Social cognition impairments in Asperger syndrome and schizophrenia

Schizophrenia Research 143 (2013) 277–284

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Social cognition impairments in Asperger syndrome and schizophrenia Tove Lugnegård a, b,⁎, Maria Unenge Hallerbäck a, c, Fredrik Hjärthag d, Christopher Gillberg a a

Gillberg Neuropsychiatry Centre, Sahlgrenska Academy, University of Gothenburg, Gothenburg, Sweden Department of Adult Habilitation, Central Hospital, Karlstad, Sweden c Department of Child and Adolescent Psychiatry, Central Hospital, Karlstad, Sweden d Department of Psychology, Karlstad University, Karlstad, Sweden b

a r t i c l e

i n f o

Article history: Received 12 October 2011 Received in revised form 28 November 2012 Accepted 1 December 2012 Available online 23 December 2012 Keywords: Social cognition Theory of mind Asperger syndrome Schizophrenia

a b s t r a c t Social cognition impairments are well described in both autism spectrum disorders, including Asperger syndrome (AS), and in schizophrenia spectrum disorders. However, little is known about whether there are differences between the two groups of disorders regarding this ability. The aim of this study was to compare social cognition abilities in AS and schizophrenia. Fifty-three individuals (26 men, 27 women) with a clinical diagnosis of AS, 36 (22 men, 14 women) with a clinical diagnosis of schizophrenic psychosis, and 50 non-clinical controls (19 men, 31 women) participated in the study. Clinical diagnoses were confirmed either by Structured Clinical Interview on DSM-IV diagnosis or the Diagnostic Interview for Social and Communication Disorders. Verbal ability was assessed using the Vocabulary subtest of the WAIS-III. Two social cognition instruments were used: Reading the Mind in the Eyes Test (Eyes Test) and the Animations Task. On the Eyes Test, patients with schizophrenia showed poorer results compared to non-clinical controls; however, no other group differences were seen. Both clinical groups scored significantly lower than the comparison group on the Animations Task. The AS group performed somewhat better than the schizophrenia group. Some differences were accounted for by gender effects. Implicit social cognition impairments appear to be at least as severe in schizophrenia as they are in AS. Possible gender differences have to be taken into account in future research on this topic. © 2012 Elsevier B.V. All rights reserved.

1. Introduction Autism spectrum disorders (ASDs) and schizophrenia are separate syndromes in terms of defining symptom criteria, age of onset, and course. However, both syndromes are of neurodevelopmental origin (Fatemi and Folsom, 2009; Coleman and Gillberg, 2011), have a genetic basis which partly overlaps (McCarthy et al., 2009; Craddock and Owen, 2010; Owen et al., 2011), and show marked impairments in the area of social cognition (Abdi and Sharma, 2004). Although related to neurocognition, social cognition is considered a separate cognitive domain (Sergi et al., 2007; Pickup, 2008). Social cognition can be defined as “the mental operations underlying social interactions, which include the human ability to perceive the intentions and dispositions of others and the cognitive processes that subserve behaviour in response to others” (Brothers, 1990). It is a central human cognitive ability, essential for understanding social information (Frith and Frith, 2007). Social cognition is an umbrella term including functions such as theory of mind, attributional style, and social perception. Theory of mind (ToM) is a social cognitive faculty that involves the ability to attribute independent mental states to oneself and others in order to explain and predict behaviour. Attributional style is described as an individual's characteristic ⁎ Corresponding author at: Department of Adult Habilitation, Drottninggatan 27, 652 25 Karlstad, Sweden. Tel.: +46 54614090; fax: +46 54154599. E-mail address: [email protected] (T. Lugnegård). 0920-9964/$ – see front matter © 2012 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.schres.2012.12.001

