Profiling of experiential pleasure, emotional regulation and emotion expression in patients with schizophrenia

SCHRES-07497; No of Pages 6 Schizophrenia Research xxx (2017) xxx–xxx

Contents lists available at ScienceDirect

Schizophrenia Research journal homepage: www.elsevier.com/locate/schres

Profiling of experiential pleasure, emotional regulation and emotion expression in patients with schizophrenia Ying-min Zou a,b, Ke Ni a,b,c, Zhuo-ya Yang a,b, Ying Li a,b,d, Xin-lu Cai a,b,e,f, Dong-jie Xie a,b, Rui-ting Zhang a,b, Fu-Chun Zhou g, Wen-xiu Li d, Simon S.Y. Lui h, David H.K. Shum a,i,j, Eric F.C. Cheung h, Raymond C.K. Chan a,b,⁎ a

Neuropsychology and Applied Cognitive Neuroscience Laboratory, CAS Key Laboratory of Mental Health, Institute of Psychology, Beijing, China Department of Psychology, University of Chinese Academy of Sciences, Beijing, China Qigihar Mental Health Center, Heilongjiang, China d Haidian District Mental Health Prevent-Treatment Hospital, Beijing, China e Sino-Danish College, University of Chinese Academy of Sciences, Beijing 100190, China f Sino-Danish Center for Education and Research, Beijing 100190, China g Beijing Key Laboratory of Mental Disorders, Beijing Anding Hospital, Capital Medical University, Beijing, China h Castle Peak Hospital, Hong Kong Special Administrative Region i Menzies Health Institute Queensland, Griffith University, Gold Coast, Australia j School of Applied Psychology, Griffith University, Brisbane, Australia b c

a r t i c l e

i n f o

Article history: Received 28 April 2017 Received in revised form 7 August 2017 Accepted 23 August 2017 Available online xxxx Keywords: Schizophrenia Cluster analysis Experience Expression Regulation

a b s t r a c t Background: Emotion deficits may be the basis of negative symptoms in schizophrenia patients and they are prevalent in these patients. However, inconsistent findings about emotion deficits in schizophrenia suggest that there may be subtypes. Aim: The present study aimed to examine and profile experiential pleasure, emotional regulation and expression in patients with schizophrenia. Methods: A set of checklists specifically capturing experiential pleasure, emotional regulation, emotion expression, depressive symptoms and anhedonia were administered to 146 in-patients with schizophrenia and 73 demographically-matched healthy controls. Psychiatric symptoms and negative symptoms were also evaluated by a trained psychiatrist for patients with schizophrenia. Results: Two-stage cluster analysis and discriminant function analysis were used to analyze the profile of these measures in patients with schizophrenia. We found a three-cluster solution. Cluster 1 (n = 41) was characterized by a deficit in experiential pleasure and emotional regulation, Cluster 2 (n = 47) was characterized by a general deficit in experiential pleasure, emotional regulation and emotion expression, and Cluster 3 (n = 57) was characterized by a deficit in emotion expression. Results of a discriminant function analysis indicated that the three groups were reasonably discrete. Conclusion: The present findings suggest that schizophrenia patients can be classified into three subtypes based on experiential pleasure, emotional regulation and emotion expression, which are characterized by distinct clinical representations. © 2017 Elsevier B.V. All rights reserved.

1. Introduction Emotion deficits, such as blunted experiential pleasure and diminished emotion expression, may be the basis of negative symptoms (Oorschot et al., 2013), and are prevalent among patients with schizophrenia (Aleman and Kahn, 2005; Kring and Elis, 2013). However, not all patients with schizophrenia have emotion deficits (Hooker and Park, 2002). For example, recent-onset patients with schizophrenia ⁎ Corresponding author at: Institute of Psychology, Chinese Academy of Sciences, 16 Lincui Road, Beijing 100101, China. E-mail address: [email protected] (R.C.K. Chan).

(Lui et al., 2015) do not exhibit decreased pleasure experience in daily life compared with healthy controls, but patients with chronic schizophrenia do (Y. Li et al., 2015; Z. Li et al., 2015). Moreover, different aspects of emotion deficits may also contribute to different aspects of negative symptoms (Mandal et al., 1999; Oorschot et al., 2013). A recent re-conceptualization of negative symptoms stresses that negative symptoms are mainly composed of two factors, namely, diminished pleasure/motivation and diminished emotional expression (Blanchard and Cohen, 2005; Kring et al., 2013). Empirical findings also suggest that reward circuit abnormalities underlying negative symptoms may involve reduced activation of the rostral medial prefrontal cortex, the right parahippocampus/amygdala, and other limbic regions when

http://dx.doi.org/10.1016/j.schres.2017.08.048 0920-9964/© 2017 Elsevier B.V. All rights reserved.

Please cite this article as: Zou, Y., et al., Profiling of experiential pleasure, emotional regulation and emotion expression in patients with schizophrenia, Schizophr. Res. (2017), http://dx.doi.org/10.1016/j.schres.2017.08.048

