The World Journal of Biological Psychiatry, 2014; 15: 479–487
ORIGINAL INVESTIGATION
Reduced embodied simulation in psychopathy
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DANIELA MIER1, LEILA HADDAD1, KERSTEN DIERS2, HARALD DRESSING1, ANDREAS MEYER-LINDENBERG1 & PETER KIRSCH1 1Central
Institute of Mental Health, Medical Faculty Mannheim/University of Heidelberg, Mannheim, Germany, and University of Dresden, Dresden, Germany
2Technical
Abstract Objectives. Psychopathy is characterized by severe deficits in emotion processing and empathy. These emotional deficits might not only affect the feeling of own emotions, but also the understanding of others’ emotional and mental states. The present study aims on identifying the neurobiological correlates of social-cognitive related alterations in psychopathy. Methods. We applied a social-cognitive paradigm for the investigation of face processing, emotion recognition, and affective Theory of Mind (ToM) to 11 imprisoned psychopaths and 18 healthy controls. Functional magnetic resonance imaging was used to measure task-related brain activation. Results. While showing no overall behavioural deficit, psychopathy was associated with altered brain activation. Psychopaths had reduced fusiform activation related to face processing. Related to affective ToM, psychopaths had hypoactivation in amygdala, inferior prefrontal gyrus and superior temporal sulcus, areas associated with embodied simulation of emotions and intentions. Furthermore, psychopaths lacked connectivity between superior temporal sulcus and amygdala during affective ToM. Conclusions. These results replicate findings of alterations in basal face processing in psychopathy. In addition, they provide evidence for reduced embodied simulation in psychopathy in concert with a lack of communication between motor areas and amygdala which might provide the neural substrate of reduced feeling with others during social cognition. Key words: psychopathy, social cognition, functional magnetic resonance imaging, mirror neuron system, amygdala
Introduction Psychopathy is a personality disorder that is marked by significant emotional deficits. These emotional deficits affect not only the recognition of the psychopath’s own emotions, but also the feeling for others. Intriguingly, despite these signs of emotional detachment, psychopaths show superficial charm and can be effectively manipulative (Hare and Neumann 2008). This pattern is especially interesting, because it suggests some intact social-cognitive abilities, in the presence of severe emotional deficits. One of the diagnostic features of psychopathy is a lack of empathy (Hare and Neumann 2008); the ability to feel with others. Being able to show an emotional reaction to the fate of someone else is highly dependent on our social-cognitive abilities, such as emotion recognition and Theory of Mind (ToM) that help us understanding the emotional as well as mental states of others (Blair 2005). On the
neural level empathy is associated with activation in areas belonging to the human mirror neuron system (see below) as well as with activation in insula and amygdala (Carr et al. 2003). Interestingly, it was shown that emotion recognition and affective ToM – the understanding of affective mental states and their emotional impact – rely exactly on the same brain areas as empathy, namely areas of the human mirror neuron system and amygdala (Mier et al. 2010a), pointing to a common ground of empathy and social cognition and with this suggesting a link to social-cognitive deficits in psychopathy. Indeed, there is ample evidence for deficits in emotion recognition (for a review see Marsh and Blair 2008) in psychopathy, while studies on ToM abilities in psychopathy reveal heterogeneous results, leading Blair (2005) to conclude that psychopaths have no ToM deficit. Interestingly however, Shamay-Tsoory et al. (2010) showed that it is specifically the affective ToM
Correspondence: Dr Daniela Mier, Department of Clinical Psychology, J5, Central Institute of Mental Health, Mannheim, Germany. Tel: 49 621 1703 6512. Fax: 49 621 1703 6505. E-mail: [email protected] (Received 16 July 2013 ; accepted 27 February 2014 ) ISSN 1562-2975 print/ISSN 1814-1412 online © 2014 Informa Healthcare DOI: 10.3109/15622975.2014.902541
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that is affected in psychopathy, but not cognitive ToM, suggesting the core social-cognitive dysfunction in psychopathy to be emotional. Studies investigating the neurobiological correlates of social cognition in psychopathy are still limited. To our knowledge, until now there was no functional imaging study that applied an explicit emotion recognition or ToM-task to psychopaths. However, there are some studies giving evidence for aberrant face processing, a necessary pre-requisite for facial emotion recognition (Mier et al. 2010a). Deely et al. (2006) found reduced fusiform activation in response to fearful emotional expressions in psychopaths, leading to the conclusion of a deficit in face processing in psychopathy. Other studies in which clinical or student populations with psychopathic traits were investigated give support for a reduced amygdala response to facial expressions in psychopathy (Gordon et al. 2004; Dolan and Fullam 2009). Moreover, reduced connectivity between amygdala and prefrontal areas has been demonstrated (Motzkin et al. 2011), supporting the notion of a reduced ability in psychopathy to integrate emotional and cognitive information, as e.g., necessary in affective ToM (Shamay-Tsoory et al. 2010). Since psychopathy is marked by reduced empathy, as well as deficits in social cognition, one could additionally imagine alterations in areas of the mirror neuron system (MNS). The MNS is the place where a direct mapping of observed and own motor expressions occurs (Gallese and Goldman 1998). Hence, the understanding of others via activation in the MNS is thought to occur via embodied simulation (Gallese 2007), respectively direct perception (Gallagher 2008). Areas that belong to the human MNS are the inferior prefrontal gyrus, the inferior parietal lobe, and the associated superior temporal sulcus (STS; Iacoboni et al. 2001; Rizzolatti and Craighero 2004). To our knowledge, there are only two studies investigating MNS functioning in psychopathy. Fecteau et al. (2008) investigated college students with differing psychopathy traits. Rather unexpected, the authors found a positive relationship between MNS activation in response to empathy elicited by videos of pain induction and coldheartedness (Fecteau et al. 2008). Sommer and colleagues showed psychopaths cartoon stories in combination with an emotional attribution task. The authors found evidence for activation in parts of the MNS in a forensic control sample, but not in psychopaths. However, group comparison was not significant (Sommer et al. 2010). Taken together, results from behavioural studies, investigating social-cognitive processes in psychopathy point to a deficit in the recognition of emotions and affective mental states. Studies set up
to investigate the neural correlates of social-cognition in psychopathy are still rare and point to alterations in face-processing, going along with hypoactivation of amygdala and fusiform gyrus, while, to our knowledge, studies on the neuronal correlates of ToM are still missing. The present study aimed on: (a) replicating results of altered face-processing in psychopathy, as reflected in amygdala and fusiform hypoactivation, (b) defining alterations in areas that are related to the embodied simulation of mental states (i.e., areas of the human MNS), and (c) exploring possible aberrations in connectivity between areas of the MNS and the amygdala. For these purposes, a paradigm was applied that allows the investigation of face-processing, emotion recognition, and affective ToM, that was shown to activate fusiform gyrus, and amygdala, as well as areas of the MNS (Mier et al. 2010a).
