Nonverbal expressive behaviour in schizophrenia

1 downloads 0 Views 456KB Size Report
Covariables include the Positive and Negative Syndrome Scale (PANSS), the anxiety level ..... social anxiety was measured by a self-rating version of the Liebowitz-Social-. Anxiety-Scale (LSAS) ..... tion, extrapyramidal symptoms and the expressive behaviour ..... Wechsler Abbreviated Scale of Intelligence (WASI).
Psychiatry Research ∎ (∎∎∎∎) ∎∎∎–∎∎∎

Contents lists available at SciVerse ScienceDirect

Psychiatry Research journal homepage: www.elsevier.com/locate/psychres

Nonverbal expressive behaviour in schizophrenia and social phobia Jonathan Del-Monte a,b,c,n, Stéphane Raffard a,b, Robin N. Salesse c, Ludovic Marin c, Richard C. Schmidt d, Manuel Varlet c, Benoît G. Bardy c, Jean Philippe Boulenger b,e, Marie Christine Gély-Nargeot a, Delphine Capdevielle b,e a Epsylon, Laboratory Dynamic of Human Abilities & Health Behaviors, Department of Sport Sciences, Psychology and Medicine, University of Montpellier & St-Etienne, France b University Department of Adult Psychiatry, Hôpital de la Colombière, CHU Montpellier, Montpellier-1 University, Montpellier, France c Movement to Health Laboratory, EuroMov, Montpellier-1 University, Montpellier, France d Department of Psychology, College of the Holy Cross, Worcester, MA, USA e INSERM U-1061, Montpellier, France

art ic l e i nf o

a b s t r a c t

Article history: Received 4 December 2012 Received in revised form 24 May 2013 Accepted 27 May 2013

Expressive behaviour plays a crucial role in the success of social interactions. Abnormality of expressive behaviour has been reported in interpersonal interactions of patients suffering from schizophrenia and social phobia, two debilitating mental disorders with important social deficits. However, no study has compared the expressive behaviour in these two disorders. Thirty schizophrenia patients, 21 social phobia patients and 30 healthy controls were evaluated and compared on expressive, cognitive and clinical dimensions. Expressive behaviour was assessed using the Motor Affective subscale of the MotorAffective-Social-Scale (MASS). Covariables include the Positive and Negative Syndrome Scale (PANSS), the anxiety level Liebowitz-Social-Anxiety-Scale (LSAS) and cognitive tasks. After controlling for depression, schizophrenia and social phobia patients both exhibited significantly fewer expressive behaviours compared to healthy controls. Moreover, our results showed specific signatures: schizophrenia patients performed fewer spontaneous gestures (hand gestures and smiles) whereas social phobia patients had an impaired ability to produce voluntary smiles in comparison to healthy controls. Interestingly, poor social functioning was significantly correlated with a decrease of expressive behaviour for schizophrenia patients. Expressive behaviour is impaired in different ways in social phobia and schizophrenia and is associated in schizophrenia with poorer social functioning. The Motor Affective subscale of the MASS is an interesting tool for assessing the dysfunction of interpersonal expressive behaviour in mental disorders. & 2013 Elsevier Ireland Ltd. All rights reserved.

Keywords: Nonverbal expressive behaviours Schizophrenia Social phobia Negative symptoms Social functioning

1. Introduction Nonverbal expressive behaviour is a critical feature of successful social interaction and interpersonal rapport (Krauss et al., 1996). Expressive gestures that accompany speech play a fundamental role in human communication, particularly to improve communication's quality, to modulate listener's actions and to convey information beyond that of the speakers' words (Ekman and Friesen, 1969; Goldin-Meadow, 1999; Schmidt and Richardson, 2008). Social deficits are a feature of many mental disorders, such as schizophrenia and social phobia (American Psychiatry Association, 2004), including many symptoms such as emotional

n Correspondence to: Laboratory Epsylon EA 4556, Laboratory Dynamics of Human Abilities & Health Behaviors, Department of Medicine, Subject and Society Sciences, Sport Sciences, University of Montpellier and St-Etienne, 4 Boulevard Henri IV, 34000 Montpellier, France. Tel.: +33 411 757065. E-mail address: [email protected] (J. Del-Monte).

(Phillips and Seidman, 2008; Bourke et al., 2012) or social functioning deficits (Sidlova et al., 2011; Panayiotou and Karekla, 2012). Past studies have attempted to explain social interaction disorders through social cognition deficits in both schizophrenia (Green et al., 2008) and social phobia (Tibi-Elhanany and ShamayTsoory, 2011). Brüne et al. (2009) have explored links between social cognition and nonverbal expressiveness in schizophrenia spectrum disorders. Patient's non-verbal behaviours were assessed using the Ethological Coding System for Interviews (ECSI). Results showed that schizophrenia patients had fewer prosocial behaviours compared to healthy controls and a partial correlation existed between reduced prosocial behaviour and social competence especially as indexed by the false-belief mentalising task for the schizophrenia group. Impairment in expressiveness thus seems to be a fundamental component of the social interaction disorder in schizophrenia. However, too few studies take into account the importance of the expressive behaviour in mental disorders with social interaction

0165-1781/$ - see front matter & 2013 Elsevier Ireland Ltd. All rights reserved. http://dx.doi.org/10.1016/j.psychres.2013.05.034

Please cite this article as: Del-Monte, J., et al., Nonverbal expressive behaviour in schizophrenia and social phobia. Psychiatry Research (2013), http://dx.doi.org/10.1016/j.psychres.2013.05.034i