2

Y. Zou et al. / Schizophrenia Research xxx (2017) xxx–xxx

processing in-the-moment positive stimuli, and decreased activation of the left putamen (Yan et al., 2015). As reviewed by Kring and Elis (2013), three components of emotion deficits in schizophrenia have been studied extensively: expression, experience and physiology. Emotion experience deficits in schizophrenia are thought to reflect a blunted inner experience of emotional stimuli in daily life (Myin-Germeys et al., 2000). Diminished pleasure experience has attracted much attention in previous studies (Chan et al., 2010; Kring and Caponigro, 2010; Z. Li et al., 2015a) because of its prevalence and contribution to poor prognosis. Emotion expression deficits refer to diminished outer expression of emotion (Mandal et al., 1998; Aghevli et al., 2003). Kring and Elis (2013) concluded that emotion experience and expression could be taken as different components of emotion response. To better understand why patients with schizophrenia show deficits in emotion response, Trémeau (2006) suggested that the regulatory domain should be taken into consideration. In a consensus model of emotion proposed by Gross (1998, 2002), emotion starts with a cue, and subjective evaluation of the emotional cue triggers emotion response tendencies (e.g. behavioural, experiential and physiological), which can be modulated before emotion response appears. In short, emotion response is regulated in two ways: processing the input (antecedent-focused emotion regulation) and dealing with the output (response-focused emotion regulation) (Gross and Thompson, 2007). The most common antecedent-focused emotion regulation is reappraisal, which is defined as the subjective interpretation of emotional cues before emotion response tendencies are shaped (Gross, 1998). For response-focused emotion regulation, the most commonly used strategy is suppression, which is defined as the inhibition of emotion expression, which rarely influences the subjective experience of emotion (Gross and Levenson, 1993, 1997; Webb et al., 2012). With respect to data analysis, most previous studies have employed group comparison between patients and healthy controls rather than cluster analysis. Because emotion deficits consist of several domains, group comparisons focusing on a specific domain cannot address the issue of heterogeneity of patients. For example, Strauss and Herbener (2011) identified two emotional experience subgroups in schizophrenia, using their rating scores of emotional pictures as an index. In their study, Cluster 1 was comparable with healthy controls, whereas for Cluster 2, participants with schizophrenia rated negative pictures more negatively and felt more aroused than healthy controls. Moreover, participants in Cluster 2 had more severe negative symptoms than those in Cluster 1. This finding suggests that there may be subgroups of schizophrenia patients with different patterns of emotion deficits. Integrating the emotion response and regulation framework, we aimed to examine the subtypes of emotion deficits in patients with schizophrenia in three domains: experiential pleasure, emotional regulation and emotion expression. Based on Strauss and Herbener's (2011) previous findings and the findings that emotional regulation would influence emotion experience and expression, we hypothesized that there would be subtypes of schizophrenia patients characterized by their unique manifestations of experiential pleasure, emotional regulation and emotion expression. In particular, the potential subtypes would be manifested in terms of 1) no deficits in experiential pleasure, emotion expression and emotional regulation; 2) a deficit in experiential pleasure; 3) a deficit in emotion expression; 4) a deficit in emotional regulation; 5) a deficit in experiential pleasure and emotion expression; 6) a deficit in experiential pleasure and emotional regulation; 7) a deficit in emotion expression and emotional regulation; and 8) a general deficit in experiential pleasure, emotional expression and regulation. 2. Method 2.1. Participants One hundred and forty-six patients with schizophrenia and 73 demographically-matched healthy controls were recruited for the present

study. All patients fulfilled DSM-IV (American Psychiatric Association, 1994) criteria for schizophrenia. Diagnosis and clinical ratings were carried out by an experienced psychiatrist. Patients were recruited from the Qigihar Mental Health Center, the Haidian District Mental Health Hospital and the Beijing Anding Hospital. Inclusion criteria were: (a) meeting DSM-IV criteria for schizophrenia; (b) an IQ of N70, estimated using the short-form of the Chinese Wechsler Adult Intelligence Scale (WAIS-R; Gong, 1992); (c) years of education of more than nine years; and (d) aged 18 to 60 years. Potential participants were excluded if they met any of the following criteria: (a) a history of head trauma; (b) a history of substance or alcohol dependence; (c) mental retardation; (d) a history of neurological disorders; and (e) a history of having TMS or ECT in the past 12 weeks. All patients were clinically stable outpatients and medicated with antipsychotic medications with an average chlorpromazine equivalence of 322.05 (± 165.95) mg/day. The mean duration of illness was 30.39 (±15.23) months. Healthy controls were recruited from the neighbouring communities of the hospitals. The inclusion criteria were: (a) an estimated IQ of N70; (b) years of education of more than nine years; (c) aged 18 to 60 years; and (d) a Beck Depression Inventory-I (BDI-I, Beck et al., 1988) score of lower than 7. Exclusion criteria were: (a) a history of head trauma; (b) a history of substance or alcohol dependence; (c) mental retardation; (d) a history of neurological disorders; and (e) a personal or family history of mental illness. Schizophrenia patients and healthy controls did not differ in gender (χ2218 = 0.699, p = 0.485), age (t218 = 0.667, p = 0.156), years of education (t218 = 0.869, p = 0.385) and estimated IQ (t218 = 0.254, p = 0.699). All participants gave informed consent, and received 100RMB as compensation for their time. The study protocol was approved by the Ethics Committees of all the institutes involved in this study. 2.2. Measures All participants completed the self-report scales listed below. The IQ test was administered by trained research psychologists. For schizophrenia patients, an experienced psychiatrist ascertained their diagnoses and administered the clinical rating scales. 2.2.1. Self-report scales The Temporal Experience of Pleasure Scale (TEPS; Chan et al., 2012; Gard et al., 2006) was administered to evaluate pleasure experience. The Chinese version of the TEPS comprises 19 items and consists of four factors: Abstract Anticipatory (e.g., “I looking forward to a lot of things in my life.”), Contextual Anticipatory (e.g., “When I hear about a new movie starring my favorite actor, I can't wait to see it.”), Abstract Consummatory (e.g., “I enjoy taking a deep breath of fresh air when I walk outside.”), and Contextual Consummatory (e.g., “I really enjoy the feeling a good yawn.”). Participants rated each item of pleasure experience from 1 to 6 (1 = very false to me, 6 = very true to me). A higher score indicates feeling or anticipating more pleasure in daily life. In the present study, the Cronbach's α of the TEPS was 0.843. The Toronto Alexithymia Scale (TAS-20; Taylor et al., 2003; Yuan et al., 2003) was used to assess difficulties in verbal expression of positive (e.g., “Looking for hidden meanings in movies or plays distracts from their enjoyment.”) and negative emotions (e.g., “When I am upset, I don't know if I am sad, frightened, or angry.”). The 20-item Chinese version of this scale utilizes a five-point Likert rating scale (1 = totally disagree, 5 = totally agree) and has three factors (difficulty recognizing feeling, difficulty describing feeling; and externally oriented thinking). A higher score indicates greater difficulty in verbal expression of emotion. Previous studies have shown that schizophrenia patients only scored higher than healthy controls on difficulty in identifying and describing feeling, but not on externally oriented thinking (Cedro et al., 2001). We would, therefore, leave out the externally oriented thinking factor in our data analysis. The Cronbach's α of the TAS in this study was 0.765.