way of explaining events (Pinkham et al., 2003; Penn et al., 2008). Social perception comprises abilities crucial for social cognition such as emotion perception, including facial affect recognition, and social cue recognition. Impairment in social cognition is among the core features of ASDs. ASDs, classified as pervasive developmental disorders (PDD) in the DSM-IV-TR (APA, 2000), are relatively common social communication disorders that affect approximately 0.6–1.6% of the general population (Baird et al., 2006; Fernell and Gillberg, 2010). ASDs share a core triad of characteristics: 1) qualitative impairments in reciprocal social interactions, 2) qualitative impairments in verbal and non-verbal communication, and 3) restricted social imagination with repetitive and stereotyped patterns of interests and behaviour. The DSM-IV includes autistic disorder (AD) (pervasive deficits in all three domains), Asperger syndrome (AS) (pervasive deficits in social interaction and behaviours in the presence of superficially normal expressive verbal development) and pervasive developmental disorder not otherwise specified (PDD-NOS) (not meeting full criteria for either AD or AS, but with pervasive deficit in social interaction) (APA, 2000). Extensive research on different aspects of social cognition disabilities in ASD, in particular ToM and social perception, has shown predominantly reduced performance (Klin, 2000; Tager-Flusberg, 2007; Pisula, 2010), even though some recent studies question this assumption (Wright et al., 2008; Williams and Happe, 2010), and the real life impairments can be difficult to fully capture in experimental tasks.

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During the last decade, there has been an increasing focus on social cognitive deficits also in schizophrenia and closely related disorders. Numerous studies have shown that people with schizophrenia perform poorly on tests of social cognition (Couture et al., 2006; Sprong et al., 2007; Green et al., 2008). Moreover, it has been shown that social cognitive impairment is a major factor contributing to low functional outcome among patients with schizophrenia (Bell et al., 2009; Couture et al., 2011; Fett et al., 2011). Although social cognition is currently of great research interest in both ASD and schizophrenia, only a few prior studies have made direct comparisons between the two conditions. One recent study comparing ToM in the two disorders, demonstrated worse performance in individuals with AS (Ozguven et al., 2010). However, in this study, schizophrenia patients with a high level of negative symptoms showed as marked ToM impairments as the AS group. A few small-scale studies on adults have revealed no differences between schizophrenia and “high-functioning” ASD on social cognition tasks (Craig et al., 2004; Murphy, 2006; Couture et al., 2010). One study on children showed poor ToM abilities in both ASD and schizophrenia (Pilowsky et al., 2000). In contrast, in a study on facial affect recognition in children and young adults, those with ASD performed significantly worse than those with schizophrenia (Bolte and Poustka, 2003). A small comparative study indicated a shared abnormality between the two disorders in utilising facial information (Sasson et al., 2007). Neural activation during social cognitive demands was compared in an fMRI study, showing a similar pattern between ASD and paranoid schizophrenia, but not between ASD and nonparanoid schizophrenia (Pinkham et al., 2008). None of the comparative studies have taken potential gender effects into account. The aim of the present study was to compare social cognition abilities in adults with AS and adults with schizophrenia, comparing the results of these groups to those of an age matched non-clinical group. Our purpose was to include both men and women, so as to allow analysis of possible gender influences on the results obtained. Our intention was to select instruments assessing different components of social cognition, and with low demands on verbal memory. In order to control for the possible influence of verbal ability on the results, such a measure was included. Although numerous instruments have been developed, there is no consensus on the assessment of the different components of social cognition. Traditional ToM measures, usually consisting of social vignettes followed by questions, rely heavily on verbal memory, which may, especially in patients with schizophrenia, influence results. In addition, standard ToM tasks based on social stories do not capture “on-line” spontaneous ToM as it occurs in daily life (Klin, 2000; Frith, 2004). We sought to address these concerns by using the Animations Task, which is designed to assess implicit aspects of ToM, without requiring high demands on verbal memory. The task was originally developed for ASD research (Abell et al., 2000; Castelli et al., 2000, 2002), but has also been applied in studies on schizophrenia in its original version (Russell et al., 2006; Horan et al., 2009; Koelkebeck et al., 2010), as well as in a modified adaptation (Bell et al., 2010). In order to add a complementary task on social perception, a facial affect recognition task, the Reading the Mind in the Eyes Test (Baron-Cohen et al., 2001a), was included. Originally, the instrument was described as an advanced ToM measure, sensitive to “mind reading” ability in adults with normal intelligence. However, according to the general definitions of social cognition concepts, we consider it a measure of facial affect recognition (social perception) rather than a measure of ToM. 2. Method 2.1. Participants A total of 139 individuals with clinical diagnoses of either AS (n=53) or schizophrenic psychosis (n =36) or no known neurodevelopmental/ neuropsychiatric clinical diagnosis (n =50) were included in the study.