Methods and materials Sample Eleven male inmate subjects with psychopathy and 18 male control subjects participated in the study (two more subjects with psychopathy had been recruited, but one had to be excluded due to strong movement, and one due to gross brain abnormalities). Inmates were recruited from forensic hospitals and had been already detained for 127.73 months on average (SD 86.77) at the time of study participation. They had diagnoses of personality disorders and/or disorders of sexual preference and were sentenced to forensic psychiatry due to assault, murder and/or sexual offences, and rape. None of them had a history of substance abuse within the last 2 years. Psychopathy was assessed based on the Psychopathy Check List (PCL-R) by an experienced psychiatrist. Average PCL score was 26.67 (range 25–29). Two of the patients received antidepressive medication. Control subjects matched for age, school education and estimates for crystalline (Lehrl 1999) as well as fluid IQ (Horn 1983) were recruited via local announcements (see Table I). None of the control subjects had a history of lifetime psychiatric or neurological disorder, as assessed by self-reports. To assess psychopathic traits in the control group, control subjects completed the German version of the Psychopathy Personality Inventory (Eisenbarth and Alpers 2007) with an average score of 326.53 (SD 26.18), resembling the average score reported in the validation study by Eisenbarth and Alpers (2007) from a male student population (mean 325.42, SD 24.92). All subjects were monetarily reimbursed for their participation. Before participating in the study, subjects were thoroughly informed
Reduced embodied simulation in psychopathy 481 Table I. Demographic information for both groups.
Demographic information Age (years) School education (years) Crystalline intelligence (IQ) Fluid intelligence (IQ)
Psychopaths 44.55 9.45 102.05 106.47
(8.97) (1.37) (15.69) (11.00)
Healthy controls 44.00 (10.35) 10.11 (1.13) 106.08 (12.03) 109.00 (10.37)
Significance T(27) 0.15 T(27) 1.40 T(27) 0.78 T(27) 0.62
(P 0.87) (P 0.17) (P 0.44) (P 0.54)
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Results are reported in means and standard deviations in brackets; Crystalline intelligence was assessed with the Mehrfach-Wortwahl-Test (MWTB) and fluid intelligence with two subtests (LPS3 and LPS4) of the Leistungsprüfsystem (LPS). Raw scores from the intelligence measures were converted with help of the according norm tables into the intelligence quotient normal distribution with a mean of 100 and a standard deviation of 15.
about study procedures and gave written informed consent. The study was approved by the local ethics board of the University of Heidelberg and conducted in accordance with the declaration of Helsinki.
goggles (Resonance Technology Inc., Northridge, USA).
Experimental task
Blood oxygen level-dependent (BOLD) fMRI was performed on a 3.0-Tesla Siemens TRIO system (Siemens, Erlangen) using an echo-planar-imaging sequence with the following scanning parameters: repetition time (TR) 2000 ms, echo time (TE) 30 ms, flip angle 80°, 64 64 matrix, 32 4-mm axial slices with 1-mm gap). Prior to the functional imaging a T1-weighted MPRage (TR 1570 ms, TE 2.75 ms, flip angle 15°, 256 256 matrix, 176 1-mm slices) was acquired for all subjects to control anatomies for gross structural aberrations.
The applied paradigm is described in detail elsewhere (Mier et al. 2010a,b) and has been successfully used to investigate alterations in social cognition in schizophrenia, and borderline personality disorder (Mier et al. 2010b, 2013). In brief, with this paradigm, three stages of social cognition are assessed by different conditions within one experiment: (i) affective ToM, (ii) emotion recognition, and (iii) neutral face processing. These stages are operationalized by the presentation of statements that differ in their emotional, respectively intentional content, followed by face photographs. The task is to evaluate the matching of picture and preceding statement. The face photographs have an emotional (happy, angry, or fearful) expression, in the emotion recognition, and in the affective ToM condition, and a neutral one in the neutral face processing condition. The paradigm is suitable to: (a) investigate general aberrations in face processing (main effect of group), and (b) to investigate aberrations that are associated with specific social-cognitive processes (interaction between group and stage). The statements are presented for 2 s and the photographs for a maximum of 2 s, which can be terminated by the subject’s response. A fixation cross is shown during the inter-trial interval for 2 s, on average (0.5–3.5 s jitter). Conditions are presented in a pseudo-randomized order. An example for the conditions is presented in Figure 1. The paradigm was presented and behavioural responses recorded with Presentation Presentation V.9.50 (Neurobehavioral Systems, Albany, CA). Responses were given with a Lumitouch optical response device (Photon Control Inc., Burnaby, Canada). The stimuli were presented to the participants via VisuaStim video
Functional magnetic resonance imaging data acquisition
Data analysis Functional brain imaging data was analysed with SPM5 (http://www.fil.ion.ucl.ac.uk/spm/). Prior to data analysis, images were preprocessed to correct for motion artefacts, acquisition time and interindividual differences in brain anatomy. For this purpose, data was realigned, slice time corrected, normalized to the EPI-template, and smoothed with an 8-mm Gaussian kernel. In a first level analysis a model was set-up for each subject. This model contained three regressors (affective ToM, emotion recognition, neutral face processing) with onsets of those trials that were solved correctly, and a further regressor with the onsets of all trials with wrong answers, independent of the respective stage. In addition, the six realignment parameters derived from preprocessing were included into the model to control for possible remaining movement related variance. Regressors were folded with a stick function and convolved with a synthetic hemodynamic response function, as implemented in SPM5. Second-level random-effects analyses were investigated by applying a full-factorial model (3 conditions 2
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Figure 1. Experimental design, with an example for each of the three conditions. ToM affective theory of mind; Emotion emotion recognition; Neutral neutral face processing; ITI inter-trial interval.
groups) to the resulting contrasts from the firstlevel. To explore not only possible alterations in activity, but also in the strength of connectivity between key areas of the social cognition network, psychophysiological interactions (PPI) were analysed. For this purpose, first the point of coordinates with the highest activation in the contrast affective ToMneutral face processing was defined by applying the above described full-factorial model. Second, the time series around this point of coordinates (right STS: 57 –57 12) were extracted with a sphere of 8 mm. To assure having variance in the time series for each subject no significance threshold was set. These extracted time series were deconvolved, adjusted for task influences, and the interaction term was modelled, using the PPI-function as implemented in SPM5. A new first level model was set-up for each subject with the parameters derived from the PPI, with the psychophysiological interaction as regressor of interest. The resulting contrasts were analysed on the second level with one-sample and two-sample t-tests. Significance threshold for whole brain analyses was set to P 0.001 uncorrected. These results are reported in the Supplementary Tables I–IV available online at http://www.informahealthcare.com/doi/ abs/10.3109/15622975.2014.902541. In addition, region of interest (ROI) analyses were conducted for the amygdala, BA 44, STS, and fusiform gyrus.
Masks were taken from the wfu_pickatlas (http:// fmri.wfubmc.edu/software/PickAtlas). The mask for BA 44 was smoothed with a 1-mm 3D kernel. The mask for the superior temporal sulcus was created from activation in the STS in a previous study (Mier et al. 2010a). Significance threshold for ROI-analyses was set to P 0.05 small volume-corrected. Behavioural data were analysed with SPSS (Version 20). Reaction times, as well as the performance (percentage of correct answers) were compared between groups with ANOVAs (3 conditions 2 groups). In addition, Pearson’s product moment correlations were calculated to analyze the relationship of the performance between conditions, and between psychopathic pathology and performance.