Please cite this article as: Zou, Y., et al., Profiling of experiential pleasure, emotional regulation and emotion expression in patients with schizophrenia, Schizophr. Res. (2017), http://dx.doi.org/10.1016/j.schres.2017.08.048

Y. Zou et al. / Schizophrenia Research xxx (2017) xxx–xxx

The Emotion Regulation Questionnaire (ERQ; Gross and John, 2003; Li et al., 2007) was used to evaluate the frequency of two emotion regulation strategies (appraisal and suppression) for both positive (e.g., “When I want to feel more positive emotion, I change the way I'm thinking about the situation.”) and negative events (e.g., “When I'm faced with a stressful situation, I make myself think about it in a way that helps me stay calm.”). Items for appraisal include “I control my emotions by changing the way I think about the situation I am in”, and items for suppression include “I control my emotion by not expressing them”. The Chinese version of the ERQ comprises 14 items with a seven-point Likert rating scale (1 = strongly disagree, 7 = strongly agree). A higher score indicates a higher frequency of using one specific strategy. In this study, the Cronbach's α of the ERQ reappraisal and suppression subscale was 0.768 and 0.767 respectively. The Chinese versions of the Revised Physical Anhedonia Scale (Chan et al., 2016; Chapman et al., 1976; Wang et al., 2012) and the Revised Social Anhedonia Scale (Chan et al., 2016; Eckblad et al., 1982; Wang et al., 2012) were used to assess physical and social anhedonia. Physical anhedonia refers to subjective pleasure experience derived from physical sensations, while social anhedonia refers to pleasure experience derived from social activities. A higher score indicates a higher capacity to experience pleasure. The Beck Depression Inventory-I (BDI; Beck et al., 1988) was used to evaluate the severity of depressive symptoms. Items on the BDI-I are rated on a four-point scale and a higher score indicates more severe depressive symptoms. 2.2.2. Clinical assessments The Scale for Assessment of Negative Symptoms (SANS; Andreasen, 1989) was used to assess negative symptoms. It includes five domains, namely, affective flattening (poverty of affect), alogia (poverty of speech), avolition (diminished motivated activities), anhedonia (diminished pleasure and interest), and attentional impairment (inattentiveness). The Positive and Negative Syndrome Scale (PANSS; Kay et al., 1987) was administered to assess positive and negative symptoms of schizophrenia. A higher score indicates more severe psychotic symptoms. 2.3. Statistical analysis Statistical analyses were carried out using the Statistical Package for Social Science (version 17.0 for Windows; SPSS Inc., Chicago, IL, USA). Demographic and descriptive data of self-report measures were computed. Group differences in demographic data and self-report measures were tested using the chi-square or independent group t-test. Cluster analysis and discriminant function analysis were conducted for patients with schizophrenia. Cluster analysis was carried out with the scores on the TEPS anticipatory (ANT) pleasure subscale, the TEPS consummatory (CON) pleasure subscale, the ERQ reappraisal (RAP) subscale, the ERQ suppression (SUP) subscale, the TAS recognition (REC) subscale, and the TAS (DES) subscale. In the first step, all variables were used as dependent variables in the cluster analysis. Following standard cluster analysis procedures (Lange et al., 2002), we ran a two-step cluster analysis. Squared Euclidean distance was chosen as the dissimilarity index due to its consideration of both profile shape and elevation (Everitt et al., 2001). The resulting dendrogram plot produced the optimal cluster number. The Schwarz Bayesian Criterion (BIC) was used as the determining parameter for the optimal cluster number, that is, when BIC became small and the change in BIC between adjacent numbers of cluster was small (Mooi and Sarstedt, 2011). Next, based on the cluster number from step 1, we ran a K-means cluster analysis to check the assignment of cluster members (Lange et al., 2002). Finally, a discriminant function analysis was carried out to test whether the six variables (ANT, CON, RAP, SUP, REC, and DES) were accurately assigned to the target clusters using an iterative partitioning method. To check the clinical representations among clusters, we compared

3

their medication dosage, duration of illness, scores on the BDI, the Chapman Physical and Social Anhedonia Scales, the SANS (total and factor scores) and the PANSS using ANOVAs.

