View metadata, citation and similar papers at core.ac.uk
OPEN
Received: 29 April 2016
Accepted: 10 March 2017
Published: xx xx xxxx
CORE
brought to you by
www.nature.com/scientificreports
provided by Institutional Repository of the Freie Universität Berlin
social cognition in aggressive
offenders: Impaired empathy, but
intact theory of mind
Korina Winter1,2, Stephanie Spengler1, Felix Bermpohl1, Tania singer3 & Philipp Kanske
3
Aggressive, violent behaviour is a major burden and challenge for society. It has been linked to deficits
in social understanding, but the evidence is inconsistent and the specifics of such deficits are unclear.
Here, we investigated affective (empathy) and cognitive (Theory of Mind) routes to understanding
other people in aggressive individuals. Twenty-nine men with a history of legally relevant aggressive
behaviour (i.e. serious assault) and 32 control participants were tested using a social video task
(EmpaToM) that differentiates empathy and Theory of Mind and completed questionnaires on
aggression and alexithymia. Aggressive participants showed reduced empathic responses to emotional
videos of others’ suffering, which correlated with aggression severity. Theory of Mind performance,
in contrast, was intact. A mediation analysis revealed that reduced empathy in aggressive men was
mediated by alexithymia. These findings stress the importance of distinguishing between socioaffective and socio-cognitive deficits for understanding aggressive behaviour and thereby contribute to
the development of more efficient treatments.
Aggressive behaviour towards others is a severe societal problem. More than 1.1 million cases of violent crimes
occur per year in the US alone (such as assault, grievous bodily harm, homicide)1. The causes for aggressive
behaviour are assumed to be diverse, but deficits in social understanding have been repeatedly proposed as core
mechanisms2, 3. Nevertheless, evidence for such deficits is limited and, crucially, the specifics of impaired social
understanding remain unclear4. The present study therefore aims to test if deficits impact affective or cognitive
routes of understanding others equally or selectively, thus mainly impairing the ability to share others’ emotions
or take others’ perspectives.
Aggressive behaviour is defined as “any behaviour directed toward another individual that is carried out with
the proximate (immediate) intent to cause harm”5–8. It is hypothesised that aggressive behaviour is inhibited when
we correctly represent the related consequences for others9. This link seems plausible, assuming that those who
are neither capable of feeling another person’s pain nor understanding their motives, intentions, and goals are
in fact more likely to cross personal boundaries and inflict bodily, psychological or material harm. Deficits in
social understanding are also associated with a number of mental disorders and conditions that are characterised
by aggressive and violent behaviour, including antisocial personality disorder, psychopathy, and autism spectrum disorder10–12. Social psychology and social neuroscience have identified two critical routes to understanding others: an affective route that allows for sharing others’ emotions and feeling for them (including empathy,
and compassion) and a cognitive route that enables the representation of and reasoning about others’ mental
states (Theory of Mind [ToM], perspective-taking)13. While empathy has been defined “as the process by which an
individual infers the affective state of another by generating an isomorphic affective state in the self, while retaining
knowledge that the cause of the affective state is the other”14, compassion, complementarily, refers to “an emotional
and motivational state characterised by feelings of loving-kindness and a genuine wish for the well-being of others”15.
ToM, in contrast, is the ability to understanding others’ mental and affective states by means of reasoning about
the thoughts, emotions or beliefs of others16–18. This conceptual dissociation is supported by a dissociation of
empathy, compassion and ToM on a behavioural and neural basis19–21.
In general, aggressive behaviour is not limited to those with mental disorders such as anti-social personality
disorder or specific exceptional contexts such as war, but is also carried out by healthy people during everyday
1
Department of Psychiatry and Psychotherapie, charité University Medicine Berlin, Berlin, Germany. 2Department of
forensic Psychiatry, Krankenhaus d. Maßregelvollzugs Berlin, Berlin, Germany. 3Department of Social neuroscience,
Max Planck institute for Human cognitive and Brain Sciences, Leipzig, Germany. correspondence and requests for
materials should be addressed to P.K. (email: kanske@cbs.mpg.de)
Scientific RepoRts | 7: 670 | DOI:10.1038/s41598-017-00745-0
1
www.nature.com/scientificreports/
social interactions. Regarding aggression in healthy individuals, a couple of meta-analyses22–24 have aimed at integrating the literature over the last few years. An early meta-analysis by Miller and Eisenberg23 reported a negative
association of empathy and aggression in questionnaire studies, but no significant relation for experimental studies, most of which, however, were done in children. Only including questionnaire studies in offenders, Jollife and
Farrington22 found a weak negative association of aggression with empathy, but a stronger negative relationship
to cognitive perspective-taking. More recently, Vachon et al.24 reviewed all available evidence on social understanding and aggression in adults and also only found a very weak association. Empathy and cognitive perspective
taking did not differ in their (non-) relation to aggression. Again, most of the included studies were done using
questionnaires. Overall, the evidence is, thus, largely inconsistent. One reason for this may be methodological
problems in assessing empathy and Theory of Mind using questionnaires. Both constructs represent socially
desirable traits, and questionnaire items assessing them are almost identical to those used in social desirability
scales. Also, to allow for direct comparison, empathy and Theory of Mind should be tested in the same individuals. Thus, experimental studies are needed that allow us to assess both empathy and ToM in a group of individuals
with aggressive tendencies.
Both empathy and aggression have been related to alexithymia, a personality trait describing difficulties in
identifying and expressing one’s own emotional states. The prevalence of alexithymia in the general public is
approximately 10%25, but it seems to be increased in aggressive individuals26, 27. Hitherto, increased alexithymia
has been associated with empathy deficits28–31 decreased empathic concern, for instance for victims in harmful
third-party acts32 and for victims in moral dilemmas33, 34, and more egocentric moral attitudes35, both in healthy
adults and clinical groups36, 37. There is consistent evidence that people with alexithymia are less empathic as they
lack the ability to accurately identify, describe and reflect their own emotions, which makes it even harder—if not
impossible—to represent those of others38. Recent studies reported that participants with alexithymia showed
lower abilities in complex empathy tasks28, 36, 39–41. Therefore, aggressive behaviour may be linked to lower empathy capabilities owing to an elevated manifestation of alexithymia.