2

J. Del-Monte et al. / Psychiatry Research ∎ (∎∎∎∎) ∎∎∎–∎∎∎

deficits. Yet, reductions in expressive behaviour have been reported in patients suffering from schizophrenia, in the expressions of facial affect or in body movements (Trémeau et al., 2005; Brüne et al., 2009), and from social phobia, in facial expressions or eye gaze (Melfsen et al., 2000; Schneier et al., 2011). Despite these behavioural similarities, no study has explicitly compared expressive behaviour deficits and how they appear in these two disorders. Knowing whether expressive behaviour deficits represent the behavioural signature of similar symptoms and clinical causes, or not, seems to be particularly relevant in understanding and treating schizophrenia and social phobia. Consequently, it is fundamental to assess and to compare the expressive behaviour dimension of social interactions in both schizophrenia and social phobia. Concerning schizophrenia, several studies have demonstrated a reduction in expressive behaviour (Trémeau et al., 2005; Brüne et al., 2009). Past research has shown that schizophrenia patients show a decrease in spontaneous facial expression (SFE) (SteimerKrause et al., 1990) and more particularly have fewer spontaneous smiles in funny situations compared to healthy controls (Henry et al., 2007). SFE was also found to be negatively correlated with negative symptoms. Other studies have compared SFE in schizophrenia patients with SFE in other mental disorders. Bersani et al. (2012) compared facial expressions in schizophrenia and in obsessive-compulsive disorder (OCD). All patients watched emotion-eliciting video clips while facial activity was videotaped. Results demonstrated that facial expressions were reduced in schizophrenia and OCD compared to healthy controls but not significantly different from each other. Earlier, Trémeau et al. (2005) assessed facial expressive behaviours (FEB), including spontaneous and voluntary facial expressions (VFE) and facial coverbal gestures, and speech flow in schizophrenia patients, depressed patients and healthy controls. They used a narrative task in which an emotion was described. Results demonstrated that schizophrenia patients and depressed patients were impaired in all FEB compared to healthy controls. Schizophrenia patients and depressed patients were equally impaired in voluntary and spontaneous facial expressions and facial coverbal gestures. However, Trémeau et al. (2005) found that schizophrenia patients spoke less than the depressed patients; and moreover, in schizophrenia, all FEB correlated with an index of negative symptoms. Other studies have examined body movements, including hand and head gestures, during social interactions in schizophrenia. Recently, Lavelle et al. (2012) showed that schizophrenia patients speak less and make less use of hand gestures when speaking compared to healthy controls in a social interaction. Further, results exhibited that reductions in expressiveness in schizophrenia, seem modulated by the type and the intensity of symptomatology. Patients with more positive symptoms used more nonverbal behaviours to demonstrate understanding and provide feedback to their speaking partner. Their partners appeared to compensate for this by providing fewer of these cues when they were listening. Patients with more negative symptoms displayed less nodding when listening, thus providing fewer indicators of their understanding to their speaking partner. Their partner appears to respond to this by gesturing more while speaking. However, patients with more negative symptoms also gestured more when speaking. The patients may be increasing their use of gestures while speaking in response to the reduced nonverbal feedback being displayed by the listening partners. According to authors, patients' gestures could be used as a possible indicator of the interpersonal relationship quality within the interaction. This indicator has been also proposed by Mittal et al. (2011), suggesting that an increased amount of abnormal movement predicts poorer social functioning in individuals with a high risk for developing schizophrenia.

Despite the fact that expressive behaviours play a fundamental role in social interactions (Goldin-Meadow, 1999), few studies have assessed this dimension in social phobia. Past research suggests that adults with social phobia exhibit expressive behaviour deficits (Schneier et al., 2011). Moukheiber et al. (2010) has observed gaze avoidance during social interaction. Also Melfsen et al. (2000) assessed spontaneous and voluntary facial expressions in socially anxious children. Children's SFE were covertly recorded when they were trying to solve a puzzle and while watching a funny movie. Additionally, they were asked to produce voluntary facial expressions (VFE). Results showed that children with social anxiety exhibited fewer SFE and showed poorer performance in voluntary expression of happiness, surprise and fear. Hence, research suggests that facial and body movements might be considered as behavioural indicators of the level of anxiety. However, the lack of studies documenting expressive behaviours in social phobia suggests a need for further investigation of this domain. Moreover, often in previous research on expressive behaviours in schizophrenia and social phobia methodological issues have made it difficult to draw valid conclusions. The use of numerous different tools to assess, in laboratory, expressive behaviours does not allow a reliable comparison between studies. In order to propose a more ecological and more clinical assessment of expressive behaviours deficits, Trémeau et al. (2008) developed the Motor-Affective-Social-Scale (MASS) for schizophrenia. The first part of this scale, the Motor Affective subscale of the MASS, is used to assess fundamental expressive deficits through evaluating spontaneous smiles, hand gestures, voluntary smiles and speech flow. The second part of the MASS assesses the lack of initiation (avolition) through motor retardation, personal hygiene, attendance at groups and verbal interaction. Trémeau et al. (2008) found that the MASS score correlated highly with the PANSS negative symptomatology score. Unfortunately, researchers have not investigated how the MASS relates to measures of social functioning. Investigating such relationships will reveal whether a link exists between problems of social functioning in patients and their prosocial expressive behaviour deficits. The aims of the current study were thus (i) to investigate and compare expressive behaviours in schizophrenia and social phobia using the Motor Affective subscale of the MASS. In addition, as numerous studies have shown a link between cognition functioning and intrapersonal motor behaviours (Smits-Engelsman and Hill, 2012; Mohan et al., 2001), we investigated the relationship between nonverbal expressive behaviours and cognitive and clinical variables in schizophrenia and social phobia. We hypothesized that cognitive functioning deficits would be positively correlated with expressive behaviour impairments and that clinical variables, such as anxiety level, would be negatively correlated with expressive behaviour impairments.