3. Results 3.1. Demographical and descriptive data There were no group differences in gender, age, years of education and IQ between patients and controls (see Table 1). Compared with schizophrenia patients, healthy controls had significantly higher TEPS total scores (t217 = 3.206, p b 0.001), ANT scores (t217 = 2.332, p b 0.05) and CON scores (t217 = 3.389, p b 0.001). No significant group differences were found on REC and DES scores. For emotion regulation, compared with schizophrenia patients, healthy controls used significantly more reappraisal strategies (t218 = 3.248, p b 0.001), but comparable suppression strategies. The BDI score of schizophrenia patients was significantly higher than healthy controls (t218 = 9.848, p b 0.001). Schizophrenia patients and healthy controls did not differ on physical anhedonia scores, but schizophrenia patients scored significantly higher than healthy controls in social anhedonia (t218 = 3.597, p b 0.001).

3.2. Cluster analysis results The two-step cluster analysis produced three clusters as the best solution. When the cluster number was three, the BIC was smallest (cluster number = 2, BIC = 634.766; cluster number = 3, BIC = 631.146; cluster number = 4, BIC = 638.494). K-means cluster analysis showed that there were 41 cases in Cluster 1 (28%), 48 cases in Cluster 2 (33%), 57 cases in Cluster 3 (39%). The emotion profile of the clusters is presented in Fig. 1. According to the profiling criteria by Dawes et al. (2008), profiles are determined when a given mean differs from the overall mean score of its relative profile by N0.5 standard deviations. In this study, Cluster 1 was characterized by a deficit in experiential pleasure and emotional regulation, Cluster 2 was characterized by a general deficit in experiential pleasure, emotional regulation and emotion expression, and Cluster 3 was characterized by a deficit in emotion expression. Discriminant function analysis showed that two discriminant functions contributed to the three subgroups. The first discriminant function explained 73.9% of the variance (Wilk's lambda = 0.185, p b 0.001), while the second discriminant function explained 26.1% of the variance (Wilk's lambda = 0.574, p b 0.001). For the first discriminant function, the most important contributors were difficulty in describing emotion, reappraisal, and consummatory pleasure. For the second discriminant function, the most important contributors were difficulty in describing emotion, anticipatory pleasure, and consummatory pleasure. Results of the cross-validation method indicated that overall 92.5% of the cases were accurately classified, with 87.8% classification accuracy for Cluster 1, 91.7% classification accuracy for Cluster 2, and 96.5% classification accuracy for Cluster 3.

3.3. Differences in clinical representations between the three clusters There were no group differences in medication dosage and duration of illness between the three clusters. Group differences were found on BDI (F(2,143) = 5.306, p = 0.006) and SANS affective flattening score (F(2,143) = 4.079, p = 0.019) between the clusters. Post-hoc analyses revealed that Cluster 2 had more severe depressive symptoms than Cluster 1 and 3, and Cluster 1 and Cluster 2 showed more severe affective flattening than Cluster 3 (Table 2).

Please cite this article as: Zou, Y., et al., Profiling of experiential pleasure, emotional regulation and emotion expression in patients with schizophrenia, Schizophr. Res. (2017), http://dx.doi.org/10.1016/j.schres.2017.08.048

4

Y. Zou et al. / Schizophrenia Research xxx (2017) xxx–xxx

Table 1 Differences in demographical and self-reported scores between SZ and HC. Variables

SZ (n = 146)

HC (n = 73)

t/χ2

p

Cohen's d

Comparisons

Gender (% male) Age (years) Education (years) Age of onset (years) Duration of illness (months) Medication (CPZ/mg/day) WAIS-R TEPS ANT CON REC DES RAP SUP BDI Chapman social anhedonia Chapman physical anhedonia

56.16% 36.29 (10.30) 11.42 (2.84) 24.62 (7.13) 30.39 (15.23) 322.05 (165.95) 103.20 (20.76) 69.86 (17.11) 31.76 (8.63) 38.10 (9.86) 18.72 (6.08) 14.70 (3.86) 25.65 (8.45) 15.73 (4.83) 15.94 (10.73) 14.81 (6.98) 25.60 (6.45)

49.30% 35.95 (10.63) 11.77 (2.85)

−0.699 0.667 −0.869

0.485 0.156 0.386

110.16 (22.73) 76.86 (10.73) 34.31 (5.09) 42.54 (7.45) 17.45 (5.06) 14.58 (3.76) 29.15 (5.13) 15.61 (4.53) 3.39 (2.45) 8.45 (5.49) 24.16 (3.88)

0.254 −3.206 −2.332 −3.389 1.536 0.216 −3.248 0.174 9.848 3.597 −1.557

0.699⁎ b0.001⁎⁎⁎ b0.05⁎⁎ 0.001⁎⁎⁎

0.084 0.032 −0.123 – – – −0.319 −0.490 −0.359 −0.508 0.227 0.031 −0.500 0.025 1.612 1.012 0.270

– – – – – – – HC N SZ HC N SZ HC N SZ – – HC N SZ – SZ N HC SZ N HC –

0.126 0.829 b0.001⁎⁎⁎ 0.862 b0.001⁎⁎⁎ b0.001⁎⁎⁎ 0.125

Percent for gender, mean and standard deviations for other measures. SZ, schizophrenia; HC, healthy controls; CPZ, chlorpromazine equivalents; WAIS-R, the Chinese Wechsler Adult Intelligence Scale; TEPS, Temporal Experience of Pleasure Scale; ANT, anticipatory pleasure; CON, consummatory pleasure; REC, difficulty in recognizing emotion; DES, difficulty in describing emotion; RAP, reappraisal; SUP, suppression; BDI, Beck Depression Inventory-I. ⁎ p b 0.05. ⁎⁎ p b 0.01. ⁎⁎⁎ p b 0.001.