Taken together, it is yet unclear what the specific deficits that contribute to aggressive behaviour are in social
understanding. Therefore, we aimed (1) to test whether social understanding is impaired in men with a history of
aggressive behaviour and (2) which components of social understanding are specifically affected. We also hypothesise that (3) a putative deficit in empathy in aggressive healthy men may be mediated by increased alexithymia.
To address these questions, we tested empathy, compassion and Theory of Mind in men with a history of legally
relevant aggressive behaviour and non-aggressive control participants. We applied a validated experimental paradigm20 that presents short video clips of either emotionally negative or neutral valence and asks participants to
rate how much they share the narrator’s emotion (empathy rating) and how much compassion they experience
for the narrator (compassion rating). Subsequently, multiple-choice questions probed participants’ ToM reasoning and factual reasoning (control condition) capabilities (see Fig. 1). Additionally, we assessed aggression and
alexithymia in established questionnaires.
Results
Aggression self-reports. As expected, the experimental group showed significantly higher aggression than
the control group as indicated in increased Buss-Perry-Aggression-Questionnaire (BPAQ) and Reactive-Proactive
Aggression Questionnaire (RPQ) scores (see Table 1, for repeated analysis with covariates see Supplement S2).
EmpaToM task. Empathy ratings. Regarding the main effect of valence, all participants showed more negative affect ratings for emotionally negative videos than neutral videos (see Fig. 2A and Table 2; F(1,57) = 140.31,
p < 0.001, η² = 0.711, d = 3.16). There was no significant main effect of group (F(1,57) = 7.91, p = 0.152, η² = 0.122,
d = 0.075). Most importantly, we found a significant interaction of group and valence (F(1,57) = 7.910, p = 0.007,
η² = 0.122, d = 0.746). Post-hoc analysis revealed that the experimental group showed significantly less negative
affect after watching emotionally negative videos than the control group (mean difference = −1.107, SD = 0.097,
F(1,57) = 8.05, p = 0.001, η² = 0.124, d = 0.75). This reduced sharing of negative affect indicates diminished empathy in the aggressive group. After including IQ and years of education as covariates, the significant interaction
effect remained significant (see Supplement S4).
Compassion ratings. All participants reported more compassion after watching emotionally negative videos
compared to neutral videos (see Fig. 2B, and Table 2; F(1,57) = 155.50, p < 0.001, η² = 0.732, d = 3.327). There was
no significant main effect of group (F(1,57) = 2.119 p = 0.151, η² = 0.036, d = 0.388). The interaction of emotionality
and group was marginally significant (F(1,57) = 3.21, p = 0.079, η² = 0.53, d = 0.47), pointing to reduced compassion after emotionally negative videos in the experimental group compared to the control group (mean difference = 3.911, SD = 0.152, F(1,57) = 4.93, p = 0.030, η² = 0.080, d = 0.59). This effect remained marginally significant
after including IQ as covariate, the main effect of valence remained significant as well (see Supplement S4).
Theory of Mind performance. The main effect of ToM performance vs. factual reasoning was not significant
in the entire sample: Performance was the same for the ToM and factual reasoning questions (see Fig. 2C and
Table 2; F(1,57) = 0.499, p = 0.483, η² = 0.0089, d = 0.019). The main effect of group was marginally significant
(F(1,57) = 3.55, p = 0.065, η² = 0.060, d = 0.506). Critically, the interaction between group and ToM was not significant (F (1,57) = 0.87, p = 0.356, η² = 0.016, d = 0.251). Including IQ as covariate did not change this pattern, but led
to a further, strong reduction of the size of the group main effect (see Supplement S4).
Relations of aggression with EmpaToM behaviour.
Corroborating the findings, RPQ scores correlated negatively across groups with empathy ratings (see Supplement S4 and S5; RPQ: r = −0.342, p = 0.004;
Scientific RepoRts | 7: 670 | DOI:10.1038/s41598-017-00745-0
2
www.nature.com/scientificreports/
Figure 1. Schematic of the EmpaToM trial sequence and task overview (adapted from Kanske et al.20).
Aggressive
Controls
d
(cohen)
MEAN
SD
MEAN
SD
t
df
p value
Age
32.172
7.700
31.706
5.713
0.276
61
0.784
−0.068
Years of education
13.966
3.268
17.203
3.108
−3.965
59
0.001***
1.012
Intelligence
95.552
11.758
105.438
10.854
−3.415
59
0.001***
0.874
−1.460
Buss-Perry-Aggression-Questionnaire
Physical Aggression
36.759
11.716
21.912
8.346
5.853
61
0.001***
Verbal Aggression
20.345
5.334
17.618
6.035
1.885
61
0.064
−0.479
Anger
25.690
8.146
17.118
5.493
4.958
61
0.001***
−0.382
Hostility
27.483
11.134
18.912
6.820
3.743
61
0.001***
−0.928
Aggression Sum Score
110.276
29.366
75.559
20.465
5.505
61
0.001***
−1.372
Reactive-Proactive Aggression Questionnaire
Proactive Aggression
5.929
5.956
1.794
2.267
3.737
60
0.001***
−0.917
Reactive Aggression
11.339
5.052
4.441
3.751
6.165
60
0.001***
−1.550
Reactive-Proactive
Aggr. Sum Score
17.268
10.160
6.235
5.549
5.430
60
0.001***
−1.348
Difficulty identifying
feelings
14.964
4.484
12.179
3.580
2.569
54
0.013**
−0.687
Difficulty describing
feelings
14.107
3.178
12.536
4.910
1.422
54
0.161
−0.380
Externally oriented
thinking
17.071
4.422
13.857
3.894
2.887
54
0.006**
0.772
Alexithymia Sum Score
46.143
6.969
38.571
7.089
4.030
54
0.001
1.077
Toronto-Alexithymia-Scale
***
Table 1. Characteristics of men with a history of aggressive behaviour and controls, Buss-Perry-AggressionQuestionnaire (BPAQ), Reactive-Proactive Aggression Questionnaire (RPQ) and (Toronto-AlexithymiaScale-26). Note: *Indicates statistical significant p-value: *p ≤ 0.05, **p ≤ 0.01, ***p ≤ 0.001.
Scientific RepoRts | 7: 670 | DOI:10.1038/s41598-017-00745-0
3
www.nature.com/scientificreports/
Figure 2. EmpaToM ratings and performance: (A) empathy ratings (emotional and neutral condition), (B)
compassion ratings (emotional and neutral condition), and (C) ToM and factual reasoning performance
(composite score of error rates and reaction time ratings, performance scores were z-transformed and for
display purpose depicted with a mean of 2) for the aggressive and the control group. Error bars represent 95%
confidence intervals.