2. Material and method 2.1. Recruitment Fifty-one patients diagnosed with schizophrenia (n ¼30) and social phobia (n ¼21), according to DSM-IV-TR, participated in the study. The control group consisted of 30 healthy participants. All control participants were communitydwelling adults living in Montpellier, France, and were recruited from local associative networks. They had no personal history of psychosis nor did any firstdegree relative. Exclusion criteria for the controls were a positive history of neurological or psychiatric disease or the presence of medication intake known to influence cognition. Controls meeting clinical criteria for major depressive episode or anxiety disorder as confirmed using the mini-international neuropsychiatric interview (Sheehan et al., 1998) were also excluded. According to the current treating psychiatrist, patients were in the stable phase of the illness defined as having no hospitalizations or changes in housing in the month prior to entering

Please cite this article as: Del-Monte, J., et al., Nonverbal expressive behaviour in schizophrenia and social phobia. Psychiatry Research (2013), http://dx.doi.org/10.1016/j.psychres.2013.05.034i

J. Del-Monte et al. / Psychiatry Research ∎ (∎∎∎∎) ∎∎∎–∎∎∎ the study. All patients were receiving outpatient treatment in the urban community of Montpellier. Individuals with schizophrenia were receiving antipsychotic medication at the time of participation in this study. Exclusion criteria for both groups were (a) known neurological disease, (b) developmental disability, or (c) substance abuse in the past month. Participants were recruited from the University Department of Adult Psychiatry in Montpellier. The Ethics Committee of the University Hospital of Montpellier approved the study (CPP Sud Méditérannée III, Montpellier, France, AFSSAPS 2009-A00513-54 24, 07/22/2009). 2.2. Instruments Subjects were asked to participate in nonverbal expressive behaviour tasks and to complete questionnaires. In the first session, for schizophrenia patients, symptom ratings were obtained using the Positive and Negative Syndrome Scale (PANSS) (Kay et al., 1987) and social functioning was assessed by the modified prosocial subscale of the PANSS (Baran and Docherty, 2008) by a first experimenter. The prosocial subscale is composed of four items: G16: Active social avoidance, N2: Emotional withdrawal, N4: Passive/apathetic social withdrawal and N5: Difficulty in abstract thinking items. A high score on the prosocial subscale reflects emotional withdrawal and a lack of social interaction. Finally, for schizophrenia patients, extra pyramidal symptoms were assessed using the Simpson–Angus-Scale (SAS) (Simpson and Angus, 1970). In the second session, expressive behaviours, cognitive functions and clinical variables were evaluated for all participants. 2.2.1. Nonverbal expressive behaviours task The Motor Affective subscale of the MASS (Trémeau et al., 2008) was used to measure expressiveness in social interactions. During a structured interview, participants were asked three questions in the same order. First, participants were asked to report everything they did the day before (for 2 min). Second, they were asked to describe a movie from memory (for 1 min). Third, they were asked to imagine what they would do if given one million Euros (for 30 s). Interviewers were instructed to ask predefined questions each time the participant's speech flow stopped for 3 s. Four behaviours were recorded and rated: spontaneous smiles, spontaneous hand gestures, speech flow and voluntary facial expression. Each occurrence of these behaviours was recorded on a pre-defined rating sheet. After the interview, participants were asked to make their “most beautiful smile”, and pre-defined behavioural anchors were used to rate the posed smiling. A high score on the Motor Affective subscale means less impairment of expressiveness. Clinical ratings were obtained after these tasks during the same interview. 2.2.2. Cognitive and clinical tasks For all subjects, verbal working memory span was measured using the Letter Number Sequencing task (Wechsler, 1999). Subjects were verbally presented with a series of letters and numbers and asked to report back the numbers in numerical order, followed by the letters in alphabetical order. Visual sustained attentional function was assessed using the Concentration–Endurance Test (d2 test) (Brickenkamp, 1994). In this test, the items are composed of the letters “d” and “p” with one, two, three or four dashes arranged either individually or in pairs above and below the letter. Participants are given 20 s to scan each line and mark all “d's” with two dashes. Finally, Premorbid IQ was assessed using the French National Adult Reading Test (fNART) (Mackinnon and Mulligan, 2005), depression was assessed using the Beck Depression Inventory-II (BDI-II) (Beck et al., 1996) and social anxiety was measured by a self-rating version of the Liebowitz-SocialAnxiety-Scale (LSAS) (Liebowitz, 1987). 2.3. Statistical analysis Clinical ratings and Motor Affective subscale scores were separately compared for the three groups with a non-parametric Kruskal–Wallis test. In order to compare the scores of schizophrenia, social phobia patients and healthy control group, non-parametric U-Mann–Whitney tests were computed. The level of significance was set to p o 0.05. Spearman non-parametric correlations were used to explore the relationships between expressive behaviour scores, cognitive data and clinical data. We did not use a Bonferroni's correction, usually employed to correct type I errors, as it is considered to be particularly conservative and to dramatically increase the risk of rejection of true correlations (Vialatte and Cichoki, 2008). Taking the multiple correlations into account, we decided to use p o 0.01 to reduce type I errors due to multiple tests.