Results Behavioural data Analysis of task performance (percentage of correct answers) revealed neither a significant main effect of group, nor a main effect of condition, or a group condition interaction (all P values 0.1). Analysis of reaction times revealed a significant main effect of condition (F(2;27) 15.35, P 0.001), but also no differences between groups (all P values 0.1). Correlation between performance and PCL score revealed trends for a negative correlation between
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Reduced embodied simulation in psychopathy 483 affective ToM performance and PCL score (r –0.589, P 0.062) and emotion recognition performance and PCL score (r –0.541, P 0.085), but not for performance in the neutral face condition and PCL score (r 0.076, P 0.824). In addition, the correlation between affective ToM and emotion recognition performance was analysed as a measure of “normal behaviour”, since a correlation between these performances has been demonstrated repeatedly in healthy controls (Mier et al., 2010a,b, 2013), but not necessarily in patients (Brune 2005; Mier et al. 2010b). These correlation analyses revealed a significant relationship in the control group (r 0.59, P 0.010), but not in the psychopathy group (r 0.19, P 0.57). Functional imaging data Task-associated activation in the healthy controls replicates previous findings with this paradigm (Mier et al. 2010a,b, 2013). The hypothesized pattern of increasing activation with increasing need to recognize emotions and intentions (neutral emotion recognitionaffective ToM) was found in bilateral STS, inferior prefrontal gyrus (S1), and with ROI analyses in bilateral amygdala (left coordinates: –27 –3 –24, T 2.39, P 0.086 (trend), sv corrected, k 10; right coordinates: 24 –9 –21, T 2.73, P 0.043, sv corrected, k 22). In the psychopaths there was no area that showed such an activation pattern at the given threshold of P 0.001 uncorrected, neither did the ROI analyses reveal any areas with a comparable activation pattern, except for a trend in right amygdala (coordinates: 21 –3 –24, T 2.47, P 0.091, sv corrected, k 11). Since we were interested in differences between groups in the processing of facial information the main effect of group was analysed, revealing a hypoactivation of right fusiform gyrus in the psychopathy group (coordinates: 24 –54 –12, T 3.71, P 0.038, sv corrected; k 162), but revealed no further significant group differences. In addition, we were interested in differences between groups that cannot be generalized to face processing per se, but to differences in specific socialcognitive abilities. For this purpose, we analysed the interaction between the groups and conditions. When investigating an increase of activation with the increasing need to put oneself into the shoes of another person in the healthy controls (neutral emotion recognition affective ToM), that is not evident in the psychopathic subjects (Figure 2), we found significant activation differences between groups in bilateral STS (left coordinates: –48 –51 15, T 4.84, P 0.001, sv corrected; k 206; right
coordinates: 57 –51 12, T 3.36, P 0.024, sv corrected; k 30), BA44 (left coordinates: –57 18 9, T 3.30, P 0.040, sv corrected; k 134; right coordinates: 60 18 6, T 3.48, P 0.025, sv corrected; k 69), and left amygdala (coordinates: –21 –3 –15, T 2.74, P 0.040, sv corrected; k 19). The reversed interaction contrast gave no significant results. Between group comparisons of the single conditions, revealed stronger activation in the control subjects than in the psychopathic subjects in right fusiform gyrus (coordinates: 24 –54 –12, T 4.15, P 0.011, sv corrected, k 200) and left amygdala (coordinates: –18 –3 –18, T 2.86, P 0.031, sv corrected, k 22) during affective ToM. Comparison of groups in the neutral face processing condition revealed a trend for stronger activation in the healthy controls in right fusiform gyrus again (coordinates: 24 –57 –15, T 3.42, P 0.083, sv corrected, k 129). No other comparisons of brain activation between groups were significant. Moreover, no significant correlations between performance and brain activation occurred either across all participants or within the groups. To account for the possibility that fusiform gyrus hypoactivation in the psychopathy group influenced the above reported group differences, ROI analyses were rerun with average fusiform gyrus activation over all conditions (extracted with an 8-mm sphere around the peak voxel in the whole group) as covariate. Applying this covariate did not change the results, all effects remained significant (P 0.05 sv corrected), suggesting that these results cannot be reduced to the between group difference in fusiform activation. ROI analysis of right STS connectivity with other key areas of the social-cognitive network revealed a positive association with the left amygdala (coordinates: –21 –3 –15, T 3.31, P 0.033, sv corrected, k 41) in the healthy controls. ROI analyses showed no areas with significant negative connectivity to the right STS. Neither ROI analysis of positive, nor of negative connectivity revealed a significant association in the psychopaths. Group comparison showed that the connectivity to the left amygdala was significantly stronger in the healthy controls than in the psychopaths (coordinates: –18 –3 –27, T 2.81, P 0.048, sv corrected; k 6). Discussion The present study was designed to investigate neural correlates of social cognition in psychopathy. Based on theoretical assumptions and previous studies, it was hypothesized that psychopaths would have
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Figure 2. Group by condition interactions: (a) display of group by condition interactions in left amygdala (P 0.005 for display purposes); (b) mean activation change in left amygdala, displayed separately for the two groups and three conditions; (c) display of group by condition interactions in cortical regions (P 0.001); (d) mean activation change in left BA 44, displayed separately for the two groups and three conditions; (e) mean activation change in left superior temporal sulcus, displayed separately for the two groups and three conditions. Note: the mean activation changes are displays of means and according standard deviations. PP, psychopaths; HC, healthy controls; ToM, affective theory of mind; Emo, emotion recognition; Neutral, neutral face processing.