Scientific RepoRts | 7: 670 | DOI:10.1038/s41598-017-00745-0
4
www.nature.com/scientificreports/
EmpaToM
behaviour
F
df
p value
eta²
d
Main Effect of
Group
7.91
57
0.152
0.122
0.075
Main Effect of
Valence
140.31
57
0.001***
0.711
3.16
7.910
57
0.007**
0.122
0.746
8.05
57
0.001***
0.124
0.75
Main Effect of
Group
2.119
57
0.151
0.036
0.388
Main Effect of
Valence
155.50
57
0.001***
0.732
3.327
3.21
57
0.079
0.53
0.47
4.93
57
0.030*
0.080
0.59
Main Effect of
Group
3.55
57
0.065
0.060
0.506
Main Effect of
ToM
0.499
57
0.483
0.0089
0.019
Interaction
0.87
57
0.356
0.016
0.251
Empathy
Interaction
Post-hoc
MeanDiff = −1.107
Compassion
Interaction
Post-hoc
MeanDiff = 3.911
ToM
Table 2. EmpaToM measures analysed by means of separate repeated-measures analyses of variance. Note:
*Indicates statistical significant p-value: *p ≤ 0.05, **p ≤ 0.01, ***p ≤ 0.001.
Figure 3. Mediation model for the effect of aggressive behaviour on empathic responses, alexithymia is
modelled as mediator.
BPAQ: r = −3.22, p = 0.048 n.s. after Bonferroni correction) and compassion ratings (see Supplement S4 and S5;
RPQ: r = −0.355, p = 0.006, BPAQ: r = −0.132, p = 0.319 n.s.), but not with ToM performance (BPAQ: r = 0.072,
p = 0.589; RPQ: r = 0.089, p = 0.505).
Relations of alexithymia with aggression and EmpaToM behaviour.
Alexithymia and
Aggression. Participants with a history of aggressive behaviour reported significantly higher scores of alexithymia than controls (see Table 1). Across groups, alexithymia was correlated with aggression as measured in the
BPAQ (see Supplement S3 and S6; r = 0.37, p = 0.005) and the RPQ (rs = 0.32, p = 0.017).
Alexithymia and EmpaToM measures. Empathy and compassion correlated negatively across groups with alexithymia (see Supplement S3 and S6; empathy: r = −0.35, p = 0.001, compassion: rs = −0.36, p = 0.016). There
was no significant correlation between ToM performance and alexithymia (r = 0.137, p = 0.332). Interestingly,
compassion and empathy scores correlated negatively with the TAS subscale “externally oriented thinking”
(empathy ratings: r = −0.374, p = 0.006; compassion ratings: r = −0.525, p < 0.001), but not with ToM scores
after Bonferroni correction (r = −0.247, p = 0.078).
Pathmodel of alexithymia in aggression. Mediation analysis42 was used to test the hypothesis that the
empathy deficit in aggressive participants is mediated by increased alexithymia (see Fig. 3). This analysis revealed
a significant relationship between group (men with a history of aggressive behaviour vs. controls) and empathy ratings (c path: coeff = 0.4988, se = 0.2126, t = 2.3457, p = 0.0229). This relationship was statistically not significant when alexithymia was included as mediator (c’ path: effect = 0.2248, se = 0.2528, t = 8892, p = 0.3781).
Furthermore, the mediator variable (alexithymia scores) was associated with both group (coeff = −6.4686,
se = 1.8870, t = −3.4279, p = 0.0012) and empathy ratings (coeff = −0.0424, se = 0.0168, t = −2.5193, p = 0.0150).
Scientific RepoRts | 7: 670 | DOI:10.1038/s41598-017-00745-0
5
www.nature.com/scientificreports/
Bootstrapping procedures were used to test the significance of the mediation effect. The bias-corrected bootstrap
confidence interval for the indirect effect (c path) based on 1000 bootstrap samples was above 0 (0.0774–0.6125).
Additionally, a partial correlation analysis was conducted between group affiliation, empathy ratings, and alexithymia scores to validate these results. As expected, no significant correlation was found (rs = 0.145, p = 0.306).
In conclusion, the mediation analysis revealed alexithymia as crucial mediator for lower empathy ratings in men
with a history of aggressive behaviour. Given that groups differed with regard to verbal IQ and years of education, mediation analyses were repeated using these variables as covariates (see Supplement S7), which altered the
results.
To further assess the influence of verbal IQ and years of education, within-group correlation analyses were
carried out between both empathy and compassion measures and verbal IQ, as well as between both empathy and
compassion measures and years of education (see Supplement S8). These analyses did not show an association
between empathy and compassion measures on the one hand and measures of intelligence and education on
the other. Although the interaction effect for the compassion ratings in the EmpaToM task was only marginally
significant, an exploratory mediation analysis was conducted, which showed that alexithymia does not mediate
reduced compassion in the experimental vs. control group (see Supplement S7).
Discussion
The present study yields several new insights into the role of social understanding and alexithymia for aggressive
behaviour. Firstly, men with a history of aggressive behaviour showed decreased sharing of negative affect with
others, indicating diminished empathy, and reduced compassion after emotionally negative videos. Secondly, no
ToM deficit was found, demonstrating intact cognitive perspective-taking in men with a history of aggressive
behaviour. These results were observed both when comparing men with and without a history of aggressive
behaviour and when correlating aggression severity with empathy, compassion and ToM. Thirdly, the empathy
deficit in men with a history of aggressive behaviour was mediated by increased alexithymia.
The results of the present study confirm the hypothesised link between aggression and impaired social understanding, showing that it is a deficit in feeling another person’s pain, but not the reasoning about their motives,
intentions, and goals, that allows crossing personal boundaries and inflicting bodily harm. Thus, the present data
clarify the on-going questions of whether and how aggression relates to impaired social understanding. While
previous meta-analyses yielded largely inconsistent evidence22, 24, the clear results observed here speak for an
experimental operationalization of social understanding, which, in contrast to the mostly applied questionnaire
assessments, is not subject to response tendencies, for example related to social desirability. It also seems critical
to test the different aspects of social understanding within the same individuals to allow conclusions about their
specific impairment. Lastly, replicating group differences with correlational data validates the observed relationships as suggested by Vachon et al.24 and by Mariano et al.43.