3. Results 3.1. Mean ratings and group comparisons Mean ratings and group comparisons on the demographical data, fNART (premorbid IQ) and BDI-II are reported in Table 1. The

3

results revealed significant group differences on the premorbid IQ and level of education. Social phobia group has significantly higher scores than schizophrenia and healthy control groups, which were statistically equivalent. Mean ratings and group comparisons on the d2 test, Letter Number Sequencing and the LSAS are reported in Table 2. Schizophrenia patients were impaired in d2 test relative to the healthy control and social phobia groups. We found no significant difference between social phobia patients and healthy controls on the d2 test. The LSAS score showed that social phobia patients had a significantly higher score compared to the schizophrenia and healthy control groups. No significant difference was found between the schizophrenia patients and the healthy controls. Mean ratings and group comparisons on the expressive behaviours assessed by the Motor Affective subscale are presented in Fig. 1. Schizophrenia and social phobia groups were significantly impaired on expressiveness compared to the healthy control group (Mean: 10.66, S.D.: 2.08/ Mean: 10.76, S.D.: 2.16/ Mean: 12.3, S.D.: 1.68, respectively, H¼ 11.267, p o0.05). Results showed that schizophrenia patients exhibited fewer expressive behaviours compared to the healthy controls (z¼ −3.094, p o0.05). Additonally, social phobia patients produced fewer expressive behaviours compared to the healthy controls (z ¼−2.445, p o0.05). Finally, the analysis failed to reveal significant differences between the schizophrenia and social phobia groups. The item scores of the Motor Affective subscale, presented in Fig. 2 reveal significant differences between patient groups and healthy controls as well. Schizophrenia patients were impaired in the number of spontaneous smiles (Mean: 2.66, S.D.: 0.95) and hand gestures (Mean: 2, S.D.: 0.90) in comparison to the healthy controls (Smiles: Mean: 3.5, S.D.: 0.68, Hand gestures: Mean: 2.66, S.D.: 0.71, Smiles: z ¼ −3.343, p o0.05, Hand gestures: z¼ −2.787, p o0.05), but not in comparison with the social phobia patients (Smiles: Mean: 2.95, S. D.: 1.20; Hand gestures: Mean: 2.23, S.D.: 0.94, Smiles: z ¼−0.973, p4 0.05; Hand gestures: z¼ −0.919, p 40.05). Moreover, social phobia patient's scores were equivalent to healthy controls. Thus, schizophrenia patients exhibited a spontaneous gesture deficit whereas social phobia patients failed to reveal this deficit. Concerning the speech flow dimension, social phobia patients exhibited significantly higher scores compared to healthy controls (Mean: 3.52; S.D.: 0.75, Mean: 3.33, S.D.: 0.68, respectively, z ¼ −2.141, p o0.05) and schizophrenia patients (Mean: 3.21, S.D.: 0.61, z¼ −2.739, p o0.05). No difference was found between schizophrenia patients and healthy controls. Finally, social phobia patients were qualitatively impaired on the voluntary facial expressions (VFE) relative to the healthy controls (Mean: 2.04, S.D.: 1.12, Mean: 2.83, S.D.: 1.06, respectively, z¼ −2.346, p o0.05) and the schizophrenia patients (Mean: 2.80, S.D.: 1.09, z¼ −2.256, p o0.05). Healthy control and schizophrenia groups were equivalent. Thus, social phobia patients exhibited a VFE deficit whereas schizophrenia patients have normal scores. 3.2. Correlations analyses All confounding variables such as depression, education level and premorbid IQ have been controlled in correlation analyses for the schizophrenia and the social phobia groups. In schizophrenia group, Spearman's correlations revealed a negative correlation between the expressive behaviour scores and negative symptomatology as assessed by the PANSS (r ¼−0.460, p ¼0.016). Finally, a negative correlation was also observed between the prosocial functioning score evaluated by the modified prosocial and the expressive behaviour scores (r ¼ −0.441, p o0.02). There is a link between the social difficulties exhibited by schizophrenia patients and their expressive behaviour deficits. Analyses failed to reveal any other correlations between clinical variables and the Motor

Please cite this article as: Del-Monte, J., et al., Nonverbal expressive behaviour in schizophrenia and social phobia. Psychiatry Research (2013), http://dx.doi.org/10.1016/j.psychres.2013.05.034i

J. Del-Monte et al. / Psychiatry Research ∎ (∎∎∎∎) ∎∎∎–∎∎∎

4

Table 1 Demographic characteristics of patients and healthy controls.

Age (years) Sex ratio Education level fNART (Premorbid IQ ) BDI-II PANSS positive PANSS negative PANSS psychopathology PANSS Total Prosocial PANSS items Simpson–Angus scale First generation antipsychotic Second generation antipsychotic

Schizophrenia (SZ) (n¼ 30)

Social phobia (SP) (n¼21)

Control (CT) (n¼ 30)

Means

S.D.

Means

S.D.

Means

S.D.

37.50 18M/12F 11.43 104.13 14 14.63 19.50 35.16 69.36 14.65 6.10 11 19

10.50

33.19 12M/9F 13.85 111.19 20.52 – – – – – – – –

12.67

31.66 11M/19F 12.13 106.70 7.53 – – – – – – – –

13.22

2.36 7.84 8.59 5.46 5.29 7.71 14.14 3.90 3.23

2.30 4.87 11.07 – – – – – – – –

2.28 7.96 5.63 – – – – – – – –

d.f.

Statisticsa

p

Contrasts

2 1 2 2 2 – – – – – – – –

H¼ 4.151 X2 ¼ 3.750 H¼ 11.428 H¼ 11.428 H¼ 21.008 – – – – – – – –

0.125 0.153 0.003* 0.004* 0.000* – – – – – – – –

– – SP 4CT ¼SZ SP 4CT ¼SZ SP 4SZ 4 CT – – – – – – – –

BDI-II: Beck Depression Inventory II and PANSS: Positive and Negative Syndrome Scale. a n

Kruskal–Wallis test or analysis of variance. p o0.05.

