, BA18 R/L 1 −72 18 34911
Superior Temporal Gyrus, BA39 L−48 −59 17 6750
Interaction: emotional content x social relation
Parahippocampal Gyrus, BA36 R 24 −38 −10 3294
Parahippocampal Gyrus, BA37 L−28 −44 −10 3861
Middle Temporal Gyrus, BA19 L −34 −78 26 540
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did not reveal differences between VVG users and controls for
empathy and aggression measures, even though some differences
emerged for measures assessing novelty seeking and antisocial
personality.
Most previous studies have focused on immediate effects
of VVG use (Brockmyer, 2015). For example, Weber et al.
(2006) looked at fMRI activations during the performance
of violent computer games and reported a suppression of
amygdala and anterior cingulate gyrus activity which was taken
to suggest a blunted emotional reactivity. Other researchers
reported a decreased interaction between amygdala and the
lateral orbitofrontal cortex directly after exposure to violent
media (Kelly et al., 2007). Gentile et al. (2014) reported
suppression of fMRI responses to violent compared to non-
violent video games in VVG users. Evidently, these studies used
stimulation with violent media/games immediately before or
even during the experiment and therefore the results may by
influenced not only by desensitization but also by other factors
such as increased attention toward motor actions or immediate
activation of aggressive cognitions. In any case, these reflect only
possible short term influence of VVG on emotional processing.
Studies focussing on long term effects are rare and show results
that are in line with the present study (Szycik et al., 2016).
The missing group effect in our fMRI data is not really
surprising giving the fact that both groups showed also no
differences in empathy and aggressiveness as assessed by
psychological tests. Our data therefore is in line with the
Catalyst Model of violent media influence on individual behavior
which posits that these do not increase aggressive behavior but
may influence the way how aggressive behavior is displayed.
Therefore, aggressiveness itself results more from other aspects
than violent media use. This idea is supported by our data.
VVG users differ in personality trait Novelty Seeking. As Novelty
Seeking is highly correlated with Sensation Seeking (Zuckerman
et al., 1993) subjects with high values on this scale are vulnerable
for risky activities and tend to excessive behavior resulting often
both in substance related and behavioral addictions like e.g.,
excessive use of video games (Bardo et al., 1996;McCoul and
Haslam, 2001;Roberti, 2004;Grucza et al., 2006;Wang et al.,
2015). VVG users of our study also showed high values on
the antisocial scale of the clinical personality inventory. This
again may be the basis for specific problematic behavior often
suggested for this population. In this sense VVG use might be
a yet another symptom not the cause of problems in this group.
One interesting question arises from the fact that the significant
group difference in antisocial personality found in this study was
not accompanied by significant differences in empathy scores.
Empathy is only one part of many (e.g., disregard for social
norms, rules, and obligations, incapacity to maintain enduring
relationships, incapacity to experience guilt or to profit from
experience) involved in the psychological construct of antisocial
personality. Keeping that in mind or VVG group could score
significant higher on antisocial personality without differing from
the control group in empathy scores.
Before concluding our results we want to put some attention
to the limitations of the study. Thus we did not found group
differences in our fMRI data set. Null findings in imaging studies
are notoriously problematic (Hupe, 2015) and may result also
from to small effects in relation to the extent of the population
included. One possibility to handle this problem is to decrease
statistical threshold used with the risk of making “false positive”
conclusions. We tried to maximize our ability to find group
differences and to safeguard against “false negatives” and lowered
the statistical threshold used to very liberal one of p=0.01,
uncorrected. But also after the adaptation of the threshold no
group differences could be found. Second relevant limitation of
this study relies on the fact, that our both populations were
not controlled for consumption of other than VVG violent
media, e.g., violent cinema movies or internet content. Thus we
cannot rule out the possibility that our control subjects consumed
in similar excessive extent other violent contents and have
experienced desensitization at same level as our experimental
group.
To summarize, our results provide additional evidence
against the desensitization hypothesis of VVG use and human
aggression. Research on media impact on aggressive behavior
should focus on short term (influencing the subject’s state) as well
as long term impact (possibly influencing trait aggressiveness).
Moreover, additional paradigms should be employed, e.g., facial
expression tasks (van Zutphen et al., 2015), to examine these
aspects within VVG users. Also the use of more ecological
valid paradigms could be promising to put more light on
this topic. Interesting approach could be to put individuals
with VVG use and controls into situations requiring acting
upon emotional stimuli like it is the case in the Taylor
Aggression Paradigm. A number of recent imaging studies
have used a version of this paradigm to assess impulsive
aggression in response to provocation (Krämer et al., 2007;
Beyer et al., 2014a,b, 2015;Dambacher et al., 2015;Gan et al.,
2015).
AUTHOR CONTRIBUTIONS
GS designed the study, collected and analyzed the data,
interpreted the results and wrote the manuscript. BM collected
the data and supported the interpretation of the results.
TM supported the interpretation of the data and wrote the
manuscript. BtW designed the study, collected the data and
supported the interpretation of the results.
FUNDING
This study was supported by the TUI-Foundation, the VW-
Foundation, the Draeger-Foundation, the DFG (TR-SFB 134, TP
C1, TP C2) and the BMBF.
SUPPLEMENTARY MATERIAL
The Supplementary Material for this article can be found
online at: http://journal.frontiersin.org/article/10.3389/fpsyg.
2017.00174/full#supplementary-material
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Conflict of Interest Statement: The authors declare that the research was
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