4. Discussion The present study examined the emotion profile of schizophrenia patients based on an integrated theoretical framework proposed by Kring and Elis (2013) and Gross and Thompson (2007). There are two main findings. First, emotion deficits in schizophrenia can be clustered into three subtypes, namely, “a deficit in experiential pleasure and emotional regulation”, “a general deficit in experiential pleasure, emotional regulation and emotion expression” and “a deficit in emotion expression”. Second, patients with “a general deficit in experiential pleasure, emotional regulation and emotion expression” reported more severe depressive symptoms than the other two groups; while patients with “a deficit in experiential pleasure and emotional regulation” and patients with “a general deficit in experiential pleasure, emotional regulation and expression” had more affective flattening than patients with “a deficit in emotion expression”. Results of the three-cluster solution partly supported our hypothesis. The present study identified emotion deficit subtypes with different features in patients with schizophrenia. Patients in Cluster 1 employed insufficient reappraisal strategies; those in Cluster 2 employed

insufficient reappraisal and excessive suppression; while those in Cluster 3 employed excessive suppression leading to malfunctioning of emotion regulation. No cluster was characterized by “no deficits in experiential pleasure, emotion expression and emotional regulation”. The fact that our sample was recruited solely from hospitalized patients might have contributed to the higher prevalence of negative symptoms due to institutionalization (an der Heiden et al., 2016; Mancevski et al., 2007). The three clusters we found were all characterized by distinct clinical manifestations. Group-level comparisons showed that patients with “a general deficit in experiential pleasure, emotional regulation and emotion expression” reported more severe depressive symptoms than the other two groups, which is consistent with findings in previous studies (Häfner et al., 2005; Majadas et al., 2012). Low experiential pleasure in daily life in schizophrenia patients may result in higher prevalence of depression. From the perspective of emotion regulation, patients with “a general deficit in experiential pleasure, emotional regulation and emotion expression” may employ insufficient reappraisal and excessive suppression strategies, which may increase negative emotions and decrease positive emotions (Gross and John, 2003; Heiy

Fig. 1. Profiles of means for emotion domains using Z-scores. Error bars represent 95% confidence intervals.

Please cite this article as: Zou, Y., et al., Profiling of experiential pleasure, emotional regulation and emotion expression in patients with schizophrenia, Schizophr. Res. (2017), http://dx.doi.org/10.1016/j.schres.2017.08.048

Y. Zou et al. / Schizophrenia Research xxx (2017) xxx–xxx

5

Table 2 Differences in clustering variables and clinical representations among emotion clusters in SZ. Variables

Cluster 1 (n = 41)

Cluster 2 (n = 48)

Cluster 3 (n = 57)

F

p

Cohen's d

Comparisons

Clustering variables ANT CON REC DES RAP SUP

28.95 (7.12) 34.70 (9.08) 13.56 (5.73) 10.63 (2.57) 20.29 (8.37) 12.87 (4.80)

26.10 (6.78) 31.58 (6.80) 21.41 (4.21) 16.62 (2.58) 23.79 (6.39) 16.79 (3.54)

38.54 (6.17) 46.05 (6.70) 20.49 (4.80) 16.28 (2.61) 31.52 (5.56) 17.17 (4.51)

50.655 54.676 33.602 74.033 36.589 13.577

b0.001⁎⁎⁎ b0.001⁎⁎⁎ b0.001⁎⁎⁎ b0.001⁎⁎⁎ b0.001⁎⁎⁎ b0.001⁎⁎⁎

0.415 0.433 0.320 0.509 0.339 0.160

3N1N2 3N1=2 2=3N1 2=3N1 3N2N1 3=2N1

Validating variables Duration of illness (months) Medication (CPZ/mg/day) BDI Chapman social anhedonia Chapman physical anhedonia PANSS Positive symptoms Negative symptoms General SANS Affective flattening Alogia Avolition Anhedonia Attentional impairment

31.22 (17.74) 310.43 (173.14) 13.75 (11.47) 16.40 (5.22) 25.40 (3.57) 69.67 (17.39) 18.02 (6.67) 17.95 (4.84) 33.70 (8.20) 49.01 (17.81) 14.05 (4.46) 9.07 (3.92) 11.01 (4.14) 9.52 (4.10) 5.35 (2.93)

30.78 (14.52) 284.46 (130.52) 20.04 (10.04) 15.77 (7.52) 27.61 (6.46) 64.29 (18.27) 16.46 (7.68) 15.57 (4.67) 32.25 (9.57) 46.50 (17.72) 13.89 (5.43) 8.23 (4.25) 10.53 (4.62) 9.74 (3.90) 4.10 (3.74)

29.59 (14.64) 360.81 (184.94) 14.35 (9.83) 13.61 (6.95) 23.66 (6.70) 64.84 (20.40) 17.14 (7.58) 16.03 (5.99) 31.66 (9.50) 41.95 (19.15) 11.51 (5.08) 7.42 (4.62) 9.86 (4.67) 9.08 (4.20) 4.07 (3.58)

0.147 2.860 5.306 0.596 1.747 1.051 0.481 2.432 0.588 1.869 4.079 1.737 0.790 0.351 1.917

0.863 0.061 0.006⁎⁎ 0.556 0.188 0.352 0.619 0.092 0.557 0.158 0.019⁎

0.002 0.039 1.107 0.028 0.084 0.366 0.282 0.736 0.222 0.624 0.973 0.592 0.193 0.345 0.634