reduced activation in amygdala and fusiform gyrus related to face processing, alterations in areas of the MNS related to affective ToM, and altered connectivity between areas of the MNS and the amygdala. To test these assumptions we applied a socialcognitive task that allows the investigation of general face processing, as well as emotion recognition and affective ToM to 11 male psychopaths and 18 matched healthy controls. While both groups performed equally well overall, there was some evidence for altered social-cognitive processing in the psychopathy group. Patients with higher psychopathy scores tended to have more deficits in emotion recognition and affective ToM. In addition, we did not find a correlation between the psychopaths’ emotion recognition and affective ToM performance. This correlation between emotion
recognition and ToM performance was demonstrated in several studies in healthy controls and a lack of this correlation seems to be a marker for aberrant socialcognitive processing (Mier et al. 2010b). Moreover, we found alterations of the functioning in key areas of the social-cognitive network in psychopathy. In accordance with the study by Deely et al. (2006), we found fusiform, but not amygdala, hypoactivation in psychopaths in response to face stimuli. The fusiform gyrus is a higher order visual area, believed to be specialized for the processing of faces (Kanwisher et al. 1997; Saygin et al. 2011). In addition, activation in the fusiform gyrus was shown to be expertise dependent (Bilalic et al. 2011), and modulated by attention to the emotional content of faces (Monroe et al. 2013). Hence, this fusiform hypoactivation in psychopathy points to a basal
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Reduced embodied simulation in psychopathy 485 deficit in the processing of (emotional) faces. However, it should be noted that this hypoactivation seems to have no influence on further group by condition interactions in this study, since applying average fusiform gyrus activation as covariate did not change the results discussed below. In addition to this task-independent hypoactivation, we found evidence for alterations related to higher-order social cognition. First, psychopaths did not show the increased utilization of STS, BA44 and amygdala with increasing demand to recognize feelings, respectively intentions of the depicted persons. It was argued that activation in the MNS leads to a direct, automatic understanding of and feeling with others; i.e., embodied simulation (Gallese 2007) and several studies showed an involvement of MNS as well as amygdala to emotion recognition and empathy (Carr et al. 2003; Mier et al. 2010a,b). Hypoactivation in these areas points towards an impaired automatic matching of emotions and intentions in psychopathy, hence a reduced capacity for embodied simulation. In his review in 2005, Blair describes three forms of empathy: cognitive empathy that he equates with ToM, motor empathy equating with imitation and MNS functioning, and emotional empathy equating the feeling with others. The author concludes from the literature that psychopaths have only a deficit in emotional empathy, but not in cognitive empathy or motor empathy (that, however, had not been tested up to this date). The results from the present study do not only support Blairs’ (2005) assumption of an emotional empathy deficit in psychopathy, but also point to a deficit in motor empathy (Blair 2005). As mentioned above, we found no significant deficit in the psychopathy group on the behavioural level. While the current literature suggests a pronounced deficit in affective aspects of social cognition in psychopaths (Shamay-Tsoory et al. 2010), not all studies support this assumption (Dolan and Fullam 2004; Domes et al. 2013). Especially interesting in this context seems a study by Dolan and Fullham (2004). The authors found no deficit in the recognition of Faux Pas in a sample of psychopaths, but in the understanding of the emotional impact such a Faux Pas can have. These results support the clinical observation that psychopaths can be effectively manipulative (what should require an intact ToM), but are unable to empathize with others. The results from our study are in good agreement with this clinical observation, too. While psychopaths were not affected in their understanding of emotional and mental states, they showed reduced activation in areas associated with emotional, as well as motor empathy. Second, and even more intriguing in this context, we found reduced connectivity between right STS
and left amygdala in psychopaths during affective ToM as compared to the neutral face processing condition. Shamay-Tsoory et al. (2010) suggested that an orbitofrontal cortex dysfunction in psychopaths results in a split between representations of mental states and their affective value leading to intact cognitive ToM, but deficient affective ToM. What we find in the present study, investigating affective ToM, is reduced activation in areas representing the motor state of others (Gallese and Goldman 1998), reduced activation in an area representing the affective value of this state (Carr et al. 2003), and a reduced coupling between these areas. Iacoboni et al. (2001) showed that the right STS is an important component of the human imitation system and seems to act as an integration area for motor input from other MNS areas. Our results give evidence that the STS is not only an important area for the integration of motor-related information, but might be the area in which motor information is fed into the amygdala during affective ToM. This conclusion is also in agreement with Blairs’ (2005) empathy theory. He reviewed that the STS is a central component for all forms of empathy and with this might be the connecting point between cognition, motoric and emotion. Hence, reduced amygdala activation during affective ToM might be caused by reduced input from the MNS, which seems to be hypoactive itself in psychopathy. It is tempting to speculate about causes of this hypoactivation in areas of the MNS. One possible explanation is that the hypoactivation is a result of the psychopaths’ emotional detachment. In the concept of embodied simulation, it is assumed that we are able to understand others by representing their (motor) state in the same network that represents our own (motor) states (Gallese 2007). Hence, the reduced ability of psychopaths to experience strong emotions for themselves might be in turn impairing their ability to embody – and subsequently empathize with – strong emotions of others. Consequently, it could be that before cognitive approaches, or imitation trainings are applied to improve empathy in psychopathy, psychopaths need to start feeling empathy for themselves. A promising therapeutic approach to this end might be the treatment of psychopaths by focused schema therapy. This approach has been under investigation in the Netherlands for a couple of years and preliminary evidence for its success in treating emotional deficits in psychopaths has been presented (Bernstein et al. 2007; van den Broek et al. 2011). Independent from the causes, the finding of reduced embodied simulation, possibly causing weaker STS–amygdala connectivity might explain why psychopaths are not able to feel with others
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486 D. Mier et al. although possessing a cognitive representation of their emotions and intentions and might provide one piece of the puzzle explaining antisocial behaviour in this condition. The study has several limitations. First of all, the psychopathic sample was small, resulting in limited power to detect group differences, and to reveal significant correlations between measures of psychopathy and performance. Second, we restricted our sample to males, preventing generalization to the whole psychopathic population. While there is consensus that females are underrepresented in the psychopath population, there is an ongoing discussion about prevalence and nature of female psychopathy (Wynn et al. 2012). It would be of particular interest whether the profile of female psychopaths particularly differs in the social domain. Due to the mentioned limitations, the results have to be seen as preliminary. Hence, future studies are needed, incorporating bigger samples to: (a) investigate the exact nature and consequences of the fusiform gyrus hypoactivation in psychopathy, (b) apply more difficult affective ToM tasks that also involve orbitofrontal cortex in addition to MNS and amygdala functioning, and (c) explore whether gender differences can be observed for the social-cognitive aberrations found here. Moreover, it should be mentioned that the brain areas we are discussing to be involved in embodied simulation (Gallese 2007) have a vast amount of different functions. By summarizing their activation under the aspect of embodied simulation we are neglecting other important functions of these brain regions. However, since these regions have been found to be co-activated for all core processes of social cognition, namely imitation (Iacoboni et al. 2001), empathy (Carr et al. 2003), emotion recognition and ToM (Mier et al. 2010a), we believe that in the process of social cognition the most plausible interpretation of these regions’ functionality is the embodied simulation of emotional and mental states of others. In conclusion, the results of the present study provide evidence that on top of alterations in basal face processing mechanisms, the automatic matching of the emotional and motor state of others; i.e., embodied simulation, is compromised in male psychopaths. Furthermore, the results point to a lack of information flow from these areas representing the motor state of others to areas representing its affective value, which might cause psychopaths to have a diminished capacity to feel with others through impaired embodied simulation. Acknowledgements We thank Dagmar Gass for assistance with data collection.
Statement of Interest None to declare.
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Reduced embodied simulation in psychopathy 487 Marsh AA, Blair RJ. 2008. Deficits in facial affect recognition among antisocial populations: a meta-analysis. Neurosci Biobehav Rev 32:454–465. Mier D, Lis S, Esslinger C, Sauer C, Hagenhoff M, Ulferts J, et al. 2013. Neuronal correlates of social cognition in borderline personality disorder. Soc Cogn Affect Neurosci 8:531–537. Mier D, Lis S, Neuthe K, Sauer C, Esslinger C, Gallhofer B, et al. 2010a. The involvement of emotion recognition in affective theory of mind. Psychophysiology 47:1028–1039. Mier D, Sauer C, Lis S, Esslinger C, Wilhelm J, Gallhofer B, et al. 2010b. Neuronal correlates of affective theory of mind in schizophrenia out-patients: evidence for a baseline deficit. Psychol Med 40:1607–1617. Monroe JF, Griffin M, Pinkham A, Loughead J, Gur RC, Roberts TP, et al. 2013. The fusiform response to faces: explicit versus implicit processing of emotion. Hum Brain Mapp 34:1–11. Motzkin JC, Newman JP, Kiehl KA, Koenigs M. 2011. Reduced prefrontal connectivity in psychopathy. J Neurosci 31:17348–17357.