The observed deficit in healthy men with a history of aggressive behaviour in affective social understanding is in line with evidence from psychopathology. For instance, psychopathy, which is characterised by severe
antisocial behaviour, has been related to reduced empathic responses, while Theory of Mind performance is not
affected44–49. A similar pattern has been reported in patients with narcissistic personality disorder, who also show
reduced prosocial behaviour50, 51. A primary lack of empathy and compassion is also found in frontotemporal
dementia and, more generally, the frontal lobe syndrome. Paralleling our present findings, studies of these conditions reported a lack of empathy and compassion associated with elevated levels of aggressive behaviour52–56.
Violent behaviour toward others and themselves has also been reported in some patients with autism spectrum disorder57, 58, which is mainly associated with deficits in ToM, but not empathy37, 59, 60. However, prevalence
for alexithymia is largely increased in autism and can lead to reduced empathic responses in autistic individuals as
well31, thus raising the question of whether the aggressive behaviour is primarily associated with the ToM deficits
or rather alexithymia37. The present findings highlight that the relationship between lack of empathy and aggressive behaviour is not confined to people with psychiatric disorders but is also crucial in understanding aggression
in healthy individuals, such as criminal offenders.
In line with our findings, recent studies reported that criminal offenders had no deficits in judging other people’s behaviour as right or wrong – possibly indicating intact ToM – but had deficits in sharing the suffering of
other people43, as well as deficits in emotion recognition and empathy in ecological, context-sensitive measures61.
Our findings are also in line with investigations that link enhanced social understanding to prosocial behaviour4, 23, 62, 63, 64 possibly through enhanced early detection of others’ emotions13, 20. While the specific and relative contributions of empathy, compassion and ToM to prosocial behaviour are not yet entirely clear, some first
evidence demonstrated that training in compassion-focused meditation can increase helping and non-selfish
behaviour in interactive game paradigms65, 66. This may be an avenue for future intervention studies in chronically
aggressive individuals.
Alexithymia has already been shown to play an important role in empathic responses, which was replicated
in this study28, 36, 38, 39, 67. In General, alexithymia, as the ability to empathise with other people’s emotional states
relies on parts of those networks that are involved when the emotional states are experienced by oneself, difficulties in identifying one’s own feelings seem to be paralleled by reduced empathy31. The present findings suggest that
the empathy deficit in men with a history of aggressive behaviour is mediated by increased alexithymia, suggesting that it may actually be aberrant alexithymia that brings about reduced empathic responses. Further suggestions for the relation of alexithymia to aggression have been made by Zillmann68, assuming that monitoring one’s
own level of excitement is crucial for leaving dangerous situations, which people with high levels of alexithymia
may consequently be unable to do69. Furthermore, awareness of one’s own emotions is correlated with tolerating
negative emotions70, and a reduced capacity to identify emotions results in more maladaptive coping-styles71, 72.
Training emotional awareness may, therefore, be another promising approach in psychotherapeutic intervention.
Scientific RepoRts | 7: 670 | DOI:10.1038/s41598-017-00745-0
6
www.nature.com/scientificreports/
There are some limitations to the present study. On average the group of men with history of aggressive behaviour scored lower on all measures of education and intelligence. When years of education and verbal IQ were
used as covariates in our analyses, the results of the group-by-valence interaction and the group difference in
the negative valence condition remained largely the same, while the mediating effect of alexithymia on empathic
responding did not remain significant. It is thus acknowledged that we cannot fully exclude that differences in
education and IQ may play a role and that future studies in groups matched for education and IQ will have to
replicate the present findings. In line with conceptual considerations, the present data did, however, not reveal
a correlation between empathy measures and years of education or IQ nor between compassion measures and
years of education or IQ, when the two groups were analysed separately (see Supplement S8). Thus, empathy and
compassion and the deficits therein observed in the group of men with a history of aggressive behaviour seem not
to be linked with education and intelligence. In contrast, one may rather have expected differences in education
and IQ to affect performance in ToM73. Strikingly, we found no group difference in ToM measures, suggesting
again that, in the present study, group differences do not simply and unspecifically occur due to differences in
education and intelligence74.
A second point concerns the ratings in the EmpaToM, which are still subjective in nature. However, the
EmpaToM ratings have previously been shown to directly trace neural responses in empathy related brain
regions on a trial-wise level and also correspond to changes in heart rate20. Future studies in aggression should,
nevertheless, include more of such objective measures, in particular to elucidate the influence of differences in
alexithymia on subjective and objective affective social understanding. Despite the exclusion of DSM-IV Axis I
and II disorders, psychopathy67 and other inter-individual difference characteristics such as cognitive schemata
and scripts75, 76 were not assessed. Future research should include such measures to test the specific relations to
aggressive behaviour. Lastly, we only tested aggression in men. While the prevalence for physical aggression, in
particular, is much lower in women77, it still remains to be tested whether the same mechanisms observed here
can be generalised to women.
To conclude, based on the finding that affective and cognitive routes to understanding others are distinct and
can be assessed separately20, we investigated the role that deficits in these social functions play for aggressive
behaviour. We observed a selective deficit in affective responses, but not cognitive perspective-taking, in men
with a history of aggressive behaviour, which suggests that it is the sharing of others’ emotions and feeling for
them, that inhibit aggression. Deficits in cognitive understanding of others’ mental states, however, do not play
a critical role for aggressive behaviour. Selectivity of the impairment also corroborates the separation of affective
and cognitive routes to social understanding. Furthermore, as alexithymia mediates reduced empathic responses
in men with a history of aggressive behaviour, the present results underline the importance of awareness of one’s
own emotions for affect sharing and allow suggestions for future developments in psychotherapeutic treatment
to include emotional awareness training.
Methods
Participants. A total sample of N = 63 participants (all male, all without mental disorders) was recruited via
flyers that were posted in online communities and via focus groups that were directly contacted. With N = 29
in the aggressive group (participants with a history of aggressive behaviour) and N = 34 in the control group.
