Psychiatry Research 220 (2014) 825–833

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Subjective experience of emotions and emotional empathy in paranoid schizophrenia Anja Lehmann a, Katja Bahçesular a, Eva-Maria Brockmann a, Sarah-Elisabeth Biederbick a, Isabel Dziobek b, Jürgen Gallinat a, Christiane Montag a,n a b

Department of Psychiatry and Psychotherapy, Charité University Medicine Berlin (Charité Universitätsmedizin Berlin), Campus Mitte, 10117 Berlin, Germany Cluster of Excellence “Languages of Emotion”, Affective Neuroscience and Psychology of Emotions, Freie Universität Berlin, Berlin, Germany

art ic l e i nf o

a b s t r a c t

Article history: Received 5 October 2013 Received in revised form 28 August 2014 Accepted 16 September 2014 Available online 28 September 2014

Unlike the cognitive dimensions, alterations of the affective components of empathy in schizophrenia are less well understood. This study explored cognitive and affective dimensions of empathy in the context of the subjective experience of aspects of emotion processing, including emotion regulation, emotional contagion, and interpersonal distress, in individuals with schizophrenia and healthy controls. In addition, the predictive value of these parameters on psychosocial function was investigated. Fifty-five patients with paranoid schizophrenia and 55 healthy controls were investigated using the Multifaceted Empathy Test and Interpersonal Reactivity Index, as well as the Subjective Experience of Emotions and Emotional Contagion Scales. Individuals with schizophrenia showed impairments of cognitive empathy, but maintained emotional empathy. They reported significantly more negative emotional contagion, overwhelming emotions, lack of emotions, and symbolization of emotions by imagination, but less selfcontrol of emotional expression than healthy persons. Besides cognitive empathy, the experience of a higher extent of overwhelming emotions and of less interpersonal distress predicted psychosocial function in patients. People with schizophrenia and healthy controls showed diverging patterns of how cognitive and emotional empathy related to the subjective aspects of emotion processing. It can be assumed that variables of emotion processing are important moderators of empathic abilities in schizophrenia. & 2014 Elsevier Ireland Ltd. All rights reserved.

Keywords: Social cognition Emotion processing Emotion regulation Emotional contagion Psychosocial function Multifaceted Empathy Test Subjective Experience of Emotions Scale

1. Introduction Empathy, in its broad definition, includes any phenomenon by which an individual comes to understand and/or to feel the emotional state of another through direct perception or imagination. The extreme ends of this spectrum are emotional contagion, the automatic affective resonance without self-other distinction (Hatfield and Rapson, 1998), and cognitive empathy, the understanding of others by engaging one's own representations (Preston and Hofelich, 2012) which might bear some overlap with theory of mind, the purely cognitive process of mental state inferencing (Premack and Woodruff, 1978). Empathy in the narrow sense, or “true empathy”, refers to other-directed, vicarious affective responses, and requires a clear distinction between self and other. In addition, empathy depends on emotion regulation, cognitive control and non-social cognitive functioning (Decety and Jackson, 2004; Pickup, 2008).

n

Corresponding author. Tel.: þ 49 30 2311 2969; fax: þ 49 30 2311 2903. E-mail address: [email protected] (C. Montag).

http://dx.doi.org/10.1016/j.psychres.2014.09.009 0165-1781/& 2014 Elsevier Ireland Ltd. All rights reserved.

Impairments of social cognition and empathic attunement to the social world belong to the core features of schizophrenia and seem to be highly predictive for functional outcome (Minkowski, 1953; Bora et al., 2006; Brüne, 2005a; Fett et al., 2011). However, existing evidence mainly focuses on theory of mind and the cognitive aspects of empathy in schizophrenia, while affective empathy (Derntl et al., 2009; Achim et al., 2011) and the affective preconditions of empathic attunement have drawn attention not so frequently (Brüne, 2005b). While some studies suggest alterations of emotional contagion (Falkenberg et al., 2008) and emotion regulation in schizophrenia (Van der Meer et al., 2009; Badcock et al., 2011; Kimhy et al., 2012), no research has systematically focused their relationship with empathy. This is noteworthy, as the interplay between human social and emotional behaviors and also between affect regulation and mentalizing has been an important topic of research (Fonagy et al., 2002; Ochsner, 2008; Schipper and Petermann, 2013). This study set out to investigate the cognitive and affective dimensions of empathy in the context of the subjective experience of aspects of emotion processing, including self-rated emotion regulation (Van der Meer et al., 2009; Llerena et al., 2012; Morris et al., 2012; Strauss et al., 2013), emotional contagion (Hatfield and