– – 2N1=3 – – – – – – – 1=2N3 – – – –

0.180 0.456 0.705 0.151

Mean and standard deviations for all measures. ANT, anticipatory pleasure; CON, consummatory pleasure; REC, difficulty in recognizing emotion; DES, difficulty in describing emotion; RAP, reappraisal; SUP, suppression; CPZ, chlorpromazine equivalents; BDI, Beck Depression Inventory-I; PANSS, Positive and Negative Syndrome Scale; SANS, Scale for Assessment of Negative Symptoms. ⁎ p b 0.05. ⁎⁎ p b 0.01. ⁎⁎⁎ p b 0.001.

and Cheavens, 2014). The findings that both patients with “a general deficit in experiential pleasure, emotional regulation and emotion expression” and “a deficit in experiential pleasure and emotional regulation” exhibited more affective flattening symptoms than patients with “a deficit in emotion expression” warrants further discussion. First, there was no significant difference between the three clusters in the duration of illness and medication dosage, suggesting that the differences between the three clusters were not confounded by the course of illness and severity of psychotic symptoms (especially the potential impact of insight impairment) in these patients. It should also be noted that the SANS did not capture comprehensively the most up-to-date construct of negative symptoms for schizophrenia, that is, a 2-facet model of negative symptoms involving anticipatory-consummatory anhedonia (Berridge et al., 2009) as well as “expression” and “motivation/pleasure” (Blanchard et al., 2011; Kring et al., 2013). It is possible that affective flattening may not be the best measure to capture the subtle individual differences in dispositional expressiveness in patients with schizophrenia. The recently developed tool, the Clinical Assessment Interview for Negative Symptoms (CAINS) (Kring et al., 2013), has been shown to capture the “expression” and “motivation/pleasure” component of negative symptoms in schizophrenia, and hence, may be more sensitive to detect such subtle deficits in expression component of negative symptoms. Future study adopting both the CAINS and other measures specifically capturing dispositional expressivity in a larger clinical sample should be conducted to verify this speculation. The systematic delineation of different subtypes based on emotion in patients with schizophrenia has both theoretical and clinical implications. Theoretically, the three clusters we identified from the present clinical sample supports the notion that negative symptoms consist of both emotional and cognitive domains (Bora and Murray, 2014; Foussias and Remington, 2010; Kring et al., 2013; Painter and Kring, 2016). This finding supports the model proposed by Gross and Thompson (2007), which suggests that emotion regulation has an impact on emotion response (experience and expression). In other words, our findings appear to support the “experience, expression and regulation” framework in explaining negative symptoms in

schizophrenia. Clinically, the identified unique clusters of emotional experience, regulation and expression may provide insights into the development of interventions based on the characteristics of each distinct cluster. For example, cluster with just emotion expression deficits may benefit more from intervention targeting emotional expression rather than general training in emotion. Moreover, different clusters may be associated with different functional outcomes and recovery patterns. The identification of these clusters or subtypes may help to predict prognosis in the future. This study has several limitations. First, we were unable to exclude the influence of antipsychotic medications as our sample consisted of only hospitalized schizophrenia patients. As such, our results may not be generalizable to the different stages of schizophrenia. Second, the present study was limited to self-report measures of experiential pleasure, emotional regulation, and emotion expression and cognitive functions were not assessed. Future study adopting experimental tasks to capture these constructs is indicated. Similarly, our assessment of emotion expression was only limited to clinical ratings of affective flattening and did not include other quantifiable measure of facial expression. Future study could include more sophisticated measures to assess emotion expression. Notwithstanding the above limitations, our findings may facilitate the early identification of emotion subtypes in schizophrenia, which, in turn, may guide individualized treatment of negative symptoms according to different clustering in emotion deficits. Future studies should include objective emotion assessment methods and investigate other clinical groups (e.g. major depressive disorder, bipolar disorder) which also have emotion deficits. Role of funding source The funding agents had no further role in the study design; in the collection, analysis and interpretation of the data; in the writing of the manuscript; and in the decision to submit the paper for publication. Contributors YMZ collected, analyzed and interpreted the data, and wrote up the first draft of the manuscript. KN conducted clinical interview, collected data and helped analyzed data.

Please cite this article as: Zou, Y., et al., Profiling of experiential pleasure, emotional regulation and emotion expression in patients with schizophrenia, Schizophr. Res. (2017), http://dx.doi.org/10.1016/j.schres.2017.08.048

6

Y. Zou et al. / Schizophrenia Research xxx (2017) xxx–xxx

ZYY, YL, XLC, DJX, RTZ administered tests and helped literature search. FCZ conducted clinical interview and administered assessment. WXL, SSYL, DHKS, and EFFC made significant comment to the first draft of the manuscript. RCKC generated the idea, interpreted findings and helped write the first draft of the manuscript. All authors contributed to and have approved the final manuscript. Conflict of interests The authors declared that there are no conflicts of interest in relation to the subject of this study. Acknowledgements This study was supported by the National Science Fund China (81571317), the Beijing Training Project for the Leading Talents in Science and Technology (Z151100000315020), the Beijing Municipal Science & Technology Commission Grant (Z161100000216138), and the National Basic Research Programme of China (Precision psychiatry Programme, 2016YFC0906402).