Demographic characteristics for the three study groups are presented in Table 1. The recruitment procedures for the two clinical groups have been described in detail in two previous papers (Lugnegård et al., 2011; Unenge Hallerbäck, 2012). All participants provided informed consent and were seen personally in an outpatient setting. The study was approved by the Medical Ethical Review Board at Uppsala. 2.1.1. Asperger syndrome group (AS) The 53 individuals (26 males, 27 females) with a clinical diagnosis of AS were recruited from two different outpatient clinics in Värmland, providing services for people with neurodevelopmental/neuropsychiatric disorders including AS and other ASDs. Clinical diagnoses had originally been assessed by psychiatrists and/or psychologists working in neurodevelopmental assessment teams, and diagnoses were based on DSM criteria. For the majority of participants (45 out of 53), an assessment with the Eleventh version of the Diagnostic Interview for Social and Communication Disorders (DISCO-11) (Wing et al., 2002) with a parent was performed within the present study. The diagnosis of AS was confirmed in all of the 45 DISCO-11-assessed cases. However, 20 of these 45 had some (n = 12) or considerable (n = 8) symptoms before age 3 years, and were discussed for a diagnosis of AD. However, given that symptom criteria for AS were met in all cases, the clinical AS diagnosis was also considered to be confirmed in these cases. None of the DISCO-11-assessed cases fulfilled criteria of PDD-NOS, and individuals with an original clinical diagnosis of PDD-NOS were never included in the study. Originally, 54 individuals were included; however, assessment results essential for this study were not available for one participant. Clinical characteristics of the AS group are shown in Table 2. 2.1.2. Schizophrenic psychosis group (SCH) The 36 individuals (22 males, 14 females) with a clinical diagnosis of schizophrenic psychosis (schizophrenia, schizoaffective disorder or schizophreniform disorder) were recruited from the only psychiatric outpatient clinic in the county of Värmland (n =33) or one of the psychiatric outpatient clinics in Gothenburg (n =3). By administering the Structured Clinical Interview for DSM-IV diagnosis (SCID-I) (First and Gibbon, 2004), a diagnosis of schizophrenic psychosis was confirmed in 31 of the 36 patients. Five patients met criteria for Psychotic disorder Not Otherwise Specified instead; all five of these had a history of several, schizophrenia-like psychotic episodes requiring inpatient treatment; however, a distinction between schizoaffective disorder and schizophrenia was not possible due to uncertain information on mood symptoms, neither was a distinction between schizophrenia and schizophreniform disorder possible due to uncertain information on the duration of episodes. Due to the SCID-I-based symptom information, and due to their original clinical diagnosis, these five patients with psychotic disorder NOS were still retained for participation in the study. Clinical characteristics of the SCH group are shown in Table 3. Originally, 46 patients with a clinical diagnosis of schizophrenic psychosis had been included in the study. However, for two patients no psychotic disorder could be confirmed by the SCID-I, two other patients were instead shown to have bipolar I disorder, one patient had only substance-induced psychotic disorder, and for five individuals the social cognition measures were not possible to assess due to participation withdrawal from this part of the study. Table 1 Demographic and clinical characteristics of all participants. Characteristic

SCH n = 36

AS n = 53

NCC n = 50

Statistics

p

Mean age, years (s.d) Male:female Mean WAIS Vocabulary, scaled scorea (s.d.)

28.8 (4.1) 22: 14 9.4 (2.2)

27.3 (4.1) 26: 27 10.4 (2.3)

28.8 (9.3) 19: 31 9.9 (2.1)

F= 0.934 x2 = 4.503 F= 2.176

.396 .105 .118

a

Data missing for four SCH and four AS participants.

T. Lugnegård et al. / Schizophrenia Research 143 (2013) 277–284 Table 2 Medication of the 53 participants with AS. Men (n = 26)

Current medication type No medication Antipsychotics Antidepressants Mood stabilisers a

Women (n = 27)

n

%

n

%

15 2 7 0

58 8 27 0

14 1 10 1

52 4 37 4

a

Several participants have more than one medication type.