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Rapson, 1998; Falkenberg et al., 2008; Manera et al., 2013) and personal distress in social situations (Davis, 1983; Achim et al., 2011) in a sample of remitted patients with schizophrenia compared to matched healthy controls. In addition, we aimed to determine associations of empathy, emotional experience and contagion with functional outcome, symptoms and illness characteristics in patients. Empathic functioning and various aspects of emotion processing were investigated using a set of behavioral empathy assessments ‐ the Multifaceted Empathy Test (Dziobek et al., 2008)—as well as self-report questionnaires addressing subjective empathic functioning (Interpersonal Reactivity Index; Davis, 1983), dimensions of emotional experience (Subjective Experience of Emotions Scale; Behr and Becker, 2004) and emotional contagion (Emotional Contagion Scale; Doherty, 1997) together with clinical ratings and a neuropsychological test battery.

states. The ‘empathic concern’ scale (“I am often quite touched by things that I see happen”) comprises respondents' pro-social feelings of warmth and compassion for others. ‘Personal distress’ (“Being in a tense emotional situation scares me”) measures self-oriented feelings of anxiety and discomfort in response to the distress of others.

2. Methods

2.2.4. The Subjective Experience of Emotions Scale (SEE) The Subjective Experience of Emotions Scale (SEE; Behr and Becker, 2004) is a 42-item-self-report questionnaire. It comprises seven dimensions of the subjective experience of emotion processing: (a) ‘congruence’ (“All my emotions have the right to be just as they are”: acceptance of emotions), (b) ‘overwhelming emotions’ (“I'm so full of emotions that I can hardly stand it”: overload of aversive feelings), (c) ‘lack of emotions’ ( “I don't often feel my inner world”: emotional numbing), (d) ‘symbolization of emotion by bodily experience’ (“When I make decisions, I rely on my bodily feelings”: awareness of bodily correlates of emotion), (e) ‘symbolization by imagination’ (“In order to cope with stress it often helps me to focus on my daydreams”: positive regard for inner mental processes), (f) ‘regulation of emotions’ (“Most of the time I know how to calm down when I'm heated up”: ability to regulate one's own moods), and (g) ‘self-control’ (“When things are bubbling up inside me, unfortunately people around me can tell at once”: suppression of emotional expression). Validation studies have reported a Cronbach's α between 0.66 and 0.88. The SEE demonstrates convergent and divergent validity with conceptually similar and dissimilar measures (Behr and Becker, 2002; Watson and Lilova, 2009).

2.1. Participants The study was approved by the local ethics committee; subjects gave written informed consent. Fifty-five stabilized in- and outpatients diagnosed with paranoid schizophrenia according to DSM-IV-TR (Saß et al., 2003) were recruited from the Department of Psychiatry, Charité Universitätsmedizin Berlin. Diagnosis was confirmed using the Structured Clinical Interview for DSM-IV (SCID-I; First et al., 1995; German version: Wittchen et al., 1997). Symptom severity was assessed with the Positive and Negative Syndrome Scale (PANSS; Kay et al., 1987); global assessment of functioning (GAF; Saß et al., 2003) was performed in patients. Five PANSS subscores according to Lançon et al. (2000) were calculated to allow for a better differentiation between negative and depressive symptoms, together with the estimation of excitation, positive and cognitive symptoms. A number of 69 healthy individuals who were recruited by newspaper advertisements and screened by a psychiatrist (C.M.) with a structured interview (M.I.N.I; Sheehan et al., 1998). Fifty-five healthy participants were chosen to match the clinical sample (n¼ 55) on a 1:1 basis according to age, gender, verbal intelligence and education. Exclusion criteria for both groups were DSM-IV axis-I or axis-II disorders (except schizophrenia for patients); controls reporting axis-I mental disorders in their first-degree relatives were also excluded. Participants' characteristics are displayed in Table 1. 2.2. Measures 2.2.1. The Multifaceted Empathy Test (MET) The Multifaceted Empathy Test (MET; Dziobek et al., 2008) allows for the separate assessment of cognitive and emotional empathy. Initially developed for individuals with Asperger syndrome, (Dziobek et al., 2008), this is the first study using the MET in a sample of patients with schizophrenia. While the original MET also differentiates between emotional reactions to the depicted person and context as well as between explicit emotional empathy (the ability to share the displayed emotion) and levels of unspecific arousal, we used a modified version restricted to parameters of interest in schizophrenia studies, i. e. the scales for cognitive and explicit emotional empathy regarding the emotional state of persons. Forty photographs showing people in positively and negatively emotionally charged situations are presented. Participants are instructed to identify with the protagonist and to “feel into” the pictured emotions. To assess 1) ‘cognitive empathy’ (MET-CE), subjects are required to infer the emotional mental states of the protagonist and to select one out of four mental state descriptors. To assess 2) ‘emotional empathy’ (MET-EE), subjects are asked to rate their own tendency to share the specific emotion on a visual analog scale ranging from 0 to 9 (0 ¼ not at all, 9¼ very much). All participants received a short training before testing to ensure comprehension of the instruction. 2.2.2. The Interpersonal Reactivity Index (IRI) The Interpersonal Reactivity Index (IRI; Davis, 1983); German translation: ‘Saarbrücker Persönlichkeitsfragebogen’, SPF; Paulus, 1992) is a self-report questionnaire assessing various aspects of empathic responding. It comprises 28-items answered on a five-point Likert scale ranging from “Does not describe me well” to “Describes me very well”. The measure has four subscales, each made up of seven different items. Construct validity of the IRI scales was supported in several studies (Davis, 1983). Three relevant dimensions of the broader concept of empathic responding were used for analysis: ‘Perspective taking’ (“I believe that there are two sides to every question and try to look at them both.”) refers to the tendency to spontaneously adopt the point of view of others and to reason about their mental