References Aghevli, M.A., Blanchard, J.J., Horan, W.P., 2003. The expression and experience of emotion in schizophrenia: a study of social interactions. Psychiatry Res. 119 (3), 261–270. Aleman, A., Kahn, R.S., 2005. Strange feelings: do amygdala abnormalities dysregulate the emotional brain in schizophrenia? Prog. Neurobiol. 77 (5):283–298. http:// dx.doi.org/10.1016/j.pneurobio.2005.11.005. American Psychiatric Association, 1994. DSM-IV: Diagnostic and Statistic Manual of Mental Disorders. American Psychiatric Association, Washington DC. Andreasen, N.C., 1989. Scale for the Assessment of Negative Symptoms (SANS). Br. J. Psychiatry 155 (suppl 7), 49–52. Beck, A.T., Steer, R.A., Carbin, M.G., 1988. Psychometric properties of the Beck Depression Inventory: twenty-five years of evaluation. Clin. Psychol. Rev. 8 (1), 77–100. Berridge, K.C., Robinson, T.E., Aldridge, J.W., 2009. Dissecting components of reward: ‘liking’, ‘wanting’, and learning. Curr. Opin. Pharmacol. 9 (1), 65–73. Blanchard, J.J., Cohen, A.S., 2005. The structure of negative symptoms within schizophrenia: implications for assessment. Schizophr. Bull. 32 (2), 238–245. Blanchard, J.J., Kring, A.M., Horan, W.P., Gur, R., 2011. Toward the next generation of negative symptom assessments: the collaboration to advance negative symptom assessment in schizophrenia. Schizophr. Bull. 37 (2), 291–299. Bora, E., Murray, R.M., 2014. Meta-analysis of cognitive deficits in ultra-high risk to psychosis and first-episode psychosis: do the cognitive deficits progress over, or after, the onset of psychosis? Schizophr. Bull. 40 (4), 744–755. Cedro, A., Kokoszka, A., Popiel, A., Narkiewicz-Jodko, W., 2001. Alexithymia in schizophrenia: an exploratory study. Psychol. Rep. 89 (1), 95–98. Chan, R.C., Wang, Y., Huang, J., Shi, Y., Wang, Y., Hong, X., ... Kring, A.M., 2010. Anticipatory and consummatory components of the experience of pleasure in schizophrenia: cross-cultural validation and extension. Psychiatry Res. 175 (1), 181–183. Chan, R.C., Shi, Y.-F., Lai, M.-K., Wang, Y.-N., Wang, Y., Kring, A.M., 2012. The Temporal Experience of Pleasure Scale (TEPS): exploration and confirmation of factor structure in a healthy Chinese sample. PLoS One 7 (4), e35352. Chan, R.C.K., Gooding, D.C., Shi, H.S., Geng, F.L., Xie, D.J., Yang, Z.Y., Liu, W.H., Wang, Y., Yan, C., Shi, C., Lui, S.S.Y., Cheung, E.F.C., 2016. Evidence of structural invariance across three groups of Meehlian schizotypes. NPJ Schizophr. 2:16016. http://dx.doi.org/ 10.1038/npjschz.2016.16. Chapman, L.J., Chapman, J.P., Raulin, M.L., 1976. Scales for physical and social anhedonia. J. Abnorm. Psychol. 85 (4), 374. Dawes, S., Suarez, P., Casey, C., Cherner, M., Marcotte, T., ... Heaton, R., 2008. Variable patterns of neuropsychological performance in HIV-1 infection. J. Clin. Exp. Neuropsychol. 30 (6), 613–626. Eckblad, M.L., Chapman, L.J., Chapman, J.P., Mishlove, M., 1982. The Revised Social Anhedonia Scale. [Unpublished Psychological Test] (In press). Everitt, B., Landau, S., Leese, M., 2001. Cluster Analysis. 2001Arnold, London. Foussias, G., Remington, G., 2010. Negative symptoms in schizophrenia: avolition and Occam's razor. Schizophr. Bull. 36 (2), 359–369. Gard, D.E., Gard, M.G., Kring, A.M., John, O.P., 2006. Anticipatory and consummatory components of the experience of pleasure: a scale development study. J. Res. Pers. 40 (6), 1086–1102. Gong, Y.X., 1992. Manual of Wechsler Adult Intelligence Scale-Chinese Version. Chinese Map Press, Changsha. Gross, J.J., 1998. Antecedent-and response-focused emotion regulation: divergent consequences for experience, expression, and physiology. J. Pers. Soc. Psychol. 74 (1), 224. Gross, J.J., 2002. Emotion regulation: affective, cognitive, and social consequences. Psychophysiology 39 (3), 281–291. Gross, J.J., John, O.P., 2003. Individual differences in two emotion regulation processes: implications for affect, relationships, and well-being. J. Pers. Soc. Psychol. 85 (2), 348. Gross, J.J., Levenson, R.W., 1993. Emotional suppression: physiology, self-report, and expressive behavior. J. Pers. Soc. Psychol. 64 (6), 970. Gross, J.J., Levenson, R.W., 1997. Hiding feelings: the acute effects of inhibiting negative and positive emotion. J. Abnorm. Psychol. 106 (1), 95.