2.1.3. Non-clinical comparison group (NCC) The 50 individuals in the non-clinical comparison group (19 males, 31 females) were recruited from students at Karlstad University, studying on different programmes. Participants in the NCC group were evaluated with a short questionnaire including educational data and data on occurrence of ASD, ADHD or psychosis. No participant in the NCC group had a reported history of any of these diagnoses. 2.2. Measurements 2.2.1. Animations Task The Animations Task by Frith, Castelli and Happé consists of 12 (3× 4) computer-presented animations, lasting 34–45 s each, where a big red triangle and a small blue triangle move around the screen (Abell et al., 2000; Castelli et al., 2000). There are three types of animations: random movements, goal-directed movements (GD) and animations where the triangles are moving as if they know what the other triangle is thinking or feeling (Theory of Mind, ToM). The participants were informed that they would be shown a series of animations and that they would be asked to provide a description of how they perceived the movements after each animation. Three practice animations were shown to begin with, in order to familiarise the participant with the task. The 12 animations were then presented in a mixed order. After each animation, the participant was given the neutral question “What was happening in this animation?” On no occasion was feedback given on the content of the responses, but participants were generally praised for their descriptions. Responses were recorded, transcribed and later scored according to a scoring manual. Scoring procedure was based on work by Castelli et al. (2002). Each description was rated according to 1) Appropriateness and to 2) Intentionality. The Appropriateness score range is 0–3 for each animation (there are four animations of each of the three types (random, GD and ToM), so the maximum total score is 12 for each type of animation) according to how accurately the description captures the events in the animation, as intended by the underlying script: 0 = no answer or “I don't know”;

Table 3 Characteristics and medication of the 36 participants with SCH. Characteristic

Men (n = 22)

Age (years) Age at onset of psychosis (years) Duration of psychosis (years)

Current medication type No medication Antipsychotics Antidepressants Mood stabilisers a

Women (n = 14)

Mean

s.d.

Mean

s.d.

28.8 21.5 7.3

4.2 3.6 4.8

28.9 22.9 6.1

4.7 4.8 4.3

n

%

n

%

1 21 8 4

5 95 36 18

4 9 3 3

29 64 21 21

a

Several participants have more than one medication type.

279

1 = inappropriate answer with reference to the wrong type of interaction between the triangles or focuses only on a minor aspect of the animation; 2 = partial description of the sequence, description is related to the sequence but imprecise or incomplete; 3 = a spot-on description of the story of the actions presented. The Intentionality score range is 0–5 for each animation (maximum total score 20 for each of the three types (random, GD and ToM) of animation) and reflects the degree to which the participant describes complex, intentional mental states. On this score the verbs of the narrative are in focus. The verbs are rated independently of whether they correctly match the underlying script: 0= non-deliberate action (e.g. “bouncing off,” “moving around”); 1 =deliberate solitary action (e.g. “swimming,” “ice-skating”); 2= deliberate action with somebody else (e.g. “dancing,” “following”); 3= deliberate action in response to others actions (e.g. “the big one is preventing the little one to get out”); 4 =deliberate action with reference to mental states (e.g. “being happy,” “they are arguing”); 5 =deliberate action with explicit goal of effecting other's mental state (e.g. “surprising,” “persuading” or “teasing”). Thus, a particular description can be rated low on Intentionality and high on Appropriateness and vice versa. The scoring procedure was blinded: no personal data on participants were included in the transcripts, and group affiliation could not be revealed in any other way.

2.2.2. Reading the Mind in the Eyes Test A Swedish version of the Reading the Mind in the Eyes Test (Eyes Test) was used. It is a translation and abbreviation of the Baron-Cohen child version (Baron-Cohen et al., 2001b) consisting of 24 black and white photographs of the eye region illustrating complex mental states. The participant is asked to choose which of four words best describes what the person in the photograph is feeling or thinking. Responses are scored 1 or 0 for correctness, meaning that the maximum score on the Swedish version of the Eyes Test is 24. This abbreviated Swedish version (available from the authors on request) has previously been tested on 158 students, and the test–retest reliability has been examined, showing limits of agreement (Bland-Altman plot) of ±4 points (Hallerbäck et al., 2009).

2.2.3. WAIS-III Vocabulary subtest Verbal intellectual performance, as measured by the Vocabulary subtest of the Swedish version of the Wechsler Adult Intelligence Scale, Third Edition, (WAIS-III) (Wechsler, 1997), was examined in all participants, apart from four individuals in the SCH group and four in the AS group.