2.2.3. The Emotional Contagion Scale (ECS) The Emotional Contagion Scale (ECS; Doherty, 1997); German translation by Falkenberg (2005) is a questionnaire addressing the tendency to automatically synchronize with the expressions of others and to experience other-generated emotions. Contagion to five basic emotions (love: “I melt when the one I love holds me close”, happiness: “Being with a happy person picks me up when I'm feeling down”, fear: “I notice myself getting tense when I'm around people who are stressed out”, anger: “It irritates me to be around angry people”, and sadness: “If someone I'm talking with begins to cry, I get teary-eyed”) is measured by 15 items on a five-point Likert scale. Within the validation sample, a two-factor solution with a positive subscale consisting of the love and happiness items and a negative subscale consisting of the fear, anger, and sadness items was established; reliability and construct validity in comparison to a variety of measures were proven (Doherty, 1997).

2.2.5. General cognitive function As empathy is impacted by non-social cognition (Pickup, 2008), a multiple choice vocabulary test (Mehrfachwahlwortschatztest, MWT-B; Lehrl et al., 1995) was applied to estimate verbal comprehension as a measure of ‘premorbid’ intelligence. The Wisconsin Card Sorting Test was used to assess execute function like abstract reasoning, concept formation and response adaptation to changing contextual contingencies (Heaton, 1981). 2.2.6. Statistical calculations Statistical calculations were carried out as indicated in the results section using IBM PASW Statistics 20s. Statistical significance was defined at a two-sided po 0.05. All variables apart from WCST categories and total errors were normally distributed. Group differences were determined by t-tests (two-sided); the impact of neurocognition was controlled by use of multivariate analyses of covariance (MANCOVA) and linear regression analysis as explained in the results section. For this purpose, a cognition composite score was formed by summation of z-scores of verbal IQ, WCST perseveration score and education years across both samples. To compare sub-samples with high or low empathic abilities with respect to parameters of emotional experience within each group, z-scores for MET-‘cognitive empathy’ and IRI ‘perspective taking’ as well as for MET-‘emotional empathy’ and IRI ‘empathic concern’, respectively, were calculated separately in both samples and added to create a ‘cognitive empathy composite’ (CEC) and an ‘emotional empathy composite’ (EEC) score. CEC and EEC scores were then split along the median to differentiate ‘low’ versus ‘high’ cognitive and emotional ‘empathizers’ in both groups. Partial correlation analyses including alpha-level adjustment (Bonferroni) and estimation of Fischer's z values between groups were performed as indicated in the result section and in table legends.

3. Results 3.1. Empathy measures: MET and IRI In the behavioral task (MET) significant group differences regarding ‘cognitive empathy’ (MET-CE) were found at initial t-testing (data not shown). MET-‘emotional empathy’ (EE) showed no group differences. Internal consistency was acceptable (Cronbach's α,

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Table 1 Demographic and neuropsychological data in patients and healthy controls; characteristics of patients with schizophrenia. Patients (N ¼ 55; mean 7 S.D.)

Healthy controls (N ¼55; mean 7S.D.)

Statistics

Age (year) Gender (f/m)

39.8 7 11.9 23/32

38.9 7 12.8 25/30

Education (year)

14.0 73.3

15.0 7 2.4

Verbal IQ

108.5 714.2

111.8 7 12.4

WCST total errors WCST categories completed WCST perseveration score (%) Cognition composite Zscore Onset of psychosis (year) Duration of illness (year) First/subsequent episode PANSS total score PANSS positivec PANSS negativec PANSS depressionc PANSS excitementc PANSS cognitionc GAF Medication protocol: Antipsychotic dose (CPZ-equiv.)d

23.4 7 14.3

22.8 7 18.7

T[108]¼ 0.352 χ2 ¼0.148a T[108]¼  1.793 T[108]¼  1.299 U¼ 1064.000b

5.3 7 1.3

5.3 7 1.4

U¼ 1173.500b

25.0 7 16.9

21.9 716.0

U¼ 1.359.500b

 0.077 1.80

0.3077 1.43

T[108]¼  1.242

29.8 7 10.7 10.0 77.7 12/ 43 60.17 23.7 13.2 76.9 15.9 77.3 6.3 7 3.1 6.6 7 2.6 5.2 7 2.1 65.3 7 15.1 Unmedicated: n ¼1(2%), SGA: n¼ 52(95%), FGA: n ¼ 6(11%); in addition: antidepressant: n¼ 9(16%), benzodiazepine: n¼1(2%), lithium: n¼ 3(5%), antiepileptic: n¼ 4(7%), anticholinergic: n¼ 3(5%). 407.8 7 318.1 mg (FGA: 19.5 7 92.9 mg, SGA: 388.3 7 313.6 mg).