Supplementary material available online Supplementary Tables I–IV.
Rizzolatti G, Craighero L. 2004. The mirror-neuron system. Annu Rev Neurosci 27:169–192. Saygin ZM, Osher DE, Koldewyn K, Reynolds G, Gabrieli JD, Saxe RR. 2011. Anatomical connectivity patterns predict face selectivity in the fusiform gyrus. Nat Neurosci 15:321–327. Shamay-Tsoory SG, Harari H, Aharon-Peretz J, Levkovitz Y. 2010. The role of the orbitofrontal cortex in affective theory of mind deficits in criminal offenders with psychopathic tendencies. Cortex 46:668–677. Sommer M, Sodian B, Dohnel K, Schwerdtner J, Meinhardt J, Hajak G. 2010. In psychopathic patients emotion attribution modulates activity in outcome-related brain areas. Psychiatry Res 182:88–95. van den Broek E, Keulen-de Vos M, Bernstein DP. 2011. Arts therapies and Schema Focused therapy: A pilot study. Arts Psychother 38:325–332. Wynn R, Hoiseth MH, Pettersen G. 2012. Psychopathy in women: theoretical and clinical perspectives. Int J Womens Health 4:257–263.
ORIGINAL INVESTIGATION
Reduced embodied simulation in psychopathy
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DANIELA MIER1, LEILA HADDAD1, KERSTEN DIERS2, HARALD DRESSING1, ANDREAS MEYER-LINDENBERG1 & PETER KIRSCH1 1Central
Institute of Mental Health, Medical Faculty Mannheim/University of Heidelberg, Mannheim, Germany, and University of Dresden, Dresden, Germany
2Technical
Abstract Objectives. Psychopathy is characterized by severe deficits in emotion processing and empathy. These emotional deficits might not only affect the feeling of own emotions, but also the understanding of others’ emotional and mental states. The present study aims on identifying the neurobiological correlates of social-cognitive related alterations in psychopathy. Methods. We applied a social-cognitive paradigm for the investigation of face processing, emotion recognition, and affective Theory of Mind (ToM) to 11 imprisoned psychopaths and 18 healthy controls. Functional magnetic resonance imaging was used to measure task-related brain activation. Results. While showing no overall behavioural deficit, psychopathy was associated with altered brain activation. Psychopaths had reduced fusiform activation related to face processing. Related to affective ToM, psychopaths had hypoactivation in amygdala, inferior prefrontal gyrus and superior temporal sulcus, areas associated with embodied simulation of emotions and intentions. Furthermore, psychopaths lacked connectivity between superior temporal sulcus and amygdala during affective ToM. Conclusions. These results replicate findings of alterations in basal face processing in psychopathy. In addition, they provide evidence for reduced embodied simulation in psychopathy in concert with a lack of communication between motor areas and amygdala which might provide the neural substrate of reduced feeling with others during social cognition. Key words: psychopathy, social cognition, functional magnetic resonance imaging, mirror neuron system, amygdala
Introduction Psychopathy is a personality disorder that is marked by significant emotional deficits. These emotional deficits affect not only the recognition of the psychopath’s own emotions, but also the feeling for others. Intriguingly, despite these signs of emotional detachment, psychopaths show superficial charm and can be effectively manipulative (Hare and Neumann 2008). This pattern is especially interesting, because it suggests some intact social-cognitive abilities, in the presence of severe emotional deficits. One of the diagnostic features of psychopathy is a lack of empathy (Hare and Neumann 2008); the ability to feel with others. Being able to show an emotional reaction to the fate of someone else is highly dependent on our social-cognitive abilities, such as emotion recognition and Theory of Mind (ToM) that help us understanding the emotional as well as mental states of others (Blair 2005). On the
neural level empathy is associated with activation in areas belonging to the human mirror neuron system (see below) as well as with activation in insula and amygdala (Carr et al. 2003). Interestingly, it was shown that emotion recognition and affective ToM – the understanding of affective mental states and their emotional impact – rely exactly on the same brain areas as empathy, namely areas of the human mirror neuron system and amygdala (Mier et al. 2010a), pointing to a common ground of empathy and social cognition and with this suggesting a link to social-cognitive deficits in psychopathy. Indeed, there is ample evidence for deficits in emotion recognition (for a review see Marsh and Blair 2008) in psychopathy, while studies on ToM abilities in psychopathy reveal heterogeneous results, leading Blair (2005) to conclude that psychopaths have no ToM deficit. Interestingly however, Shamay-Tsoory et al. (2010) showed that it is specifically the affective ToM
Correspondence: Dr Daniela Mier, Department of Clinical Psychology, J5, Central Institute of Mental Health, Mannheim, Germany. Tel: 49 621 1703 6512. Fax: 49 621 1703 6505. E-mail: [email protected] (Received 16 July 2013 ; accepted 27 February 2014 ) ISSN 1562-2975 print/ISSN 1814-1412 online © 2014 Informa Healthcare DOI: 10.3109/15622975.2014.902541
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that is affected in psychopathy, but not cognitive ToM, suggesting the core social-cognitive dysfunction in psychopathy to be emotional. Studies investigating the neurobiological correlates of social cognition in psychopathy are still limited. To our knowledge, until now there was no functional imaging study that applied an explicit emotion recognition or ToM-task to psychopaths. However, there are some studies giving evidence for aberrant face processing, a necessary pre-requisite for facial emotion recognition (Mier et al. 2010a). Deely et al. (2006) found reduced fusiform activation in response to fearful emotional expressions in psychopaths, leading to the conclusion of a deficit in face processing in psychopathy. Other studies in which clinical or student populations with psychopathic traits were investigated give support for a reduced amygdala response to facial expressions in psychopathy (Gordon et al. 2004; Dolan and Fullam 2009). Moreover, reduced connectivity between amygdala and prefrontal areas has been demonstrated (Motzkin et al. 2011), supporting the notion of a reduced ability in psychopathy to integrate emotional and cognitive information, as e.g., necessary in affective ToM (Shamay-Tsoory et al. 2010). Since psychopathy is marked by reduced empathy, as well as deficits in social cognition, one could additionally imagine alterations in areas of the mirror neuron system (MNS). The MNS is the place where a direct mapping of observed and own motor expressions occurs (Gallese and Goldman 1998). Hence, the understanding of others via activation in the MNS is thought to occur via embodied simulation (Gallese 2007), respectively direct perception (Gallagher 2008). Areas that belong to the human MNS are the inferior prefrontal gyrus, the inferior parietal lobe, and the associated superior temporal sulcus (STS; Iacoboni et al. 2001; Rizzolatti and Craighero 2004). To our knowledge, there are only two studies investigating MNS functioning in psychopathy. Fecteau et al. (2008) investigated college students with differing psychopathy traits. Rather unexpected, the authors found a positive relationship between MNS activation in response to empathy elicited by videos of pain induction and coldheartedness (Fecteau et al. 2008). Sommer and colleagues showed psychopaths cartoon stories in combination with an emotional attribution task. The authors found evidence for activation in parts of the MNS in a forensic control sample, but not in psychopaths. However, group comparison was not significant (Sommer et al. 2010). Taken together, results from behavioural studies, investigating social-cognitive processes in psychopathy point to a deficit in the recognition of emotions and affective mental states. Studies set up
to investigate the neural correlates of social-cognition in psychopathy are still rare and point to alterations in face-processing, going along with hypoactivation of amygdala and fusiform gyrus, while, to our knowledge, studies on the neuronal correlates of ToM are still missing. The present study aimed on: (a) replicating results of altered face-processing in psychopathy, as reflected in amygdala and fusiform hypoactivation, (b) defining alterations in areas that are related to the embodied simulation of mental states (i.e., areas of the human MNS), and (c) exploring possible aberrations in connectivity between areas of the MNS and the amygdala. For these purposes, a paradigm was applied that allows the investigation of face-processing, emotion recognition, and affective ToM, that was shown to activate fusiform gyrus, and amygdala, as well as areas of the MNS (Mier et al. 2010a).