2.3. Statistical analysis Group differences in demographic characteristics were analysed using ANOVA and chi-square analysis. Scores on the Animations task and the Eyes Test are (1) not continuous variables, but on an ordinal level and (2) could not be assumed to be normally distributed; therefore, non-parametric statistical tests were used. Kruskal–Wallis tests were first performed as an omnibus test on overall group differences. For post-hoc between-group comparisons the Mann–Whitney U-test was applied. The significance level was set at 0.05. Holm–Bonferroni correction for multiple comparisons (Holm, 1979; Pett, 1997) was performed on the Kruskal–Wallis tests on the Animations Task (6 in total), as well as for the post hoc Mann–Whitney U-tests. Associations between social cognition measures and verbal ability were evaluated with Spearman's correlation coefficients. In order to explore gender differences, two additional analyses were performed: (1) Kruskal–Wallis tests followed by Mann–Whitney U-tests on men and women separately and, regardless of data level, (2) a complementary two-way ANOVA with diagnostic group and sex set as factors.

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3. Results

3.4. Correlations between social cognition tasks and verbal ability

3.1. Demographics

ToM Appropriateness scores as well as ToM Intentionality scores correlated weakly with the WAIS-III Vocabulary test (r = .20, p = .02 for both measures). Similarly, for the Eyes Test, a weak correlation (r = .20, p = .019) with WAIS-III Vocabulary test was seen.

The three groups did not differ in terms of age, gender distribution or verbal ability (Table 1). 3.2. Animations Task

3.5. Gender differences

Mean scores and statistical analyses on the Animations Task and on the Eyes Test for the total study group are shown in Table 4. 3.2.1. Random animations Appropriateness scores and Random animations Intentionality scores For the Random animations, there were no group differences either on Appropriateness score or on Intentionality score. 3.2.2. GD animations Appropriateness scores and GD animations Intentionality scores For the GD animations, there were no group differences either on Appropriateness score or on Intentionality score. 3.2.3. ToM animations Appropriateness scores The distributions of ToM Appropriateness scores for the three groups are presented in Fig. 1. There was a significant difference between groups, H(2) = 33.6, p b .001. Post hoc tests showed that the SCH group had lower scores than the AS group, U= 537, p = .002, which, in turn, had lower scores than the NCC group, U = 899, p = .008. 3.2.4. ToM animations Intentionality scores Intentionality score (0–5 for each animation) is a measure of verbs used by the participant: the more advanced interaction described, the higher score. There was a significant group difference, H(2) = 26.6, p b .001. Post hoc analysis showed that the SCH group had lower scores compared to the AS group, U = 565, p = .003, which, in turn, had lower scores than the NCC group, U = 1001, p = .028. (Fig. 2) 3.3. Eyes Test The distributions of Eyes Test scores are shown in Fig. 3. The overall Kruskal–Wallis test revealed a significant group difference, H(2) = 7. 9, p = .019. Post hoc tests showed a significant difference between the SCH group and the NCC group, U= 592, p = .02, although no other comparisons were significant.

3.5.1. Non-parametric statistical analyses for men and women separately Additional analyses (Kruskal–Wallis tests and follow-up Mann Whitney U tests) were performed on men and women separately, again with diagnostic group as the grouping variable (see Tables 5 and 6.) For Random animations and GD animations (Appropriateness scores and Intentionality scores), no differences between the three groups were seen. There were significant differences between diagnostic groups for both men and women on ToM animations. Among men, there was a significant overall group difference (H(2) = 14.8, p = .007) on ToM Appropriateness score. Post hoc tests showed that the NCC male group showed significantly higher scores than both the AS male group and the SCH male group (NCC vs. AS, U =132, p =.03; NCC vs. SCH, U= 71, p = .002) but there was no difference between the AS male group and the SCH male group, U = 208, p =.103. On ToM Intentionality score for men, there was similarly a significant overall group difference, H(2) = 12.5, p = .012. Post hoc tests showed that both the AS male group and NCC male group scored higher than the SCH male group (AS vs. SCH, U = 165, p = .04; NCC vs. SCH, U =82, p = .005), but no difference was seen between the AS male group and the NCC male group, U = 193, p = .211. Among women, there was a significant overall group difference on ToM Appropriateness score, H(2) = 22.1, p b .001. Post hoc tests showed that both the AS female group and the NCC female group scored significantly higher than the SCH female group (AS vs. SCH, U = 64, p = .004; NCC vs. SCH, U= 28, p = .002), but there was no difference between the AS female group and the NCC female group, U = 333, p = .180. With regard to ToM Intentionality scores, there was a significant overall group difference among women, H(2) =13.1, p = .006. Post hoc analyses revealed that the NCC female group showed significantly higher scores than the SCH female group, U = 73, p = .002, and no other group differences were significant (AS vs. SCH, U= 112, p = .102; AS vs. NCC, U= 303, p = .138). For the Eyes Test, there were no significant group differences among men, H(2) = 0.868, p = .648. Among women, there was a significant overall group difference, H(2) = 7.1, p = .029. Post hoc analysis revealed that the NCC female group scored higher than the SCH female group, U =118, p = .045, but no other significant group differences were seen.