Table 2 Cognitive and clinical variables of patients and healthy controls.

Concentration–Endurance Test (d2) Letter Number Sequencing task LSAS anxiety LSAS avoidance LSAS anxiety in social interaction LSAS avoidance in social interaction LSAS performance anxiety LSAS performance avoidance

Schizophrenia (SZ) (n¼ 30)

Social phobia (SP) (n¼ 21)

Control (CT) (n¼ 30)

Means

S.D.

Means

S.D.

Means

S.D.

118.16 8.93 25.26 21.84 11.48 9.75 14.00 11.82

37.26 2.94 13.13 12.85 7.55 6.30 7.31 7.42

185.90 11.95 40.52 32.76 18.19 15.23 22.66 17.52

46.05 3.44 14.31 17.72 8.34 8.94 6.54 9.51

180.53 11.36 25.20 19.53 9.20 8.26 15.96 10.92

41.53 3.12 13.36 9.87 4.97 4.82 9.04 5.57

d.f.

Statisticsa

p

Contrasts

2 2 2 2 2 2 2 2

H¼ 33.315 H¼ 12.342 H¼ 15.794 H¼ 9.092 H¼ 14.984 H¼ 8.296 H¼ 17.255 H¼ 8.347

o 0.0001 o 0.002 o 0.0001 0.011 o 0.001 0.016 o 0.0001 0.015

SP ¼CT 4SZ SP ¼CT 4SZ SP 4CT¼ SZ SP 4CT¼ SZ SP 4CT¼ SZ SP 4CT¼ SZ SP 4CT¼ SZ SP 4CT¼ SZ

LSAS: Liebowitz-Social-Anxiety-Scale. Significant: p o 0.05. a

Kruskal–Wallis test or analysis of variance.

Affective subscale. In the absence of a direct measure of social life that could explain expressive behaviour impairments in schizophrenia patient, we have compared the number of prompts to revive the speech for the first and third response questions for the schizophrenia patients and control participants. Results show that the groups were equivalent for both questions (Q1: Schizophrenia, Mean: 1.56, S.D.: 1.40 and Control, Mean: 0.93, S.D.: 1.11, (F(1,58)¼ 3.743, p 40.05) and Q3: Schizophrenia, Mean: 0.43, S.D.: 0.81 and Control, Mean: 0.26, S.D.: 0.58, (F(1,58)¼−0.860, p 40.05). Although they had fewer expressive gestures during the task compared to control participants, the patients were not prompted more for either question 1 or 3. In addition, to assess “retrieval fluency” and verbal output impairments at a clinical level in individuals with schizophrenia, we used items P2 (disorganization of thought and language) and N6 (lack of spontaneity and flow of conversation) from the PANSS. We found no significant correlation between P2 and N6 subscales of the PANSS and the number of stimulus to revive the speech to third question. For the social phobia group, Spearman's correlations revealed no significant relations between cognitive and clinical variables and the Motor Affective subscale scores.

4. Discussion The main goal of this study was to investigate and compare nonverbal expressiveness in schizophrenia and social phobia. We

Fig. 1. Patient groups were impaired on expressivity behaviours compared to healthy control group. Social phobia and schizophrenia patients were equivalent. *p o 0.05, **p o 0.01, and error bars represent standard error of means.

used the Motor Affective subscale of the MASS to assess spontaneous smile expressions, spontaneous hand gestures, voluntary facial expression and the speech flow in these two disorders, and a variety of measures such as the LSAS as well as modified prosocial subscale from the PANSS scale to measure social functioning. In line with our hypothesis that nonverbal expressiveness will be reduced in both disorders, results showed that schizophrenia patients and social phobia patients have significantly fewer expressive behaviours compared to the healthy controls. These results are consistent with the past literature (Melfsen et al., 2000;

Please cite this article as: Del-Monte, J., et al., Nonverbal expressive behaviour in schizophrenia and social phobia. Psychiatry Research (2013), http://dx.doi.org/10.1016/j.psychres.2013.05.034i

J. Del-Monte et al. / Psychiatry Research ∎ (∎∎∎∎) ∎∎∎–∎∎∎

5

Fig. 2. According to the Motor affective subscale of the MASS, SZ patients were impaired on the spontaneous behaviours compared to CT group. SP and CT groups were equivalent. SP patients exhibited a significant high score of speech flow compared to CT and SZ groups. SZ and CT groups were equivalent. SP patients were impaired on the voluntary expression compared to CT and SZ groups. SZ and CT were equivalent. Error bars represent standard error of the means.

Trémeau et al., 2005). Similarly to Trémeau et al. (2008), we found a negative correlation between negative symptoms and the expressive behaviour deficit for the schizophrenia group. In addition to the correlation with negative symptoms, our results showed a negative correlation between the expressive behaviour deficit and social functioning as assessed by the modified prosocial subscale of the PANSS. This measure reflects impairment in interpersonal engagement and has been shown to be an adequate assessment of real world social functioning in schizophrenia (Baran and Docherty, 2008). Thus, we have found that deficits in expressive behaviour are related to social functioning difficulties in schizophrenia, confirming that expressive behaviour deficits are a factor in social functioning impairments in schizophrenia. Nevertheless, we did not find a link between cognitive functioning deficits and nonverbal expressiveness for either disorder. These results are inconsistent with past studies (Smits-Engelsman and Hill, 2012; Mohan et al., 2001) and can perhaps be explained by a lack of sensitivity of our assessments. Future research should examine more closely the relationship between cognitive functioning deficits and expressive behaviour impairments in mental disorders with social interaction deficits. Another important finding that our results revealed is that the expressive behaviour deficit was different for the two disorders. Schizophrenia patients were found to have significantly fewer spontaneous gestures (hand gestures and smiles) compared to both the social phobia and the healthy control groups. These results are consistent with the literature since several studies have shown that patients suffering from schizophrenia have fewer spontaneous hand gestures (Kupper et al., 2010; Lavelle et al., 2012) and fewer spontaneous facial expressions (Henry et al., 2007). However, social phobia patients and healthy controls were found to have equivalent spontaneous expressive gestures. These observations, i.e., spontaneous expressive gestures impaired in schizophrenia and preserved in social phobia, suggest that the expressive behaviour deficit is expressed differently in the social deficits of these two disorders. With regard to the speech flow dimension, social phobia patients have higher scores in comparison to the schizophrenia and the healthy control groups. Observations reported by the experimenter revealed that social phobia patients did not stop talking during the interview. Even if this result seems surprising, we hypothesize, following Stopa and Clark's (1993) interpretation, that social phobia patients spoke quickly and avoided pauses in