Participants with history of aggression were included if they had committed at least one criminal act of assault or
grievous bodily harm with deceitful intent, such as attempted homicide, knife assaults causing bone fractures or
injuries of vital organs, or physical assault resulting in brain bleeding and fractures at the base of the skull78 (note
that this did not always result in incarceration, but could also be punished with community service or psychological treatment). All participants were screened by a clinical psychologist to exclude any Axis I or II disorder and
drug abuse within the last 6 months using the Structured Clinical Interview for DSM-IV I & II79. There were no
significant age differences between the two groups (see Table 1), but significant differences between school leaving
qualifications, and length of formal education. The Wortschatztest (WST), a German vocabulary and speech comprehension test, was used to evaluate verbal intelligence80. The test is a German equivalent of the National Adult
Reading Test (NART)81. The sum scores of the WST were converted to IQ scores, which also differed significantly
between the groups, possibly because the members of the aggressive group left formal education earlier.
The methods of the present study adhere to the Declaration of Helsinki (1964) and all experimental protocols
were approved by the ethics committee of the Charité – Universitätsmedizin Berlin (number EA1/119/13). All
participants gave written informed consent prior to participation.
Questionnaires. Differences in aggressive behaviour between the groups were assessed using:
(1). The Buss-Perry-Aggression-Questionnaire (BPAQ, Buss and Perry82), which is one of the most widely used
self-report tools to assess aggression. The German revised version was used83 for the present study84. The
BPAQ consists of 29 items forming four subscales (physical and verbal aggression, anger and hostility). The
sum score is used as an indicator of overall “dispositional aggression”.
(2). The Reactive-Proactive Aggression Questionnaire (RPQ, Raine et al.85), which assesses reactive aggression
(RA) and proactive-aggression (PA) and are added up to a sum score. This consists of 23 items, 11 measuring RA, 12 PA on a 3-point-scale.
Additionally, the Toronto- Alexithymia-Scale-26 (TAS-26, Taylor et al.25; rev. German version Kupfer et al.86)
was assessed to test for differences in alexithymia. It consists of 18 Items forming 3 subscales (difficulty identifying feelings, difficulty describing feelings, externally oriented thinking). The sum score is used as an indicator of
overall alexithymia.
Scientific RepoRts | 7: 670 | DOI:10.1038/s41598-017-00745-0
7
www.nature.com/scientificreports/
Task. The EmpaToM task20 was employed to assess empathy, compassion and ToM (see Fig. 1). In a series of
neuroimaging studies, these different measures of the EmpaToM have been validated with external tasks and
self-reports. The EmpaToM consists of 48 short video (~15 s) sequences that differ in emotional valence (negative
vs. neutral). Videos are followed by two rating questions (each 4 s), asking for (1) the valence of the current emotional state (negative – neutral – positive, empathy measure) and (2) the level of compassion felt for the person in
the video (none – very much, compassion measure). Participants were presented with sliding rating scales without numbers, but for analysis, the responses in the ratings were coded on a scale from −3 (negative) to +3 (positive). A subsequent multiple-choice question (max. 15 s) either demanded a ToM inference or factual reasoning
(control condition) on the content of the previous video (ToM performance measure). Lastly, a confidence rating
(4 s) probes meta-cognition by asking participants how confident they were when choosing the correct response
in the previous question. We excluded the latter aspect from the present analysis because it was not the main focus
of the current research aims.
®
®
Data analysis. All statistical analyses were performed using IBM SPSS Statistics Version 22. Effect
sizes are based on Cohen87 and Rosenthal88. Normal distribution was tested using the Shapiro-Wilk-Test (see
Supplement S1) and the used variables did not significantly deviate from a normal distribution (all p > 0.05).
Therefore, parametric tests were used for the statistical analysis (ANOVA, Pearson’s product-moment-correlation).
The ratings (affect, compassion) and performance measure of ToM (error rates and reaction times in the
questions were combined into one z-transformed and averaged composite score (for each condition), see Kanske
et al.20) were analysed by means of separate repeated-measures analyses of variance (ANOVAs). A 2 × 2 factorial
design was applied with the within-subject factors Emotionality of Video (emotionally negative vs. neutral videos) and a between-subject factor group (aggressive vs. control participants) to analyse empathy and compassion
ratings. For simplification the empathy-scoring scheme was multiplied by minus one so that high scores in the
rating system reflect high empathic responding. ToM performance was analysed with a 2 × 2 factorial design with
the within-subject factors ToM (ToM versus factual reasoning) and the between-subject factor group (aggressive
vs. control participants). Significance was set at p < 0.05. Post hoc analyses were performed using a univariate
ANOVA with Bonferroni correction for multiple comparisons (p = 0.05/3 = 0.017).
To test for associations with aggression and alexithymia questionnaires, the EmpaToM measures were correlated with the BPAQ, RPQ and TAS. Bonferroni correction was applied to account for multiple testing (p ≤ 0.017).
Lastly, a mediation analysis was calculated to elucidate whether alexithymia mediates a putative empathy deficit
in men with a history of aggressive behaviour. As participants could not be matched for intelligence and years of
education we repeated all analyses including IQ and years of education as covariates to confirm that the results
were not influenced by different IQ scores or years of education.
References
1. Federal Bureau of Investigation. Crime in the United States (2014).
2. Björkqvist, K., Österman, K. & Kaukiainen, A. Social intelligence− empathy = aggression? Aggress. Violent Behav. 5, 191–200 (2000).
3. DeWall, C. N., Anderson, C. A. & Bushman, B. J. The general aggression model: theoretical extensions to violence. Psychol. Violence
1, 245–258, doi:10.1037/a0023842 (2011).
4. Eisenberg, N., Eggum, N. D. & Di Giunta, L. Empathy‐related responding: Associations with prosocial behavior, aggression, and
intergroup relations. Soc. Issues Policy Rev. 4, 143–180, doi:10.1111/sipr.2010.4.issue-1 (2010).
5. Baron, R. A. & Richardson, D. R. Human aggression (Plenum, 1994).
6. Bushman, B. J. & Anderson, C. A. Is it time to pull the plug on hostile versus instrumental aggression dichotomy? Psychol. Rev. 108,
273–9, doi:10.1037/0033-295X.108.1.273 (2001).
7. Bushman, B. J. & Huesmann, L. R. Short-term and long-term effects of violent media on aggression in children and adults. Arch.
Pediatr. Adolesc. Med. 160, 348–352, doi:10.1001/archpedi.160.4.348 (2006).
8. Geen, R. G. Human Aggression (Milton Keynes: Open University Press 2001).
9. Richardson, D. R., Hammock, G. S., Smith, S. M., Gardner, W. & Signo, M. Empathy as a cognitive inhibitor of interpersonal
aggression. Aggress. Behav. 20, 275–289, doi:10.1002/(ISSN)1098-2337 (1994).