Table 4 Mean scores on Animations task and Eyes Test. SCH (n = 36)

AS (n = 53)

NCC (n = 50)

Statistical analysis Overallb

Eyes Test (0–24) Animations task Random App (0–12) Random Int (0–20) GD App (0–12) GD Int (0–20) ToM App (0–12) ToM Int (0–20)

SCH vs. ASc

SCH vs. NCCc

NCC vs. ASc

Meana

SD

Meana

SD

Meana

SD

H(2)

p

U

pd

U

pd

U

pd

17.2

3.2

18.2

2.5

18.9

2.4

10.1 3.1 8.8 9.4 6.4 11.4

2.5 3.2 2.1 2.7 2.1 4.4

10.8 3.1 9.8 9.5 8.1 14.1

1.6 3.4 2.1 2.3 2.2 3.9

10.6 2.9 10.0 10.8 9.4 15.9

1.6 3.9 1.7 2.3 1.7 2.5

7.9 H(2) 0.9 0.8 7.3 8.3 33.6 26.6

.019 pd NS NS NS NS b.001 b.001

779 U – – – – 537 578

NS pd – – – – .002 .003

592 U – – – – 260 324

.02 pd – – – – b.001 b.001

1082 U – – – – 899 1001

NS pd – – – – .008 .028

NS = not significant. a Although data are on ordinal level, mean and SD are reported to facilitate comparison with previous studies. b Kruskal–Wallis test for overall group differences. c Post hoc Mann–Whitney U test. d Holm–Bonferroni corrected for multiple comparisons.

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Fig. 1. Distribution of scores on Appropriateness in the 4 Theory of Mind Animations (maximum total score=12).

3.5.2. Supplementary two-way ANOVA Although scores on Animations Task and Eyes Test are on an ordinal level and non-parametric statistics are recommended, an exploratory two-way ANOVA with diagnostic group and sex as the two factors was performed. For the Eyes Test, there was a significant effect of group (F = 3.25, df= 2, p = .042); however no effect of sex (F = 1.89, df= 1, p =.172) or sex × group interaction were seen (F = 1.68, df= 2, p = .191). For ToM Appropriateness Score there was a significant effect of group (F = 24.42, df= 2, p b .001); however no effect of sex (F = 0.838, df= 1, p = .362) or sex× group interaction were seen (F = 1.27, df= 2, p = .284). The same pattern was seen for ToM Intentionality Score: a significant effect of group (F = 14.95, df= 2, p b .001); however no effect of sex (F = 0.061, df= 1, p = .806) or sex × group interaction were seen (F = 0.173, df=2, p = .841). 4. Discussion In this study, individuals with schizophrenic psychoses showed at least as marked impairments in social cognition as individuals with AS. Both clinical groups clearly deviated from a community sample on the ToM Appropriateness scores and on ToM Intentionality scores. To our knowledge, no previous study has used the Animations Task for comparison of ToM abilities across AS and schizophrenia. Nevertheless, our results are in accord with those of prior studies where traditional ToM

Fig. 2. Distribution of scores on Intentionality in the 4 Theory of Mind Animations (maximum total score=20).

Fig. 3. Distribution of scores on the Eyes Test (maximum total score = 24).