Antipsychotic 8.9 7 7.8 treatment (years) Between-group comparisons: t-test for independent samples (two-sided). Significant results are indicated by bold type; np o0.05; nnp o 0.01; nnnp o 0.001. a

χ2-Test. Mann–Whitney-U-Test. c PANSS subscores according to Lançon et al. (2000). d Chlorpromazine (CPZ) equivalents calculated according to Lambert et al. (2004) and Schulz et al. (1989); CPZ equivalents of intramuscular Risperidone estimated on the basis of recommended doses (FGA: first generation antipsychotic drug, GAF: Global assessment of functioning, PANSS: Positive and negative syndrome scale, SGA: second generation antipsychotic drug, WCST: Wisconsin card sorting test.). b

MET-CE: α ¼ 0.78, MET-EE: α ¼ 0.97) On the IRI, no group differences were found for ‘perspective taking’ and ‘empathic concern’, but subjects with schizophrenia reported more ‘personal distress’ than healthy controls. Cronbach's α of the IRI scales ranged from α ¼0.55 to α ¼ 0.70. Results were confirmed by MANCOVA controlling for neurocognition (Table 2).

3.2. Emotion contagion and experience of emotion: ECS and SEE Subjects with schizophrenia scored higher on the overall score of the ECS and rated themselves more prone to be affected by negative emotions. No differences were found for positive emotions. Results remained stable after control for neurocognition (Table 2). Regarding the subjective experience of emotions, subjects with schizophrenia reported more SEE ‘overwhelming emotions’, a greater ‘lack of emotions’ and more ‘symbolization of emotions by imagination’, as well as lower ‘self-control’. They did not differ from healthy controls regarding ‘symbolization of emotions by bodily experience’, ‘regulation of emotion’, and perceived ‘congruence’ of emotions. Results remained stable after control for general cognitive function (Table 2). Internal consistencies of the SEE scales ranged from Cronbach's α ¼ 0.59 to α ¼0.85, those of the ECS from α ¼0.47 to α ¼0.76.

3.3. Associations of cognitive and emotional empathy with self-rated emotional parameters Partial correlation analysis revealed a number of significant associations between empathy and emotional parameters (Table 3). In the patient sample, comparisons between ‘high and low cognitive empathizers’ confirmed a significantly higher tendency to ‘symbolize emotions by imagination’ in patients with good cognitive empathy (T[52]¼2.408, po0.05). ‘High emotional empathizers’ in the patient group showed significantly higher scores on the SEE ‘congruence’ (T[52]¼2.183, po0.05) and SEE ‘symbolization of emotions by bodily experience’ scales (T[52]¼ 2.632, po0.05), but scored also higher in emotional contagion with negative emotions (T[52]¼ 2.884, po0.01). In healthy controls, good ‘cognitive empathizers’ were characterized by higher SEE ‘emotion regulation’ (T[52] ¼4.130, po 0.001) and SEE ‘self-control’ scores (T[52] ¼2.041, p o0.05). Good ‘emotional empathizers’ showed higher scores of emotional contagion with positive emotions (T[52] ¼4.003, p o0.001). 3.4. Predictors of psychosocial function Linear regression analysis (method: Enter) was performed to explore the predictive value of symptom load, neurocognition, and

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Table 2 Multivariate analyses of covariance (MANCOVA) for Multifaceted Empathy Test (MET), Interpersonal Reactivity Index (IRI), Emotional Contagion Scale (ECS) and Scales for the Experience of Emotions (SEE) in patients with schizophrenia and healthy controls. Patients (N ¼55; mean 7 S.D.) Healthy controls (N ¼ 55; mean 7 S.D.) Factor diagnosis Covariate cognition composite score MANCOVA 1 F[2; 106] Post-hoc ANOVA F[1; 107] MET cognitive empathy (MET-CE) 22.5 7 4.3 positive valence 11.4 7 2.6 negative valence 11.17 2.4 MET emotional empathy (MET-EE) 217.2 7 62.3 positive valence 104.97 33.4 negative valence 112.3 7 31.3 MANCOVA 2 F[3; 105] Post-hoc ANOVA F[1; 107] IRI empathic concern IRI perspective taking IRI personal distress MANCOVA 3 F[5; 103] Post-hoc ANOVA F[1; 107] ECS happiness ECS love ECS fear ECS anger ECS sadness MANCOVA 4 F[7; 101] Post-hoc ANOVA F[1; 107] SEE congruence SEE overwhelming emotions SEE lack of emotions SEE symbol by bodily experience SEE symbol by imagination SEE emotion regulation SEE self-control