Gross, J.J., Thompson, R.A., 2007. Emotion Regulation: Conceptual Foundations. Häfner, H., Maurer, K., Trendler, G., an der Heiden, W., Schmidt, M., Könnecke, R., 2005. Schizophrenia and depression: challenging the paradigm of two separate diseases—a controlled study of schizophrenia, depression and healthy controls. Schizophr. Res. 77 (1), 11–24. an der Heiden, W., Leber, A., Häfner, H., 2016. Negative symptoms and their association with depressive symptoms in the long-term course of schizophrenia. Eur. Arch. Psychiatry Clin. Neurosci. 266 (5), 387–396. Heiy, J.E., Cheavens, J.S., 2014. Back to basics: a naturalistic assessment of the experience and regulation of emotion. Emotion 14 (5), 878. Hooker, C., Park, S., 2002. Emotion processing and its relationship to social functioning in schizophrenia patients. Psychiatry Res. 112 (1), 41–50. Kay, S.R., Flszbein, A., Opfer, L.A., 1987. The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophr. Bull. 13 (2), 261. Kring, A.M., Caponigro, J.M., 2010. Emotion in schizophrenia where feeling meets thinking. Curr. Dir. Psychol. Sci. 19 (4), 255–259. Kring, A.M., Elis, O., 2013. Emotion deficits in people with schizophrenia. Annu. Rev. Clin. Psychol. 9, 409–433. Kring, A.M., Gur, R.E., Blanchard, J.J., Horan, W.P., Reise, S.P., 2013. The clinical assessment interview for negative symptoms (CAINS): final development and validation. Am. J. Psychiatry 170 (2), 165–172. Lange, R., Iverson, G., Senior, G., Chelune, G., 2002. A primer on cluster analysis applications to cognitive rehabilitation research. J. Cogn. Rehabil. 20 (1), 16–33. Li, W., Hengchao, L., Zhongquan, L., 2007. Reliability and validity of emotion regulation questionnaire Chinese revised version. Chin. J. Health Psychol. 6, 013. Li, Z., Lui, S.S., Geng, F.-I., Li, Y., Li, W.-X., Wang, C.-Y., ... Chan, R.C., 2015. Experiential pleasure deficits in different stages of schizophrenia. Schizophr. Res. 166 (1), 98–103. Li, Y., Mou, X., Jiang, W., Yang, Z., Shen, X., Jin, Z., ... Zhang, J., 2015. A comparative study of anhedonia components between major depression and schizophrenia in Chinese populations. Ann. General Psychiatry 14 (1), 24. Lui, S.S.Y., Wang, Y., Shi, Y.-F., Au, A.C.W., Wong, P.T.Y., Chu, Z.L.S., ... Chan, R.C.K., 2015. Subjective pleasure experience in patients with recent-onset schizophrenia: a preliminary report. Psychiatry Res. 228 (1):166–169. http://dx.doi.org/10.1016/ j.psychres.2015.04.013. Majadas, S., Olivares, J., Galan, J., Diez, T., 2012. Prevalence of depression and its relationship with other clinical characteristics in a sample of patients with stable schizophrenia. Compr. Psychiatry 53 (2), 145–151. Mancevski, B., Keilp, J., Kurzon, M., Berman, R.M., Ortakov, V., Harkavy-Friedman, J., ... Dwork, A.J., 2007. Lifelong course of positive and negative symptoms in chronically institutionalized patients with schizophrenia. Psychopathology 40 (2), 83–92. Mandal, M.K., Pandey, R., Prasad, A.B., 1998. Facial expressions of emotions and schizophrenia: a review. Schizophr. Bull. 24 (3), 399. Mandal, M.K., Jain, A., Haque-Nizamie, S., Weiss, U., Schneider, F., 1999. Generality and specificity of emotion-recognition deficit in schizophrenic patients with positive and negative symptoms. Psychiatry Res. 87 (1), 39–46. Mooi, E., Sarstedt, M., 2011. Cluster Analysis. A Concise Guide to Market Research. pp. 237–284. Myin-Germeys, I., Delespaul, P.A., deVries, M.W., 2000. Schizophrenia patients are more emotionally active than is assumed based on their behavior. Schizophr. Bull. 26 (4), 847. Oorschot, M., Lataster, T., Thewissen, V., Lardinois, M., Wichers, M., van Os, J., ... MyinGermeys, I., 2013. Emotional experience in negative symptoms of schizophrenia—no evidence for a generalized hedonic deficit. Schizophr. Bull. 39 (1):217–225. http:// dx.doi.org/10.1093/schbul/sbr137. Painter, J.M., Kring, A.M., 2016. Toward an understanding of anticipatory pleasure deficits in schizophrenia: memory, prospection, and emotion experience. J. Abnorm. Psychol. 125 (3), 442. Strauss, G.P., Herbener, E.S., 2011. Patterns of emotional experience in schizophrenia: differences in emotional response to visual stimuli are associated with clinical presentation and functional outcome. Schizophr. Res. 128 (1–3):117–123. http://dx.doi.org/ 10.1016/j.schres.2011.01.010. Taylor, G.J., Bagby, R.M., Parker, J.D., 2003. The 20-Item Toronto Alexithymia Scale: IV. Reliability and factorial validity in different languages and cultures. J. Psychosom. Res. 55 (3), 277–283. Trémeau, F., 2006. A review of emotion deficits in schizophrenia. Dialogues Clin. Neurosci. 8 (1), 59. Wang, Y., Neumann, D., Shum, D.H.-K., Chan, R.C.K., 2012. A cross-validation study of clustering of schizotypy using a non-clinical Chinese sample. Psychiatry Res. 200, 55–58. Webb, T.L., Miles, E., Sheeran, P., 2012. Dealing with feeling: a meta-analysis of the effectiveness of strategies derived from the process model of emotion regulation. Psychol. Bull. 138 (4), 775. Yan, C., Yang, T., Yu, Q.-J., Jin, Z., Cheung, E.F.C., Liu, X., Chan, R.C.K., 2015. Rostral medial prefrontal dysfunctions and consummatory pleasure in schizophrenia: a meta-analysis of functional imaging studies. Psychiatry Res. Neuroimaging 231 (3):187–196. http://dx.doi.org/10.1016/j.pscychresns.2015.01.001. Yuan, Y., Shen, X., Zhang, X., 2003. The reliability and validity of Toronto alexithymia scale (TAS-20) [J]. Sichuan Ment. Health 1.

Please cite this article as: Zou, Y., et al., Profiling of experiential pleasure, emotional regulation and emotion expression in patients with schizophrenia, Schizophr. Res. (2017), http://dx.doi.org/10.1016/j.schres.2017.08.048