their speech because they believed other people might think that they were boring or anxious if they stopped talking. By comparison, the schizophrenia group and the healthy control group were equivalent on the speech flow dimension. This higher speech flow score is a second difference between schizophrenia and social phobia that allows a greater degree of differentiation between these two disorders in terms of expressive gestures assessed by the Motor Affective subscale of the MASS. In addition to the speech flow differences, we found that social phobia patients had impaired ability to produce a voluntary facial expression (i.e., a smile) compared to schizophrenia patients and healthy controls. This result is consistent with the literature (Melfsen et al., 2000). More precisely, Clark and Well's cognitive model (1995) suggests that, based on early experience, patients with social phobia develop a series of assumptions about themselves and their social world. When individuals with social phobia believe that they are in a situation in which they may receive a negative evaluation by others, they shift their attention to detailed monitoring and observation on themselves. During the voluntary facial expression (VFE) assessment, social phobia patients were afraid of being ridiculous. This anxiety might have led them to eliminate behaviours that could be judged negatively. However, it is surprising that our analysis failed to reveal any correlation between VFE score and level of anxiety assessed by the LSAS in social phobia group. This lack of significant effect can be explained by the fact that the LSAS does not take into account safety behaviours (e.g., avoidance of eye contact) that allow patients to be reassured when they are in a difficult situation. By comparison, our analysis failed to reveal significant differences between schizophrenia patients and healthy controls on the VFE. This result is not consistent with past research, which has shown that schizophrenia patients exhibited difficulties to produce VFE (Trémeau et al., 2005). However, Trémeau et al. (2005) assessed the production of VFE using the Facial Action Coding System with a measurement that may be more accurate than the MASS. On the other hand, we cannot compare our data with those of Trémeau et al. (2008) since the authors presented only a global score of expressive behaviour deficits and not the results found for the different subscales of the MASS. However, our and Trémeau's expressive behaviour scores were qualitatively equivalent (our study: M¼ 10.66, S.D. ¼2.08 and Trémeau's study: M¼ 10.10, S.D.¼ 3.4). This suggests that the groups in both experiments were equivalent in expressivity. We thus speculate that Trémeau et al. (2008) might have also found

Please cite this article as: Del-Monte, J., et al., Nonverbal expressive behaviour in schizophrenia and social phobia. Psychiatry Research (2013), http://dx.doi.org/10.1016/j.psychres.2013.05.034i

6

J. Del-Monte et al. / Psychiatry Research ∎ (∎∎∎∎) ∎∎∎–∎∎∎

that schizophrenia patients had a normal score in voluntary facial expression. This result, i.e., that VFE is preserved in schizophrenia and impaired in social phobia, corresponds to the third main difference in expressive behaviour between the two disorders. In sum, both schizophrenia and social phobia patients exhibited expressive behaviour deficits compared to healthy controls. However, our results showed that social interaction deficits in these disorders could be differentiated on the basis of specific subdeficits. On the one hand, schizophrenia patients have a spontaneous gestures deficit but preserved voluntary facial expression while, social phobia patients have a voluntary facial expression deficit but preserved spontaneous gestures. It is important to note that our study controlled for potential confounding variables such as depression (Trémeau et al., 2005) that could have otherwise explained the nonverbal expressive behaviour abnormalities in schizophrenia patients. The lack of association between medication, extrapyramidal symptoms and the expressive behaviour deficit provides supplementary support to the hypothesis that expressive behaviour deficits are specific and directly related to schizophrenic disorder. From a more methodological point of view, we have assessed social behaviours such as spontaneous hand gestures, spontaneous smiles, speech flow and voluntary facial expressions as evaluated with the Motor Affective subscale of the MASS. The scale is an accurate and easy to use clinical tool. The scale, however, is limited by its item quantification on a Likert scale of 0–4 and does not take into account other nonverbal body movements such as spontaneous head movements. Recently, Ramseyer and Tschacher (2006) developed a Motion Energy Analysis tool (MEA), which was specifically dedicated to quantify spontaneous movements during a recorded interview. Kupper et al. (2010) have used the MEA method to assess body movements during social interactions of those with schizophrenia. Results showed that patients have a decrease in body movements compared to healthy controls. They also showed that body movements were correlated with negative symptoms assessed by the PANSS. On the other hand, spontaneous head nods were correlated with positive symptoms such as symptoms of suspiciousness. These studies showed that body movement deficits seem more reflected in social functioning dimensions rather than only in the negative symptoms of schizophrenia. Body movement assessment seems to open new perspectives in the understanding of mental illness and future research should take into account research on expressive behaviour deficits in mental disorders to emphasize specific social motor markers in these disorders. The detection of specific markers will allow one to develop new group therapy methods with the aim of limiting the number of relapses and improve the quality of life for patients. The present study possesses several limitations. First, as mentioned above, the Motor Affective subscale of the MASS is limited by its item quantification on a Likert scale of 0–4, which limits the tool's sensibility, and by the assessment of voluntary facial expression, which is quantified by only one item. A tool more sensitive, such as the Motion Energy Analysis tool (MEA), could enable more accurate assessment of the global expressive behaviours. A second limitation of the current study is that the MASS has not been validated for the social phobia. However, it is important to note that among the 21 social phobia participants, none refused to participate until the end of the experiment. A study exploring the validity and reliability of the MASS for social phobics is needed. A third limitation is that raters were not blind to the diagnosis of the participants. Nevertheless it must be noted that our study was exploratory without an inital hypothesis that could have biased our result. A fourth limitation is the possibility that social isolation and verbal fluency impairments may to some extent explain the results of the schizophrenia patients. In future