10. Association, A. P. Diagnostic and statistical manual of mental disorders (DSM-5 ) (American Psychiatric Pub, 2013).
11. Hare, R. D. & Neumann, C. S. Psychopathy as a clinical and empirical construct. Annu. Rev. Clin. Psychol. 4, 217–246, doi:10.1146/
annurev.clinpsy.3.022806.091452 (2008).
12. Mokros, A. et al. Variants of psychopathy in adult male offenders: A latent profile analysis. J. Abnorm. Psychol. 124, 372–386,
doi:10.1037/abn0000042 (2015).
13. Kanske, P., Böckler, A. & Singer, T. Models, Mechanisms and Moderators Dissociating Empathy and Theory of Mind. Curr. Top.
Behav. Neurosci. 30, 193–206, doi:10.1007/978-3-319-47429-8 (2017).
14. Engen, H. G. & Singer, T. Empathy circuits. Curr. Opin. Neurobiol. 23, 275–282, doi:10.1016/j.conb.2012.11.003 (2013).
15. Bernhardt, B. C. & Singer, T. The neural basis of empathy. Neuroscience 35, 1–23, doi:10.1146/annurev-neuro-062111-150536
(2012).
16. Frith, C. & Frith, U. Theory of mind. Curr. Biol. 15, R644–646, doi:10.1016/j.cub.2005.08.041 (2005).
17. Mitchell, J. P. The false dichotomy between simulation and theory-theory: the argument’s error. Trends in cognitive sciences 9,
363–364, 10.1016/j.tics.2005.06.010, author reply 364 (2005).
18. Premack, D. & Woodruff, G. Does the chimpanzee have a theory of mind? Behav. Brain. Sci. 1, 515–526, doi:10.1017/
S0140525X00076512 (1978).
19. Kanske, P., Böckler, A., Trautwein, F.-M., Parianen Lesemann, F. H. & Singer, T. Are strong empathizers better mentalizers? Evidence
for independence and interaction between the routes of social cognition. Soc. Cogn. Affect. Neurosci. 9, 1383–1392, doi:10.1093/
scan/nsw052 (2016).
20. Kanske, P., Böckler, A., Trautwein, F.-M. & Singer, T. Dissecting the social brain: Introducing the EmpaToM to reveal distinct neural
networks and brain–behavior relations for empathy and Theory of Mind. Neuroimage 122, 6–19, doi:10.1016/j.
neuroimage.2015.07.082 (2015).
21. Valk, S. L. et al. Socio-cognitive phenotypes differentially modulate large-scale structural covariance networks. Cereb. Cortex (in
press).
22. Jolliffe, D. & Farrington, D. P. Empathy and offending: A systematic review and meta-analysis. Aggress. Violent Behav 9, 441–476,
doi:10.1016/j.avb.2003.03.001 (2004).
®
Scientific RepoRts | 7: 670 | DOI:10.1038/s41598-017-00745-0
8
www.nature.com/scientificreports/
23. Miller, P. A. & Eisenberg, N. The relation of empathy to aggressive and externalizing/antisocial behavior. Psychol. Bull. 103, 324–344,
doi:10.1037/0033-2909.103.3.324 (1988).
24. Vachon, D. D., Lynam, D. R. & Johnson, J. A. The (non)relation between empathy and aggression: surprising results from a metaanalysis. Psychol. Bull. 140, 751–773, doi:10.1037/a0035236 (2014).
25. Taylor, G. J., Parker, J. D. & Bagby, R. M. Emotional intelligence and the emotional brain: points of convergence and implications for
psychoanalysis. J. Am. Acad. Psychoanal. 27, 339–354 (1999).
26. Ates, M. A. et al. The relationship between alexithymia, aggression and psychopathy in young adult males with antisocial personality
disorder/Antisosyal kisilik bozuklugu olan genc erkeklerde aleksitimi, saldirganlik ve psikopati iliskisi. Arch. Clin. Neuropsychol. 46,
135–140 (2009).
27. Konrath, S., Novin, S. & Li, T. Is the relationship between alexithymia and aggression context-dependent? Impact of group
membership and belief similarity. Pers. Individ. Dif 53, 329–334, doi:10.1016/j.paid.2012.04.004 (2012).
28. Guttman, H. & Laporte, L. Alexithymia, empathy, and psychological symptoms in a family context. Compr. Psychiatry 43, 448–455,
doi:10.1053/comp.2002.35905 (2002).
29. Teten, A. L., Miller, L. A., Bailey, S. D., Dunn, N. J. & Kent, T. A. Empathic deficits and alexithymia in trauma-related impulsive
aggression. Behav. Sci. Law 26, 823–832, doi:10.1002/bsl.v26:6 (2008).
30. Demers, L. A. & Koven, N. S. The relation of alexithymic traits to affective theory of mind. Am. J. Psychol. 128, 31–42, doi:10.5406/
amerjpsyc.128.1.0031 (2015).
31. Bird, G. et al. Empathic brain responses in insula are modulated by levels of alexithymia but not autism. Brain 133, 1515–1525,
doi:10.1093/brain/awq060 (2010).
32. Patil, I. & Silani, G. Alexithymia increases moral acceptability of accidental harms. J. Cogn. Psychol. (Hove) 26, 597–614, doi:10.108
0/20445911.2014.929137 (2014).
33. Patil, I. & Silani, G. Reduced empathic concern leads to utilitarian moral judgments in trait alexithymia. Front. Psychol. 5, 10.3389/
fpsyg.2014.00501 (2014).
34. Patil, I., Melsbach, J., Hennig-Fast, K. & Silani, G. Divergent roles of autistic and alexithymic traits in utilitarian moral judgments in
adults with autism. Sci. Rep. 6, 23637, doi:10.1038/srep23637 (2016).
35. Patil, I., Young, L., Sinay, V. & Gleichgerrcht, E. Elevated moral condemnation of third-party violations in multiple sclerosis patients
in Soc. Neurosci. 1–22 (2016).
36. Aaron, R. V., Benson, T. L. & Park, S. Investigating the role of alexithymia on the empathic deficits found in schizotypy and autism
spectrum traits. Pers. Individ. Dif. 77, 215–220, doi:10.1016/j.paid.2014.12.032 (2015).