Methods and materials Sample Eleven male inmate subjects with psychopathy and 18 male control subjects participated in the study (two more subjects with psychopathy had been recruited, but one had to be excluded due to strong movement, and one due to gross brain abnormalities). Inmates were recruited from forensic hospitals and had been already detained for 127.73 months on average (SD 86.77) at the time of study participation. They had diagnoses of personality disorders and/or disorders of sexual preference and were sentenced to forensic psychiatry due to assault, murder and/or sexual offences, and rape. None of them had a history of substance abuse within the last 2 years. Psychopathy was assessed based on the Psychopathy Check List (PCL-R) by an experienced psychiatrist. Average PCL score was 26.67 (range 25–29). Two of the patients received antidepressive medication. Control subjects matched for age, school education and estimates for crystalline (Lehrl 1999) as well as fluid IQ (Horn 1983) were recruited via local announcements (see Table I). None of the control subjects had a history of lifetime psychiatric or neurological disorder, as assessed by self-reports. To assess psychopathic traits in the control group, control subjects completed the German version of the Psychopathy Personality Inventory (Eisenbarth and Alpers 2007) with an average score of 326.53 (SD 26.18), resembling the average score reported in the validation study by Eisenbarth and Alpers (2007) from a male student population (mean 325.42, SD 24.92). All subjects were monetarily reimbursed for their participation. Before participating in the study, subjects were thoroughly informed
Reduced embodied simulation in psychopathy 481 Table I. Demographic information for both groups.
Demographic information Age (years) School education (years) Crystalline intelligence (IQ) Fluid intelligence (IQ)
Psychopaths 44.55 9.45 102.05 106.47
(8.97) (1.37) (15.69) (11.00)
Healthy controls 44.00 (10.35) 10.11 (1.13) 106.08 (12.03) 109.00 (10.37)
Significance T(27) 0.15 T(27) 1.40 T(27) 0.78 T(27) 0.62
(P 0.87) (P 0.17) (P 0.44) (P 0.54)
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Results are reported in means and standard deviations in brackets; Crystalline intelligence was assessed with the Mehrfach-Wortwahl-Test (MWTB) and fluid intelligence with two subtests (LPS3 and LPS4) of the Leistungsprüfsystem (LPS). Raw scores from the intelligence measures were converted with help of the according norm tables into the intelligence quotient normal distribution with a mean of 100 and a standard deviation of 15.
about study procedures and gave written informed consent. The study was approved by the local ethics board of the University of Heidelberg and conducted in accordance with the declaration of Helsinki.
goggles (Resonance Technology Inc., Northridge, USA).
Experimental task
Blood oxygen level-dependent (BOLD) fMRI was performed on a 3.0-Tesla Siemens TRIO system (Siemens, Erlangen) using an echo-planar-imaging sequence with the following scanning parameters: repetition time (TR) 2000 ms, echo time (TE) 30 ms, flip angle 80°, 64 64 matrix, 32 4-mm axial slices with 1-mm gap). Prior to the functional imaging a T1-weighted MPRage (TR 1570 ms, TE 2.75 ms, flip angle 15°, 256 256 matrix, 176 1-mm slices) was acquired for all subjects to control anatomies for gross structural aberrations.
The applied paradigm is described in detail elsewhere (Mier et al. 2010a,b) and has been successfully used to investigate alterations in social cognition in schizophrenia, and borderline personality disorder (Mier et al. 2010b, 2013). In brief, with this paradigm, three stages of social cognition are assessed by different conditions within one experiment: (i) affective ToM, (ii) emotion recognition, and (iii) neutral face processing. These stages are operationalized by the presentation of statements that differ in their emotional, respectively intentional content, followed by face photographs. The task is to evaluate the matching of picture and preceding statement. The face photographs have an emotional (happy, angry, or fearful) expression, in the emotion recognition, and in the affective ToM condition, and a neutral one in the neutral face processing condition. The paradigm is suitable to: (a) investigate general aberrations in face processing (main effect of group), and (b) to investigate aberrations that are associated with specific social-cognitive processes (interaction between group and stage). The statements are presented for 2 s and the photographs for a maximum of 2 s, which can be terminated by the subject’s response. A fixation cross is shown during the inter-trial interval for 2 s, on average (0.5–3.5 s jitter). Conditions are presented in a pseudo-randomized order. An example for the conditions is presented in Figure 1. The paradigm was presented and behavioural responses recorded with Presentation Presentation V.9.50 (Neurobehavioral Systems, Albany, CA). Responses were given with a Lumitouch optical response device (Photon Control Inc., Burnaby, Canada). The stimuli were presented to the participants via VisuaStim video
Functional magnetic resonance imaging data acquisition
Data analysis Functional brain imaging data was analysed with SPM5 (http://www.fil.ion.ucl.ac.uk/spm/). Prior to data analysis, images were preprocessed to correct for motion artefacts, acquisition time and interindividual differences in brain anatomy. For this purpose, data was realigned, slice time corrected, normalized to the EPI-template, and smoothed with an 8-mm Gaussian kernel. In a first level analysis a model was set-up for each subject. This model contained three regressors (affective ToM, emotion recognition, neutral face processing) with onsets of those trials that were solved correctly, and a further regressor with the onsets of all trials with wrong answers, independent of the respective stage. In addition, the six realignment parameters derived from preprocessing were included into the model to control for possible remaining movement related variance. Regressors were folded with a stick function and convolved with a synthetic hemodynamic response function, as implemented in SPM5. Second-level random-effects analyses were investigated by applying a full-factorial model (3 conditions 2
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Figure 1. Experimental design, with an example for each of the three conditions. ToM affective theory of mind; Emotion emotion recognition; Neutral neutral face processing; ITI inter-trial interval.
groups) to the resulting contrasts from the firstlevel. To explore not only possible alterations in activity, but also in the strength of connectivity between key areas of the social cognition network, psychophysiological interactions (PPI) were analysed. For this purpose, first the point of coordinates with the highest activation in the contrast affective ToMneutral face processing was defined by applying the above described full-factorial model. Second, the time series around this point of coordinates (right STS: 57 –57 12) were extracted with a sphere of 8 mm. To assure having variance in the time series for each subject no significance threshold was set. These extracted time series were deconvolved, adjusted for task influences, and the interaction term was modelled, using the PPI-function as implemented in SPM5. A new first level model was set-up for each subject with the parameters derived from the PPI, with the psychophysiological interaction as regressor of interest. The resulting contrasts were analysed on the second level with one-sample and two-sample t-tests. Significance threshold for whole brain analyses was set to P 0.001 uncorrected. These results are reported in the Supplementary Tables I–IV available online at http://www.informahealthcare.com/doi/ abs/10.3109/15622975.2014.902541. In addition, region of interest (ROI) analyses were conducted for the amygdala, BA 44, STS, and fusiform gyrus.