instruments have been used, such as the Hints task (Craig et al., 2004) or variants of false belief tasks (Murphy, 2006; Ozguven et al., 2010), also demonstrating convergence in ToM deficits across the two groups. Our findings challenge the opinion that social cognition deficits are typically more severe in ASD than in schizophrenia. Possibly, heterogeneity of symptom profiles in the schizophrenic psychosis group is one explanation, according to the results of Ozguven which have shown more pronounced social cognitive deficits in patients with negative symptoms (Ozguven et al., 2010). Furthermore, a general cognitive dysfunction, not captured by WAIS Vocabulary, may have impaired performance in the schizophrenic psychosis group. In contrast to this assumption, there was no difference between patient groups and comparison group on the “mechanical” animations (random and goal directed movements) which is in line with some previous results (Abell et al., 2000; Castelli et al., 2002; Horan et al., 2009). In two other studies, poor results on GD animations (Russell et al., 2006; Koelkebeck et al., 2010) and random animations (Russell et al., 2006) for patients with schizophrenia were reported, most likely as a consequence of general cognitive dysfunction. There were some interesting effects of gender on the Animations Task according to non-parametric statistical analyses divided by gender. Men with AS as well as men with schizophrenic psychosis showed significantly lower scores on ToM Appropriateness than non-clinical comparison men; however, the two male clinical groups did not differ from each other on this ability. In contrast, women with AS did not clearly differ from non-clinical women on ToM Appropriateness, although women with schizophrenic psychosis showed significantly poorer results than the other two groups. Gender-divided results on ToM Intentionality scores did not follow this pattern: men with schizophrenic psychosis showed lower scores than men with AS, and no significant difference between men with AS and non-clinical comparison men was seen. For women, the only significant difference on ToM Intentionality was that women with schizophrenic psychosis showed lower scores than non-clinical comparison women. Although preliminary, our findings may imply that groups differences between schizophrenic psychosis and AS are smaller in men than in women. Men with AS and men with schizophrenia appear to be fairly similar with respect to implicit social cognition while women with AS performed as well as nonclinical comparison women on both scores of ToM animations. There are several possible reasons for these findings: (1) women in the schizophrenia group had unspecifically low levels of cognition (including social cognition), (2) women in the schizophrenia group had specifically

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Table 5 Mean scores on Eyes Test and ToM animations for men. SCH (n = 22)

AS (n = 26)

NCC (n = 19)

Statistical analysis Overallb

Mean Eyes Test (0–24) Animations task ToM App (0–12) ToM Int (0–20)

a

SD

Mean

17.2

3.2

6.7 11.1

2.4 4.9

a

SD

Mean

18.1

2.4

7.9 14.3

2.3 4.0

a

SCH vs. ASc

SD

H(2)

p

U

p

17.7

2.7

0.868

NS

–

9.6 15.9

1.7 2.5

14.8 12.5

.007 .012

208 165

SCH vs. NCCc d

NCC vs. ASc U

pd

–

–

–

.002 .005

132 193

.03 NS

U

p

–

–

NS .04

71 82

d

NS = not significant. a Although data are on ordinal level, mean and SD are reported to facilitate comparison with previous studies. b Kruskal–Wallis test for overall group differences. c Post hoc Mann–Whitney U test. d Holm–Bonferroni corrected for multiple comparisons.

neurocognitive measures have not been included (Couture et al., 2008; Kettle et al., 2008). Moreover, small study samples increase the risk for random errors. To be sure, widespread within-group score heterogeneity is seen on the Eyes Test, which results in a substantial overlap between groups and small effect sizes. We have previously reported doubtful test–retest reliability for the Eyes Test (Hallerbäck et al., 2009). Such findings, and the results of the present study, suggest that the Eyes Test is not a valid “test for ASD,” and it is not helpful in differentiating ASD from schizophrenia. The question of impact of general cognitive abilities on performance on social cognitive tasks is of constant interest. Even though neurocognition and social cognition are clearly shown to be separate domains, qualities such as attention, vigilance and memory are necessary (but not sufficient) bases for social cognitive processes. Different social cognition measures differ markedly in neurocognitive demands. Furthermore, in explicit ToM tasks with a “0 or 1 response,” abstract reasoning may compensate for low functioning of implicit ToM. Neither the Animations Task nor the Eyes Test requires verbal memory or abstract reasoning. Both the Animations Task and the Eyes Test were only weakly correlated with verbal ability, indexed by WAIS-III Vocabulary, which is in line with results by Bell et al. (2010) who reported a moderate correlation between Vocabulary and a modified version of the Animations task in individuals with schizophrenia. One limitation of the present study is the small sample size, particularly when subdividing the total study group into men and women. On the other hand, many studies do not include female patients at all, maybe to facilitate statistical procedures. Another limitation may be our selection of measures, which was made in order to capture implicit, “on-line” social cognitive abilities without high demands on memory. No golden standard exists for assessing different domains of social cognition. However, with a broader battery of social cognitive instruments, clarification of further aspects could have been possible. Moreover, our study lacks a measure on social skills/social functioning which would have added ecological validity to our investigation. A structured assessment