37. Brewer, R. et al. The impact of autism spectrum disorder and alexithymia on judgments of moral acceptability. J. Abnorm. Psychol.
124, 589–95, doi:10.1037/abn0000076 (2015).
38. Jonason, P. K. & Krause, L. The emotional deficits associated with the Dark Triad traits: Cognitive empathy, affective empathy, and
alexithymia. Pers. Individ. Dif. 55, 532–537, doi:10.1016/j.paid.2013.04.027 (2013).
39. Grynberg, D., Luminet, O., Corneille, O., Grèzes, J. & Berthoz, S. Alexithymia in the interpersonal domain: A general deficit of
empathy? Pers. Individ. Dif. 49, 845–850, doi:10.1016/j.paid.2010.07.013 (2010).
40. Lane, R. D., Hsu, C.-H., Locke, D. E. C., Ritenbaugh, C. & Stonnington, C. M. Role of theory of mind in emotional awareness and
alexithymia: Implications for conceptualization and measurement. Conscious. Cogn. 33, 398–405, doi:10.1016/j.concog.2015.02.004
(2015).
41. Moriguchi, Y. et al. Impaired self-awareness and theory of mind: An fMRI study of mentalizing in alexithymia. Neuroimage 32,
1472–1482, doi:10.1016/j.neuroimage.2006.04.186 (2006).
42. Preacher, K. J. & Hayes, A. F. Assessing mediation in communication research in The Sage sourcebook of advanced data analysis
methods for communication research (eds Hayes, A. F., Slater, M. D. & Snyder, L. B.) 13–54 (Sage, 2008).
43. Mariano, M., Pino, M. C., Peretti, S., Valenti, M. & Mazza, M. Understanding criminal behavior: Empathic impairment in criminal
offenders. Soc. Neurosci. 1–7 (in press).
44. Blair, R. J. R. Applying a cognitive neuroscience perspective to the disorder of psychopathy. Dev. Psychopathol. 17, 865–891 (2005).
45. Brook, M. & Kosson, D. S. Impaired cognitive empathy in criminal psychopathy: Evidence from a laboratory measure of empathic
accuracy. J. Abnorm. Psychol. 122, 156–66, doi:10.1037/a0030261 (2013).
46. Dolan, M. & Fullam, R. Theory of mind and mentalizing ability in antisocial personality disorders with and without psychopathy.
Psychol. Med. 34, 1093–1102, doi:10.1017/S0033291704002028 (2004).
47. Goldberg, B. R. et al. Predictors of aggression on the psychiatric inpatient service: Self-esteem, narcissism, and theory of mind
deficits. J. Nerv. Ment. Dis. 195, 436–442, doi:10.1097/01.nmd.0000253748.47641.99 (2007).
48. Kosson, D. S., Lorenz, A. R. & Newman, J. P. Effects of comorbid psychopathy on criminal offending and emotion processing in male
offenders with antisocial personality disorder. J. Abnorm. Psychol. 115, 798–806, doi:10.1037/0021-843X.115.4.798 (2006).
49. Richell, R. A. et al. Theory of mind and psychopathy: can psychopathic individuals read the ‘language of the eyes’? Neuropsychologia
41, 523–526, doi:10.1016/S0028-3932(02)00175-6 (2003).
50. Campbell, W. K., Bush, C. P., Brunell, A. B. & Shelton, J. Understanding the social costs of narcissism: The case of the tragedy of the
commons. Pers. Soc. Psychol. Bull 31, 1358–1368, doi:10.1177/0146167205274855 (2005).
51. Ritter, K. et al. Lack of empathy in patients with narcissistic personality disorder. Psychiatry. Res. 187, 241–247, doi:10.1016/j.
psychres.2010.09.013 (2011).
52. Baez, S. et al. Primary empathy deficits in frontotemporal dementia. Front. Aging Neurosci. 6, 262, doi:10.3389/fnagi.2014.00262
(2014).
53. Baez, S. et al. Orbitofrontal and limbic signatures of empathic concern and intentional harm in the behavioral variant frontotemporal
dementia. Cortex 75, 20–32, doi:10.1016/j.cortex.2015.11.007 (2016).
54. Hirono, N., Mega, M. S., Dinov, I. D., Mishkin, F. & Cummings, J. L. Left frontotemporal hypoperfusion is associated with aggression
in patients with dementia. Arch. Neurol. 57, 861–866, doi:10.1001/archneur.57.6.861 (2000).
55. Mendez, M. F., Chen, A. K., Shapira, J. S. & Miller, B. L. Acquired Sociopathy and Frontotemporal Dementia. Dement. Geriatr. Cogn.
Disord. 20, 99–104, doi:10.1159/000086474 (2005).
56. Yang, Y. & Raine, A. Prefrontal structural and functional brain imaging findings in antisocial, violent, and psychopathic individuals:
a meta-analysis. Psychiatry Res. 174, 81–88, doi:10.1016/j.pscychresns.2009.03.012 (2009).
57. Allely, C. et al. Violence is rare in autism: when it does occur, is it sometimes extreme? Psychol. 151(1), 49–68, doi:10.1080/0022398
0.2016.1175998 (2017).
58. Im, D. S. Template to perpetrate: an update on violence in autism spectrum disorder. Harv. Rev. Psychiatry 24, 14–35, doi:10.1097/
HRP.0000000000000087 (2016).
59. Dziobek, I. et al. Dissociation of cognitive and emotional empathy in adults with Asperger syndrome using the Multifaceted
Empathy Test (MET). J. Autism Dev. Disord. 38, 464–473, doi:10.1007/s10803-007-0486-x (2008).
60. Frith, U. & Happe, F. Autism spectrum disorder. Curr. Biol. 15, R786–790, doi:10.1016/j.cub.2005.09.033 (2005).
61. Gonzalez-Gadea, M. L. et al. Emotion recognition and cognitive empathy deficits in adolescent offenders revealed by contextsensitive tasks. Front. Hum. Neurosci. 8, 850, doi:10.3389/fnhum.2014.00850 (2014).
62. Masten, C. L., Morelli, S. A. & Eisenberger, N. I. An fMRI investigation of empathy for ‘social pain’ and subsequent prosocial
behavior. Neuroimage 55, 381–388, doi:10.1016/j.neuroimage.2010.11.060 (2011).