Masks were taken from the wfu_pickatlas (http:// fmri.wfubmc.edu/software/PickAtlas). The mask for BA 44 was smoothed with a 1-mm 3D kernel. The mask for the superior temporal sulcus was created from activation in the STS in a previous study (Mier et al. 2010a). Significance threshold for ROI-analyses was set to P 0.05 small volume-corrected. Behavioural data were analysed with SPSS (Version 20). Reaction times, as well as the performance (percentage of correct answers) were compared between groups with ANOVAs (3 conditions 2 groups). In addition, Pearson’s product moment correlations were calculated to analyze the relationship of the performance between conditions, and between psychopathic pathology and performance.
Results Behavioural data Analysis of task performance (percentage of correct answers) revealed neither a significant main effect of group, nor a main effect of condition, or a group condition interaction (all P values 0.1). Analysis of reaction times revealed a significant main effect of condition (F(2;27) 15.35, P 0.001), but also no differences between groups (all P values 0.1). Correlation between performance and PCL score revealed trends for a negative correlation between
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Reduced embodied simulation in psychopathy 483 affective ToM performance and PCL score (r –0.589, P 0.062) and emotion recognition performance and PCL score (r –0.541, P 0.085), but not for performance in the neutral face condition and PCL score (r 0.076, P 0.824). In addition, the correlation between affective ToM and emotion recognition performance was analysed as a measure of “normal behaviour”, since a correlation between these performances has been demonstrated repeatedly in healthy controls (Mier et al., 2010a,b, 2013), but not necessarily in patients (Brune 2005; Mier et al. 2010b). These correlation analyses revealed a significant relationship in the control group (r 0.59, P 0.010), but not in the psychopathy group (r 0.19, P 0.57). Functional imaging data Task-associated activation in the healthy controls replicates previous findings with this paradigm (Mier et al. 2010a,b, 2013). The hypothesized pattern of increasing activation with increasing need to recognize emotions and intentions (neutral emotion recognitionaffective ToM) was found in bilateral STS, inferior prefrontal gyrus (S1), and with ROI analyses in bilateral amygdala (left coordinates: –27 –3 –24, T 2.39, P 0.086 (trend), sv corrected, k 10; right coordinates: 24 –9 –21, T 2.73, P 0.043, sv corrected, k 22). In the psychopaths there was no area that showed such an activation pattern at the given threshold of P 0.001 uncorrected, neither did the ROI analyses reveal any areas with a comparable activation pattern, except for a trend in right amygdala (coordinates: 21 –3 –24, T 2.47, P 0.091, sv corrected, k 11). Since we were interested in differences between groups in the processing of facial information the main effect of group was analysed, revealing a hypoactivation of right fusiform gyrus in the psychopathy group (coordinates: 24 –54 –12, T 3.71, P 0.038, sv corrected; k 162), but revealed no further significant group differences. In addition, we were interested in differences between groups that cannot be generalized to face processing per se, but to differences in specific socialcognitive abilities. For this purpose, we analysed the interaction between the groups and conditions. When investigating an increase of activation with the increasing need to put oneself into the shoes of another person in the healthy controls (neutral emotion recognition affective ToM), that is not evident in the psychopathic subjects (Figure 2), we found significant activation differences between groups in bilateral STS (left coordinates: –48 –51 15, T 4.84, P 0.001, sv corrected; k 206; right
coordinates: 57 –51 12, T 3.36, P 0.024, sv corrected; k 30), BA44 (left coordinates: –57 18 9, T 3.30, P 0.040, sv corrected; k 134; right coordinates: 60 18 6, T 3.48, P 0.025, sv corrected; k 69), and left amygdala (coordinates: –21 –3 –15, T 2.74, P 0.040, sv corrected; k 19). The reversed interaction contrast gave no significant results. Between group comparisons of the single conditions, revealed stronger activation in the control subjects than in the psychopathic subjects in right fusiform gyrus (coordinates: 24 –54 –12, T 4.15, P 0.011, sv corrected, k 200) and left amygdala (coordinates: –18 –3 –18, T 2.86, P 0.031, sv corrected, k 22) during affective ToM. Comparison of groups in the neutral face processing condition revealed a trend for stronger activation in the healthy controls in right fusiform gyrus again (coordinates: 24 –57 –15, T 3.42, P 0.083, sv corrected, k 129). No other comparisons of brain activation between groups were significant. Moreover, no significant correlations between performance and brain activation occurred either across all participants or within the groups. To account for the possibility that fusiform gyrus hypoactivation in the psychopathy group influenced the above reported group differences, ROI analyses were rerun with average fusiform gyrus activation over all conditions (extracted with an 8-mm sphere around the peak voxel in the whole group) as covariate. Applying this covariate did not change the results, all effects remained significant (P 0.05 sv corrected), suggesting that these results cannot be reduced to the between group difference in fusiform activation. ROI analysis of right STS connectivity with other key areas of the social-cognitive network revealed a positive association with the left amygdala (coordinates: –21 –3 –15, T 3.31, P 0.033, sv corrected, k 41) in the healthy controls. ROI analyses showed no areas with significant negative connectivity to the right STS. Neither ROI analysis of positive, nor of negative connectivity revealed a significant association in the psychopaths. Group comparison showed that the connectivity to the left amygdala was significantly stronger in the healthy controls than in the psychopaths (coordinates: –18 –3 –27, T 2.81, P 0.048, sv corrected; k 6). Discussion The present study was designed to investigate neural correlates of social cognition in psychopathy. Based on theoretical assumptions and previous studies, it was hypothesized that psychopaths would have
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Figure 2. Group by condition interactions: (a) display of group by condition interactions in left amygdala (P 0.005 for display purposes); (b) mean activation change in left amygdala, displayed separately for the two groups and three conditions; (c) display of group by condition interactions in cortical regions (P 0.001); (d) mean activation change in left BA 44, displayed separately for the two groups and three conditions; (e) mean activation change in left superior temporal sulcus, displayed separately for the two groups and three conditions. Note: the mean activation changes are displays of means and according standard deviations. PP, psychopaths; HC, healthy controls; ToM, affective theory of mind; Emo, emotion recognition; Neutral, neutral face processing.