23.7 7 4.5 26.17 4.0 20.6 7 4.0

3.48n 24.673.7 12.3 7 2.1 12.3 72.7 209.2 756.8 100.5 7 33.4 108.7 7 27.8

6.55

0.51

24.874.2 25.4 73.5 15.8 74.4

9.2 7 1.4 8.8 7 1.9 5.5 7 2.1 5.0 7 1.8 5.3 7 1.7

9.17 1.8 8.7 7 2.6 7.3 7 2.4 7.17 2.1 6.4 7 2.3

15.9 7 4,5 13.2 7 6.3 8.0 7 3.4 16.4 7 5.8 9.9 7 5.1 7.6 7 3.5 13.17 3.7

1.73 n

17.1 73.3 8.8 74.7 6.0 73.0 14.5 75.8 6.6 74.6 8.0 72.6 14.9 73.9

3.48

0.01

13.174nnn

459

0.28 1.69 37.50nnn

0.55 0.05 0.082

6.73nnn

0.34

0.00 0.09 16.76nnn 29.91nnn 7.75n

1.32 0.37 0.01 0.21 0.04

4.75nnn

0.30

2.27 17.03nnn 10.65nn 2.49 11.10nn 0.54 5.73n

0.2 0.03 1.30 0.28 0.01 0.00 0.10

MANCOVAs and post-hoc ANOVAs; dependent variables: MANCOVA 1: MET cognitive and emotional empathy subscores; MANCOVA 2: IRI scales. MANCOVA 3: ECS scales. MANCOVA 4: SEE scales. Factors: diagnosis, covariate: cognition composite score. Significant results are indicated by bold type (CE: cognitive empathy score, EE: emotional empathy score.). n

p o0.05. p o0.01. nnn p o 0.001. nn

Table 3 Partial correlation coefficients of cognitive and emotional empathy composite scores (CEC, EEC) versus emotion experience and contagion in patients with schizophrenia and healthy controls. Patients

SEE Congruence Overwhelming emotions Lack of emotions Symbol by bodily experience Symbolization by imagination Emotion Regulation Self-Control ECS Positive emotions Negative emotions IRI personal distress

Fischer’s z

Healthy controls

CEC

EEC

CEC

EEC

0.23  0.02  0.08 0.17 0.31n 0.00 0.14

0.34n 0.04  0.13 0.49nnn 0.14 0.24 0.13

0.24  0.13  0.20 0.02 0.11 0.35n 0.14

 0.07  0.15  0.36nn  0.12 0.00  0.05 0.12

2.225n – 1.255 (n.s.) 3.348nn 1.071 (n.s.)  1.863 (n.s.) –

0.10 0.07  0.17

0.53nnn 0.20  0.11

 1.597 (n.s.) 1.767 (n.s.) –

0.20 0.08 0.13

0.27 0.50nnn 0.19

N ¼55/55; control variables age, cognition composite score, PANSS depression factor (in schizophrenia patients only). CEC: Cognitive empathy composite score; EEC: Emotional empathy composite score; SEE: Scales for the Experience of Emotions; ECS: Emotional Contagion Scale; IRI: Interpersonal Reactivity Index. Significant results are indicated by asterisks, adjusted (Bonferroni) p ¼ 0.00104 (corr. significance indicated by bold type). Fischer’s z is calculated to test statistical significance of between-group differences. n

po 0.05. p o0.01. nnn p o0.001. nn

those self-rated emotional parameters, which had shown alterations in the patient sample, on psychosocial function. Cognition composite score, PANSS sum score, SEE factors ‘overwhelming

emotions’, ‘lack of emotions’, ‘symbolization of emotions by imagination’ and ‘self-control’ as well as IRI ‘personal distress’, MET-‘cognitive empathy’ and ECS scores for negative emotions

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Table 4 Partial Correlation coefficients for MET parameters with psychopathological symptoms and disease characteristics in patients with paranoid schizophrenia. MET-CE sum MET-CE positive valence MET-CE negative valence MET-EE sum MET-EE positive valence MET-EE negative valence PANSS positivea PANSS negativea PANSS depressiona PANSS cognitivea Duration of illness [years] Age at first manifestation [years] Neuroleptic medication [years] Neuroleptic dose [CPZ equiv.]

 0.050  0.129  0.282n  0.176  0.002 0.005  0.016  0.145

 0.149  0.245  0.408nn  0.322n  0.015 0.015  0.072  0.216

0.066 0.028  0.072 0.024 0.013  0.007 0.046  0.030

 0.062  0.182  0.076  0.019 0.328n  0.340n 0.339n 0.074

 0.070  0.238  0.085  0.027 0.265  0.275n 0.283n 0.101

 0.048  0.110  0.061  0.010 0.372nn  0.385nn 0.375nn 0.040

N ¼55; control variables: age, cognition composite score. MET: Multifaceted Empathy Test, CE: cognitive empathy score, EE: emotional empathy score. PANSS: Positive and negative syndrome scale; GAF: Global assessment of functioning; CPZ: chlorpromazine. Significant results are indicated by asterisks, adjusted (Bonferroni) p¼ 0.00313 (corr. significance indicated by bold type). n

po 0.05. p o0.01. p o 0.001. PANSS subscores according to Lançon et al. (2000).