studies, we will take into account these two variables when assessing social behaviour abilities in schizophrenia patients. Finally, the modified prosocial subscale of the PANSS includes item such as “Difficulty in abstract thinking” which is not commonly considered as reflecting social functioning. A scale more sensitive and specific such as Personal and Social Performance Scale (Morosini et al., 2000) should be used instead. In conclusion, our results have shown that the nonverbal expressive is a complex phenomenon. Two disorders with social interaction deficits lead to different and sometimes opposite behavioural sub-deficits. These results have several implications such as the need to systematize the assessment of expressive behaviour to facilitate the diagnosis in mental disorders with social interaction deficits. Our results also demonstrate the necessity of taking into account the motor dimensions of the DSM-V diagnostic categories. Moreover, we highlight the necessity to create a simple and easy to use clinical tool for more complete and accurate assessments of nonverbal expressiveness in mental disorders.

Role of funding source This study was supported by an Agence Nationale de la Recherche grant (Project SCAD # ANR-09-BLAN-0405-03).

References American Psychiatry Association. MINI DSM-IV-TR, 2004. Critères diagnostiques. Masson, Paris. Baran, X., Docherty, J., May 3–8, 2008. The A-effect of aripiprazole. Presented at the American Psychiatric Association meeting. Washington. Beck, A.T., Steer, R.A., Ball, R., Ranieri, W., 1996. Comparaison of Beck Depression Inventory-IA and II in psychiatric outpatient. Journal of Personality Assessment 67, 588–597. Bersani, G., Bersani, F.S., Valeriani, G., Robiony, M., Anastasia, A., Colletti, C., Liberati, D., Capra, E., Quartini, A., Polli, E., 2012. Comparison of social expression in patients with obsessive-compulsive disorder and schizophrenia using the Facial Action Coding System: a preliminary study. Neuropsychiatric Disease and Treatment 8, 537–547. Bourke, C., Porter, R.J., Carter, J.D., McIntosh, V.V., Jordan, J., Bell, C., Carter, F., Colhoun, H., Joyce, P.R., 2012. Comparison of neuropsychological functioning and emotional processing in major depression and social anxiety disorder subjects, and matched healthy controls. The Australian and New Zealand Journal of Psychiatry 46 (10), 972–981. Brickenkamp, R., 1994. Test d2 Aufmerksamkeits-Belastungs-Test. Handanweisung. 8., erweiterte und neu gestaltete Auflage. Hogrefe. Brüne, M., Abdel-Hamid, M., Sonntag, C., Lehmkämper, C., Langdon, R., 2009. Linking social cognition with social interaction: non-verbal expressivity, social compentence an “mentalising” in patients with schizophrenia spectrum disorders. Behavioral and Brain Fuctions 5, 6. Clark, D.M., Wells, A., 1995. A Cognitive Model of Social Phobia: Diagnosis, Assessment, and Treatment. Guilford Press, New York. Ekman, P., Friesen, W., 1969. The repertoire of nonverbal behavior. Categories, origins, usage, and coding. Semiotica 1, 49–98. Goldin-Meadow, S., 1999. The role of gesture in communication and thinking. Trends in Cognitive Sciences 3, 419–429. Green, M.F., Penn, D.L., Bentall, R., Carpenter, W.T., Gaebel, W., Gur, R.C., Kring, A.M., Park, S., Silverstein, S.M., Heinssen, R., 2008. Social cognition in schizophrenia: an nimh workshop on definitions, assessment, and research opportunities. Schizophrenia Bulletin 34, 1211–1220. Henry, J.D., Green, M.J., de Lucia, A., Restuccia, C., McDonald, S., O’Donnell, M., 2007. Emotion dysregulation in schizophrenia: reduced amplification of emotional expression is associated with emotional blunting. Schizophrenia Research 95, 197–204. Kay, S.R., Fiszbein, A., Opler, L.A., 1987. The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophrenia Bulletin 13, 261–276. Krauss, R.M., Chen, Y., Chawla, P., 1996. Nonverbal behavior and nonverbal communication: what do conversational hand gestures tell us?. In: Zanna, M. (Ed.), Advances in Experimental Social Psychology. Academic Press, San Diego, CA, pp. 389–450. Kupper, Z., Ramseyer, F., Hoffmann, H., Kalbermatten, S., Tschacher, W., 2010. Video-based quantification of bady movement during social interaction indicates the severity of negative symptoms in patients with schizophrenia. Schizophrenia Research 121, 90–100.