reduced activation in amygdala and fusiform gyrus related to face processing, alterations in areas of the MNS related to affective ToM, and altered connectivity between areas of the MNS and the amygdala. To test these assumptions we applied a socialcognitive task that allows the investigation of general face processing, as well as emotion recognition and affective ToM to 11 male psychopaths and 18 matched healthy controls. While both groups performed equally well overall, there was some evidence for altered social-cognitive processing in the psychopathy group. Patients with higher psychopathy scores tended to have more deficits in emotion recognition and affective ToM. In addition, we did not find a correlation between the psychopaths’ emotion recognition and affective ToM performance. This correlation between emotion
recognition and ToM performance was demonstrated in several studies in healthy controls and a lack of this correlation seems to be a marker for aberrant socialcognitive processing (Mier et al. 2010b). Moreover, we found alterations of the functioning in key areas of the social-cognitive network in psychopathy. In accordance with the study by Deely et al. (2006), we found fusiform, but not amygdala, hypoactivation in psychopaths in response to face stimuli. The fusiform gyrus is a higher order visual area, believed to be specialized for the processing of faces (Kanwisher et al. 1997; Saygin et al. 2011). In addition, activation in the fusiform gyrus was shown to be expertise dependent (Bilalic et al. 2011), and modulated by attention to the emotional content of faces (Monroe et al. 2013). Hence, this fusiform hypoactivation in psychopathy points to a basal
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Reduced embodied simulation in psychopathy 485 deficit in the processing of (emotional) faces. However, it should be noted that this hypoactivation seems to have no influence on further group by condition interactions in this study, since applying average fusiform gyrus activation as covariate did not change the results discussed below. In addition to this task-independent hypoactivation, we found evidence for alterations related to higher-order social cognition. First, psychopaths did not show the increased utilization of STS, BA44 and amygdala with increasing demand to recognize feelings, respectively intentions of the depicted persons. It was argued that activation in the MNS leads to a direct, automatic understanding of and feeling with others; i.e., embodied simulation (Gallese 2007) and several studies showed an involvement of MNS as well as amygdala to emotion recognition and empathy (Carr et al. 2003; Mier et al. 2010a,b). Hypoactivation in these areas points towards an impaired automatic matching of emotions and intentions in psychopathy, hence a reduced capacity for embodied simulation. In his review in 2005, Blair describes three forms of empathy: cognitive empathy that he equates with ToM, motor empathy equating with imitation and MNS functioning, and emotional empathy equating the feeling with others. The author concludes from the literature that psychopaths have only a deficit in emotional empathy, but not in cognitive empathy or motor empathy (that, however, had not been tested up to this date). The results from the present study do not only support Blairs’ (2005) assumption of an emotional empathy deficit in psychopathy, but also point to a deficit in motor empathy (Blair 2005). As mentioned above, we found no significant deficit in the psychopathy group on the behavioural level. While the current literature suggests a pronounced deficit in affective aspects of social cognition in psychopaths (Shamay-Tsoory et al. 2010), not all studies support this assumption (Dolan and Fullam 2004; Domes et al. 2013). Especially interesting in this context seems a study by Dolan and Fullham (2004). The authors found no deficit in the recognition of Faux Pas in a sample of psychopaths, but in the understanding of the emotional impact such a Faux Pas can have. These results support the clinical observation that psychopaths can be effectively manipulative (what should require an intact ToM), but are unable to empathize with others. The results from our study are in good agreement with this clinical observation, too. While psychopaths were not affected in their understanding of emotional and mental states, they showed reduced activation in areas associated with emotional, as well as motor empathy. Second, and even more intriguing in this context, we found reduced connectivity between right STS
and left amygdala in psychopaths during affective ToM as compared to the neutral face processing condition. Shamay-Tsoory et al. (2010) suggested that an orbitofrontal cortex dysfunction in psychopaths results in a split between representations of mental states and their affective value leading to intact cognitive ToM, but deficient affective ToM. What we find in the present study, investigating affective ToM, is reduced activation in areas representing the motor state of others (Gallese and Goldman 1998), reduced activation in an area representing the affective value of this state (Carr et al. 2003), and a reduced coupling between these areas. Iacoboni et al. (2001) showed that the right STS is an important component of the human imitation system and seems to act as an integration area for motor input from other MNS areas. Our results give evidence that the STS is not only an important area for the integration of motor-related information, but might be the area in which motor information is fed into the amygdala during affective ToM. This conclusion is also in agreement with Blairs’ (2005) empathy theory. He reviewed that the STS is a central component for all forms of empathy and with this might be the connecting point between cognition, motoric and emotion. Hence, reduced amygdala activation during affective ToM might be caused by reduced input from the MNS, which seems to be hypoactive itself in psychopathy. It is tempting to speculate about causes of this hypoactivation in areas of the MNS. One possible explanation is that the hypoactivation is a result of the psychopaths’ emotional detachment. In the concept of embodied simulation, it is assumed that we are able to understand others by representing their (motor) state in the same network that represents our own (motor) states (Gallese 2007). Hence, the reduced ability of psychopaths to experience strong emotions for themselves might be in turn impairing their ability to embody – and subsequently empathize with – strong emotions of others. Consequently, it could be that before cognitive approaches, or imitation trainings are applied to improve empathy in psychopathy, psychopaths need to start feeling empathy for themselves. A promising therapeutic approach to this end might be the treatment of psychopaths by focused schema therapy. This approach has been under investigation in the Netherlands for a couple of years and preliminary evidence for its success in treating emotional deficits in psychopaths has been presented (Bernstein et al. 2007; van den Broek et al. 2011). Independent from the causes, the finding of reduced embodied simulation, possibly causing weaker STS–amygdala connectivity might explain why psychopaths are not able to feel with others
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486 D. Mier et al. although possessing a cognitive representation of their emotions and intentions and might provide one piece of the puzzle explaining antisocial behaviour in this condition. The study has several limitations. First of all, the psychopathic sample was small, resulting in limited power to detect group differences, and to reveal significant correlations between measures of psychopathy and performance. Second, we restricted our sample to males, preventing generalization to the whole psychopathic population. While there is consensus that females are underrepresented in the psychopath population, there is an ongoing discussion about prevalence and nature of female psychopathy (Wynn et al. 2012). It would be of particular interest whether the profile of female psychopaths particularly differs in the social domain. Due to the mentioned limitations, the results have to be seen as preliminary. Hence, future studies are needed, incorporating bigger samples to: (a) investigate the exact nature and consequences of the fusiform gyrus hypoactivation in psychopathy, (b) apply more difficult affective ToM tasks that also involve orbitofrontal cortex in addition to MNS and amygdala functioning, and (c) explore whether gender differences can be observed for the social-cognitive aberrations found here. Moreover, it should be mentioned that the brain areas we are discussing to be involved in embodied simulation (Gallese 2007) have a vast amount of different functions. By summarizing their activation under the aspect of embodied simulation we are neglecting other important functions of these brain regions. However, since these regions have been found to be co-activated for all core processes of social cognition, namely imitation (Iacoboni et al. 2001), empathy (Carr et al. 2003), emotion recognition and ToM (Mier et al. 2010a), we believe that in the process of social cognition the most plausible interpretation of these regions’ functionality is the embodied simulation of emotional and mental states of others. In conclusion, the results of the present study provide evidence that on top of alterations in basal face processing mechanisms, the automatic matching of the emotional and motor state of others; i.e., embodied simulation, is compromised in male psychopaths. Furthermore, the results point to a lack of information flow from these areas representing the motor state of others to areas representing its affective value, which might cause psychopaths to have a diminished capacity to feel with others through impaired embodied simulation. Acknowledgements We thank Dagmar Gass for assistance with data collection.
Statement of Interest None to declare.
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