poor social cognition, (3) women in the AS group were high functioning on general cognition which may have compensated for social cognitive deficits, (4) women with AS are similar to non-clinical women in terms of social cognition, indexed by the Animations Task. Supplementary ANOVA, performed despite data being on an ordinal level, revealed no effect of gender on the Animations task. Although our results are preliminary due to small sample sizes, it will be of importance to consider possible gender influences in future social cognition research. In contrast to the majority of reported investigations, only minor group differences were seen on the Eyes Test. There was a considerable dispersion of scores in all three groups. The only significant difference was between the schizophrenia group and the non-clinical group, which was a consequence of non-clinical women scoring significantly higher on this task. The Eyes Test has been used in several studies on ASD and schizophrenia, including in three head-to-head comparative studies. In one of these, a battery of social perception tasks was used, including the Eyes Test. Individuals with AS and individuals with schizophrenia performed worse than a non-clinical group on all tasks apart from the Eyes Test where no significant group differences were seen (Couture et al., 2010). In another study individuals with AS and schizophrenia both scored worse than healthy controls, but they did not differ from each other (Craig et al., 2004). Yet another study demonstrated no difference between AS and schizophrenia on the Eyes Test, although both groups scored worse than a comparison group with personality disorder (Murphy, 2006). Eyes Test results in patients with schizophrenia have generally been reported to be poorer compared to non-clinical groups (Kelemen et al., 2005; Bora et al., 2008; Couture et al., 2008). A number of investigators report lower scores for people with ASD compared to non-clinical controls (Baron-Cohen et al., 2001a; Dziobek et al., 2006), although a recent study could not replicate this (Spek et al., 2010). Our results may be a consequence of a ceiling effect, due to the use of the child version of the Eyes Test. Another possible explanation for diverging findings may be major differences in neurocognitive abilities between study samples, since in some of the previous studies,

Table 6 Mean scores on Eyes Test and ToM animations for women. SCH (n = 22)

AS (n = 26)

NCC (n = 19)

Statistical analysis Overallb

Mean Eyes Test (0–24) Animations task ToM App (0–12) ToM Int (0–20)

a

SD

Mean

17.1

3.3

5.8 11.8

1.4 3.7

a

SD

Mean

18.3

2.5

8.3 14.0

2.2 3.7

a

SCH vs. ASc

SD

H(2)

p

U

p

19.6

2.0

7.1

.029

146

9.2 15.9

1.7 2.6

22.1 13.1

b.001 .006

64 112

NS = not significant. a Although data are on ordinal level, mean and SD are reported to facilitate comparison with previous studies. b Kruskal–Wallis test for overall group differences. c Post hoc Mann–Whitney U test. d Holm–Bonferroni corrected for multiple comparisons.

SCH vs. NCCc d

NCC vs. ASc U

pd

.045

304

NS

.002 .002

333 303

NS NS

U

p

NS

118

.004 NS

28 73

d

T. Lugnegård et al. / Schizophrenia Research 143 (2013) 277–284

of negative symptoms would have been valuable to further evaluate possible sub-groups in the schizophrenic psychosis group. Deficits in social cognition are among the core features of ASD. These deficits are not specific to ASD. Individuals with schizophrenic psychosis may have as marked impairments, or even worse. “Within-syndrome” heterogeneity is substantial for both diagnostic domains, as well as “cross-syndrome” similarities, which result in considerable overlap. Future research on neurodevelopmental disorders, such as ASD and schizophrenia, would possibly benefit from a “cross-syndrome” approach and increased focus on endophenotypes. Furthermore, possible gender differences have to be taken into account in future research on this topic. Role of funding source This study was supported by grants from the County Council of Värmland, Sweden. The funding source had no further role in study design; in the collection, analysis and interpretation of data; in writing the report; and in the decision to submit the paper for publication.

Contributors Tove Lugnegård, Maria Unenge Hallerbäck and Christopher Gillberg designed the study and wrote the protocol. Tove Lugnegård, Maria Unenge Hallerbäck and Fredrik Hjärthag were responsible for all assessment of data. Tove Lugnegård and Fredrik Hjärthag undertook the statistical analysis Tove Lugnegård managed the literature search and wrote the first draft of the manuscript. Christopher Gillberg substantially contributed to drafting and revision of the article. All four authors contributed to and have made a final approval of the article to be published.

Conflict of interest All authors declare that they have no conflicts of interest.

Acknowledgments The authors would like to thank all study participants for their contribution.

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