nn

nnn

a

were found to be non-collinear and selected as independent variables. GAF was the dependent variable. The equation explained R2corr ¼ 58.2% of the GAF variance (F[4,50] ¼19.781, p o0.001); significant predictors were PANSS sum score (β ¼ 0.651, p o0.001), SEE ‘overwhelming emotions’ (β ¼0.317, po 0.01), IRI ‘personal distress’ (β ¼  0.216, p o0.05), and MET-‘cognitive empathy’ (β ¼ 0.203, p o0.05). 3.5. Psychopathological and clinical parameters Within the patient group, partial correlation analysis of psychopathological symptoms with MET scores revealed a negative correlation of PANSS depression and cognition factors with the attribution of positive emotions in the MET-‘cognitive empathy’ task. MET-‘emotional empathy’ scores were negatively related to age at first manifestation of psychosis and positively to duration of illness and antipsychotic treatment years. Current antipsychotic dose was not associated with MET parameters (Table 4). ‘Cognitive empathy composite’ score, ‘emotional empathy composite’ score, IRI, and SEE scores as well as ECS values were unrelated to psychopathological and clinical parameters.

4. Discussion This study investigated cognitive and affective dimensions of empathy in patients with paranoid schizophrenia and healthy controls in the context of their subjective experience of aspects of emotion processing. 4.1. Empathy measures: MET and IRI As expected on the basis of previous evidence (Brüne, 2005a; Harrington et al., 2005; Sprong et al., 2007; Bora et al., 2009), patients with schizophrenia showed reduced cognitive empathy compared to healthy controls, even when general cognitive function was controlled. Group differences were comparably small, regarding that substantial impairments of affective theory of mind (Shamay-Tsoory et al., 2007; Derntl et al., 2009; Montag et al., 2011) or of empathic accuracy (Lee et al., 2011) in schizophrenia were previously reported. Contrary to our expectations and to previous research (Montag et al., 2007; Shamay-Tsoory et al., 2007; Haker and Rössler, 2009; Sparks et al., 2010), IRI ‘perspective-taking’ did not differ significantly between groups. These inconsistencies might be explained by the fact that our patients were remitted and did not differ from controls regarding verbal IQ, executive function and education. Moreover, the MET presents

verbal response alternatives in a written form, which might have alleviated cognitive demands compared to a pictorial task (Sarfati et al., 2000), and contextual load was lower compared to the test developed by Derntl et al. (2009). With respect to MET-‘emotional empathy’ no differences were found between the two groups. This finding might suggest unimpaired affective empathy in patients with schizophrenia. Our findings are in line with a number of studies reporting intact immediate experience of emotion and emotional reactions in response to evocative stimuli in schizophrenia (Kring and Moran, 2008; Cohen and Minor, 2010). This could also apply to a vicarious emotional experience. However, experimental evocation of empathic feelings might not correspond to real-world experience, as naturalistic studies using experience sampling methodology demonstrated an increase of negative emotional states in schizophrenia (Myin-Germeys et al., 2000; Oorschot et al., 2013). In contrast to intact in-the-moment emotional empathy in our patient sample, self-rated trait emotionality showed marked alterations compared to healthy controls. This disjunction between state and trait measures corresponds to previous findings of trait high negative and low positive affectivity in schizophrenia (Horan et al., 2008; Cohen et al., 2011; Yan et al., 2012). 4.2. Subjective experience of emotion and emotional contagion: ECS and SEE Regarding the subjective experience of emotion measured by the SEE, patients with schizophrenia reported more ‘overwhelming emotions’ and—at the same time—experienced more ‘lack of emotions’ than healthy controls. They also showed a higher tendency to ‘symbolize emotions by imagination’ and reported less ‘self-control’ of emotional expression. Patients acknowledged more self-directed, aversive feelings when confronted with others in distress (IRI ‘personal distress’) and showed a considerably higher susceptibility for emotional contagion with negative emotions such as fear, anger or sadness. Trait self-ratings regarding dimensions of emotional experience, ‘personal distress’ and contagion can as a whole be considered indicative for regulative deficits of negative emotion and interpersonal tension, and might also be related to aberrant attribution of salience (Kapur, 2003) and amygdala hyperreactivity (Mier et al., 2010; Anticevic et al., 2012b). Previous research suggests emotion regulation deficits in individuals with schizophrenia (Van der Meer et al., 2009; Badcock et al., 2011; Kimhy et al., 2012), although findings are not undisputed (Henry et al., 2008; Perry et al., 2011). However, the SEE ‘emotion regulation’ scale did not differ between groups in our study, which