Scientific RepoRts | 7: 670 | DOI:10.1038/s41598-017-00745-0
9
www.nature.com/scientificreports/
63. Morelli, S. A., Rameson, L. T. & Lieberman, M. D. The neural components of empathy: predicting daily prosocial behavior. Soc.
Cogn. Affect. Neurosci. 9, 39–47, doi:10.1093/scan/nss088 (2014).
64. Tusche, A., Böckler, A., Kanske, P., Trautwein, F. M. & Singer, T. Decoding the charitable brain: Empathy, perspective taking, and
attention shifts differentially predict altruistic giving. J. Neurosci 36, 4719–4732, doi:10.1523/JNEUROSCI.3392-15.2016 (2016).
65. Leiberg, S., Klimecki, O. & Singer, T. Short-term compassion training increases prosocial behavior in a newly developed prosocial
game. PLoS ONE 6, e17798, doi:10.1371/journal.pone.0017798 (2011).
66. Weng, H. Y. et al. Compassion training alters altruism and neural responses to suffering. Psychol. Sci. 24, 1171–1180,
doi:10.1177/0956797612469537 (2013).
67. Lockwood, P., Bird, G., Bridge, M. & Viding, E. Dissecting empathy: high levels of psychopathic and autistic traits are characterized
by difficulties in different social information processing domains. Front. Hum. Neurosci. 7, 760, doi:10.3389/fnhum.2013.00760
(2013).
68. Zillmann, D. Transfer of excitation in emotional behavior in Social psychophysiology: A sourcebook (eds Cacioppo, J. T. & Petty, R. E.)
(Guilford Press, 1983).
69. Kroner, D. G. & Forth, A. E. The Toronto alexithymia scale with incarcerated offenders in Pers. Individ. Dif. 19, 625–634,
doi:10.1016/0191-8869(95)00116-N (1995).
70. Wilkowski, B. M. & Robinson, M. D. Guarding against hostile thoughts: trait anger and the recruitment of cognitive control.
Emotion 8, 578–583, doi:10.1037/1528-3542.8.4.578 (2008).
71. Gohm, C. L. & Clore, G. L. Four latent traits of emotional experience and their involvement in well-being, coping, and attributional
style. Cogn. Emot. 16, 495–518, doi:10.1080/02699930143000374 (2002).
72. Roberton, T., Daffern, M. & Bucks, R. S. Emotion regulation and aggression. Aggress. Violent Behav. 17, 72–82, doi:10.1111/j.19393938.2011.01125.x (2012).
73. Bjorklund, D. F. & Kipp, K. Social cognition, inhibition, and theory of mind: The evolution of human intelligence in The Evolution
of Intelligence (eds Sternbergand, R. J. & Kaufmann, J. C.) 27-54 (Lawrence Erlbaum, 2002).
74. Hühnel, I., Fölster, M., Werheid, K. & Hess, U. Empathic reactions of younger and older adults: No age related decline in affective
responding. J. Exp. Soc. Psychol. 136–143 (2014).
75. Seager, J. A. Violent Men The Importance of Impulsivity and Cognitive Schema. Crim. Justice Behav. 32, 26–49,
doi:10.1177/0093854804270625 (2005).
76. Jensen-Campbell, L. A., Knack, J. M., Waldrip, A. M. & Campbell, S. D. Do Big Five personality traits associated with self-control
influence the regulation of anger and aggression? J. Res. Pers 41, 403–424, doi:10.1016/j.jrp.2006.05.001 (2007).
77. Office, F. C. P. Police Crime Statistics of the Federal Republic of Germany (2014).
78. Rengier, R. Strafrecht Besonderer Teil II. Delikte gegen die Personund die Allgemeinheit: Grundrisse des Rechts Vol. 16 (Beck,
2015).
79. Wittchen, H.-U., Zaudig, M. & Fydrich, T. SKID. Strukturiertes Klinisches Interview für DSM-IV. Achse I und II. Handweisung
(Hogrefe, 1997).
80. Schmidt, K. H. & Metzler, P. Wortschatztest:WST (Beltz, 1992).
81. Nelson, H. E. National Adult Reading Test (NART) (Nfer-Nelson, 1982).
82. Buss, A. H. & Perry, M. The Aggression Questionnaire. J. Pers. Soc. Psychol. 63, 452–459, doi:10.1037/0022-3514.63.3.452 (1992).
83. Amelang, M. & Bartussek, D. Differential psychology and personality research (Kohlhammer, 2001).
84. von Collani, G. & Werner, R. Self-related and motivational constructs as determinants of aggression.: An analysis and validation of a
German version of the Buss–Perry Aggression Questionnaire. Pers. Individ. Dif. 38, 1631–1643, doi:10.1016/j.paid.2004.09.027 (2005).
85. Raine, A. et al. The Reactive-Proactive Aggression Questionnaire: Differential Correlates of Reactive and Proactive Aggression in
Adolescent Boys. Aggress. Behav. 32, 159–171, doi:10.1002/ab.20115 (2006).
86. Kupfer, J., Brosig, B. & Brähler, E. Toronto-Alexithymie-Skala-26: TAS-26; deutsche Version (Hogrefe, 2001).
87. Cohen, J. Statistical power analysis for the behavioral sciences Vol. 2 (Erlbaum, 1988).
88. Rosenthal, R. Parametric measures of effect size in The Handbook of Research Synthesis (eds Cooper, H. & Hedges, L. V.) 231–244
(Sage, 1994).
Acknowledgements
The present study was supported by the Max Planck Society, the German Federal Ministry of Education and
Research (BMBF 01KR1207C to F.B.) and the German Research Foundation (DFG BE 2611/2-1 to F.B.). We
would like to express our gratitude to the participants for their engagement in this research and thereby making
it possible.
Author Contributions
K.W., F.B., T.S., P.K. contributed to the study design, K.W. recruited and assessed the participants, K.W., S.S., P.K.
performed the statistical analyses, K.W., P.K. wrote the first draft and prepared the final manuscript, with feedback
from the other authors.
Additional Information
Supplementary information accompanies this paper at doi:10.1038/s41598-017-00745-0
Competing Interests: The authors declare that they have no competing interests.
Publisher's note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and
institutional affiliations.
Open Access This article is licensed under a Creative Commons Attribution 4.0 International
License, which permits use, sharing, adaptation, distribution and reproduction in any medium or
format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this
article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the
material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the
copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
© The Author(s) 2017
Scientific RepoRts | 7: 670 | DOI:10.1038/s41598-017-00745-0
10