Please cite this article as: Del-Monte, J., et al., Nonverbal expressive behaviour in schizophrenia and social phobia. Psychiatry Research (2013), http://dx.doi.org/10.1016/j.psychres.2013.05.034i

J. Del-Monte et al. / Psychiatry Research ∎ (∎∎∎∎) ∎∎∎–∎∎∎ Lavelle, M., Healey, P.G., McCabe, R., 2012. Is nonverbal communication disrupted in interaction involving patients with schizophrenia. Schizophrenia Bulletin, http://dx.doi.org/10.1093/schbul/sbs091. Liebowitz, M.R., 1987. Social phobia. Modern Problems of Pharmacopsychiatry 22, 141–173. Mackinnon, A., Mulligan, R., 2005. [The estimation of premorbid intelligence levels in French speakers]. Encephale 31, 31–43. Melfsen, S., Osterlow, J., Florin, I., 2000. Deliberate emotional expressions of socially anxious children and their mothers. Journal of Anxiety Disorders 14, 249–261. Mittal, V.A., Jalbrzikowski, M., Daley, M., Roman, C., Bearden, C.E., Cannon, T.D., 2011. Abnormal movements are associated with poor psychosocial functioning in adolescents at high risk for psychosis. Schizophrenia Research 130, 164–169. Mohan, A., Singh, A.P., Mandal, M.K., 2001. Transfer and interference of motor skills in people with intellectual disability. Journal of Intellectual Disability Research 45 (Pt4), 361–369. Morosini, P.L., Magliano, L., Brambilla, L., Ugolini, S., Pioli, R., 2000. Development, reliability and acceptability of a new version of the DSM-IV Social and Occupational Functioning Assessment Scale (SOFAS) to assess routine social functioning. Acta Psychiatrica Scandinavica 1001, 323–329. Moukheiber, A., Rautureau, G., Perez-Diaz, F., Soussignan, R., Dubal, S., Jouvent, R., Pelissolo, A., 2010. Gaze avoidance in social phobia: objective measure and correlates. Behaviour Research and Therapy 48, 147–151. Panayiotou, G., Karekla, M., 2012. Perceived social support helps, but does not buffer the negative impact of anxiety disorders on quality of life and perceived stress. Social Psychiatry and Psychiatric Epidemiology 48 (2), 283. Phillips, L.K., Seidman, L.J., 2008. Emotion processing in persons at risk for schizophrenia. Schizophrenia Bulletin 34, 888–903. Ramseyer, F., Tschacher, W., 2006. Synchrony: a core concept for a constructivism approach to psychotherapy. Constructivism in the Human Sciences 11 (1–2), 150–171. Schneier, F.R., Rodebaugh, T.L., Blanco, C., Lewin, H., Liebowitz, M.R., 2011. Fear and avoidance of eye contact in social anxiety disorder. Comprehensive Psychiatry 52, 81–87.

7

Schmidt, R.C., Richardson, M.J., 2008. Dynamics of interpersonal coordination. In: Fuchs, A, Jirsa, V (Eds.), Coordination: Neural, Behavioral and Social Dynamics. Springer-Verlag, Heidelberg, pp. 281–308. Sheehan, D.V., Lecrubier, Y., Sheehan, K.H., Amorim, P., Janavs, J., Weiller, E., Hergueta, T., Baker, R., Dunbar, G.C., 1998. The Mini International Neuropsychiatric Intervie (M.I.N.I.): the development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. Journal of Clinical Psychiatry 59 (Suppl. 20), 22–33, quiz 34–57. Review. Sidlova, M., Prasko, J., Jelenova, D., Kovacsova, A., Latalova, K., Sigmundova, Z., Vrbova, K., 2011. The quality of life of patients suffering from schizophrenia– a comparaison with healthy controls. Biomedical papers of the Medical Faculty of the University Palacký, Olomouc, Czechoslovakia 155, 173–180. Simpson, G.M., Angus, J.W., 1970. A rating scale for extrapyramidal side effects. Acta Psychiatrica Scandinavica Supplementum 212, 11–19. Smits-Engelsman, B., Hill, E.L., 2012. The relationship between motor coordination and intelligence across the IQ range. Pediatrics 130 (4), e950–e956. Steimer-Krause, E., Krause, R., Wagner, G., 1990. Interaction regulations used by schizophrenic and psychosomatic patients: studies facial behavior in dyadic interactions. Psychiatry 53, 209–228. Stopa, L., Clark, D.M., 1993. Cognitive processes in social phobia. Behaviour Research and Therapy 31, 255–267. Tibi-Elhanany, Y., Shamay-Tsoory, S.G., 2011. Social cognition in social anxiety: first evidence for increased empathic abilities. The Israel Journal of Psychiatry and Related Sciences 48, 98–106. Trémeau, F., Goggin, M., Antonius, D., Czobor, P., Hill, V., Citrome, L., 2008. A new rating scale for negative symptoms: the Motor-Affective-Social Scale. Psychiatry Research 160, 346–355. Trémeau, F., Malaspina, D., Duval, F., Corrêa, H., Hager-Budny, M., Coin-Bariou, L., Macher, J.P., Gorman, J.M., 2005. Facial expressiveness in patients with schizophrenia compared to depressed patients and nonpatient comparison subjects. The American Journal of Psychiatry 162, 92–101. Vialatte, F.B., Cichoki, A., 2008. Slipt-test bonferroni correction for qeeg statistical maps. Biological Cybernetics 98, 295–303. Wechsler, D., 1999. Wechsler Abbreviated Scale of Intelligence (WASI). TX: Harcourt Assessment, San Antonio.

Please cite this article as: Del-Monte, J., et al., Nonverbal expressive behaviour in schizophrenia and social phobia. Psychiatry Research (2013), http://dx.doi.org/10.1016/j.psychres.2013.05.034i