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might be due to the fact that its items are not restricted to reappraisal strategies and capture emotion regulation more globally than other questionnaires (Gross, 1998). Strauss et al. (2013) provided neurophysiological evidence for dysfunctional cognitive change strategies in schizophrenia in the context of intact self-reported emotion regulation (Strauss et al., 2013), indicating that patients might not be explicitly aware of their problem. On the SEE ‘self-control’ scale, representing suppression as a response-focused emotion regulation strategy, patients scored significantly lower than controls. Our results are thus at variance with studies indicating stronger tendencies to suppress emotional reactions in schizophrenia (Van der Meer et al., 2009; Kimhy et al., 2012). Of note, SEE ‘emotion regulation’ and ‘self-control’ were associated with better cognitive empathy in healthy controls, but not in patients. This might be in keeping with the suggested relationship between affect regulation and mentalizing in non-psychotic individuals (Fonagy et al., 2002; Schipper and Petermann, 2013). In contrast, cognitive empathy in patients was not related to emotion regulation capacity, corroborating the study of Rowland et al. (2012), in which impaired social-cognitive performance was unrelated to the aberrant use of trait emotion regulation strategies in patients with schizophrenia. Although cognitive empathy in schizophrenia might be essentially determined by other variables than emotion regulation, the use of a single self-rating scale is probably the most limiting factor in our study, as self-rated, behavioral and neural correlates of emotional or empathic processing might diverge considerably (Horan et al., 2010; Anticevic et al., 2012a; Derntl et al., 2012; Dyck et al., 2014; Taylor et al., 2012; Strauss et al., 2013). Moreover, MET stimuli depict complex, but moderately arousing emotions, and cognitive empathy may not have been sufficiently challenged by interfering emotional input. For this reason, future research should include naturalistic social–interpersonal stimuli as well as psychophysiological or imaging parameters. The tendency to symbolize emotions by imagination, i. e. to use dream metaphor and reverie for the reflection about oneself and to guide decision-making, was significantly more pronounced in patients with schizophrenia compared to controls. The vividness of mental imagery was proposed as a trait marker across the schizophrenia spectrum (Oertel et al., 2009), the dreaming brain as a model for psychosis (Llewellyn, 2009). Also, imagination could serve to cognitively avoid aversive emotional states. However, in our patient sample the use of imagination was positively associated with cognitive empathy. It therefore might be considered a functional strategy. This is important, as therapeutic work emphasizing metaphorical thought and imagination might bear a greater potential to improve patients' self- and other-reflection than is currently appreciated. Patients with schizophrenia reported more ‘lack of emotions’ than controls, which at first sight is consistent with previous reports about affective blunting and alexithymia in schizophrenia (Stanghellini and Ricca, 1995; Cedro et al., 2001). However, the ‘lack of emotions’ scale assesses the patients' conscious complaints about emotional numbing on a metacognitive level, which does not correspond to questions in classical alexithymia measures. Therefore, a perceived paucity of emotions might rather relate to anhedonia (Strauss and Gold, 2012). Anhedonia may reflect a specific deficit of schizophrenic individuals in the ability to attenuate unpleasant emotional states, contaminating the experience of pleasant states, but also anticipatory and representational deficits (Cohen et al., 2011). This might explain the co-occurrence of ‘overwhelming emotions’ and ‘lack of emotions’ in our sample. At the same time, patients rated themselves more susceptible to emotional contagion for negative emotions than healthy controls. Our finding is partly in keeping with results of Falkenberg et al. (2008), who reported a lower susceptibility for love and higher susceptibility for anger on the ECS—but on a behavioral level, patients with schizophrenia showed reduced tendencies to

synchronize with facial expressions of others (Falkenberg et al., 2008; Varcin et al., 2010) or laughing and yawning (Haker and Rössler, 2009). While discrepancies may reflect a disjunction between expression and experience of emotion in schizophrenia (Kring and Neale, 1996) or medication effects, a putative increase in mirror neuron activity as reported in acutely psychotic individuals might also be related to higher levels of emotional resonance (McCormick et al., 2012). In both study samples, cognitive empathy was unrelated to emotional contagion. This is interesting, as deficits in anger recognition and contagion were shown to be related in schizophrenia (Falkenberg et al., 2008). In a study of healthy persons, Manera et al. (2013) reported a higher susceptibility to emotional contagion for negative, but not positive emotions to increase smile authenticity detection. In our sample, only emotional empathy was positively related to contagion with positive emotions in healthy controls and with negative emotions in patients with schizophrenia—even when depressive psychopathology was controlled in the latter group. Group differences regarding emotional valence might illustrate how the experience of aversive affective states dominates interpersonal resonance in psychotic individuals, while hedonic emotional exchange with others, which is preferred by healthy people, might be diminished. Emotional empathy was further related to the tendency of psychotic patients to attend to bodily manifestations of emotion. This was not the case in healthy controls. Do patients with schizophrenia, more than controls, rely on their ‘gut feeling’ when sharing emotions with others? There are two conceivable reasons for this. To rely on bodily manifestations of emotions in social interaction could mean to rely on unmentalized emotion, and mentalizing deficits have been consistently reported in schizophrenia (Brüne, 2005a), while vegetative responses might be increased (Kring and Moran, 2008). Alternatively, patients who are mindful of their bodily reactions might be less compromised in their social and emotional abilities. 4.3. Psychosocial functioning Global psychosocial function of our patients with schizophrenia was predicted—over and above PANSS scores, though to a smaller extent—by cognitive empathy, a more intense experience of ‘overwhelming emotions’ and by less IRI ‘personal distress’ facing others in need. On the one hand, this is in keeping with studies of Abramowitz et al. (2014) and Sparks et al. (2010), who reported negative associations of IRI ‘personal distress’ with social or recreational functioning, and a multitude of other studies confirming a deleterious role of interpersonal distress in psychosis (Keri and Kelemen, 2009; Mizrahi et al., 2012). On the other hand, the extent of ‘overwhelming emotions’ might indicate a predominance of positive and affective compared to negative symptoms, which are well-known predictors of outcome (Möller et al., 2002). Cognitive empathy explained a smaller share of GAF variance, paralleling findings of Tso et al. (2010), who reported a higher predictive value of emotion regulation strategies and negative emotional experience for social adjustment than cognitive empathy— underlining the importance of a successful management of negative affect for psychosocial outcome. GAF scores in our sample were not predicted by ‘lack of emotions’ and ‘self-control’, being at variance with findings of Kimhy et al. (2012), who reported associations of alexithymia measures and emotion regulation by suppression with psychosocial impairments. However, discrepancies might be explained by the fact that the ability to identify and to describe emotions covered by the alexithymia test may share a common core rather with cognitive empathy than with self-perceived emotional blunting and by controlling for negative symptoms. Unfortunately, we did not test the capability to differentiate self-generated emotions, so that a comparison of our results with studies reporting

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a role of emotional awareness and granularity for social and emotional functioning is hampered (Barrett et al., 2001; Kimhy et al., 2012, 2014). 4.4. Psychopathological and clinical parameters Correlation analysis of psychopathological parameters of the patient group with empathy scores revealed significant negative correlations between MET ‘cognitive empathy’ for positive mental states, but not MET ‘emotional empathy’, and PANSS cognition and depression factors. Deficits of affective and cognitive mentalizing have also been reported in patients with major depression (Uekermann et al., 2008; Wang et al., 2008), and depressive symptoms have been shown to influence the self-perception of empathy in schizophrenia (Lysaker et al., 2013; Abramowitz et al., 2014). MET ‘emotional’, but not ‘cognitive empathy’ was higher in individuals with an earlier onset, a longer course of disease and a higher number of years spent under antipsychotic treatment. Our finding might indicate preserved emotional reactivity in chronic, pharmacologically compliant patients, but could also be due to growing affective lability in the course of the disease. The specific role of antipsychotic therapy in this respect and its long-term effects remain to be determined (Lataster et al., 2011; Isom et al., 2013). 4.5. Limitations An important limitation of our study is the fact that all patients were medicated. Even if the acute effects of antipsychotics on social cognition were shown to be negligible in a small number of studies (Mizrahi et al., 2007), differential or long-term effects of antipsychotics cannot be excluded (Pinkham et al., 2007; Kucharska-Pietura et al., 2012). We are aware of the problem of multiple testing. Not all results were maintained after alpha-leveladjustment (Bonferroni) and have to be interpreted with caution. To our knowledge, this is the first study using the MET and the SEE in schizophrenia. As a formal validation study was beyond the scope of this investigation, results need independent replication and validation. Moreover, the use of self-rating instruments represents a major limitation in the study of emotional experience in schizophrenia. Although self-reports of patients with schizophrenia have been proven reliable and valid in a number of studies (Kring et al., 2003; Kring and Moran, 2008), psycho-physiological measures or imaging techniques should be included in future research. In summary, our results suggest that patients with schizophrenia might have difficulties to correctly infer and label other people's emotional states, but do not necessarily differ from healthy controls in their ability to feel with them, i.e. to empathize emotionally. They underline the importance of subjective processes of managing negative emotions which might impact psychosocial function even more clearly than cognitive empathy. However, future research employing multiple methods can help clarifying the scope of empathic and emotional disturbances in schizophrenia, and the psychological and neural mechanisms through which these difficulties ultimately impact psychosocial recovery. References Abramowitz, A.C., Ginger, E.J., Gollan, J.K., Smith, M.J., 2014. Empathy, depressive symptoms, and social functioning among individuals with schizophrenia. Psychiatry Research 216, 325–332. http://dx.doi.org/10.1016/j. psychres.2014.02.028. Achim, A.M., Ouellet, R., Roy, M.A., Jackson, P.L., 2011. Assessment of empathy in first-episode psychosis and meta-analytic comparison with previous studies in schizophrenia. Psychiatry Research 190, 3–8.

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