Social cognition in schizophrenia: Cognitive and affective factors

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Socialcognitioninschizophrenia:Cognitiveandaffectivefactors

ArticleinCognitiveNeuropsychiatry·January2011

DOI:10.1080/13546805.2010.492693·Source:PubMed

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Ziv, Leiser and Levine 1

Running head: Social cognition in Schizophrenia

Submitted: Cognitive Neuropsychiatry

Social cognition in schizophrenia: cognitive and affective factors

Ido Ziva*, David Leiserb, Joseph Levinec

a School of Behavioral Sciences, Academic College of Tel Aviv-Yafo, Israel b Dept. of Psychology, Ben-Gurion University, Israel

c Medical school, Ben-Gurion University, Israel; Mental Health Centre, Beer-Sheva, Israel

Keywords: Social cognition, Theory of mind, Irony, Emotion understanding

Ziv, Leiser and Levine 2

Abstract

Introduction. Social cognition refers to how people conceive, perceive and draw

inferences about mental and emotional states of others in the social world. Previous

studies suggest that the concept of social cognition involves several abilities,

including those related to affect and cognition.

The present study analyses the deficits of individuals with schizophrenia in two areas

of social cognition: Theory of Mind and emotion recognition and processing.

Examining the impairment of these abilities in patients with schizophrenia has the

potential to elucidate the neurophysiological regions involved in social cognition and

may also have the potential to aid rehabilitation

Methods. Two experiments were conducted. Both included the same five tasks: first-

and second-level false-belief Theory of Mind tasks, emotion inferencing,

understanding of irony, and matrix reasoning (a WAIS-R subtest). The matrix

reasoning task was administered to evaluate and control for the association of the

other tasks with analytic reasoning skills. Experiment 1 involved factor analysis of the

task performance of 75 healthy participants. Experiment 2 compared 30 patients with

schizophrenia to an equal number of matched controls.

Results. (1) The five tasks were clearly divided into two factors corresponding to the

two areas of social cognition, Theory of Mind and emotion recognition and

processing. (2) Schizophrenics’ performance was impaired on all tasks, particularly

on those loading heavily on the analytic component (matrix reasoning and second-

order ToM). (3) Matrix reasoning, second-level Theory of Mind, and irony were

found to distinguish patients from controls, even when all other tasks that revealed

significant impairment in the patients' performance were taken into account.

Conclusions. The two areas of social cognition examined are related to distinct factors.

The mechanism for answering ToM questions (especially ToM2) depends on analytic

reasoning capabilities, but the difficulties they present to individuals with

schizophrenia is due to other components as well. The impairment in social cognition

in schizophrenia stems from deficiencies in several mechanisms, including the

abilities to think analytically and to process emotion information and cues.

Ziv, Leiser and Levine 3

Acknowledgements

This research was done with the help of the outpatient department of the Mental

Health Hospital in Beer Sheva, Israel. The authors wish to thank the following

research members for their assistance with data collection: Merav Saweri, Eyal Akiva,

and Revital Maroz from Ben-Gurion University; and Nurit ben-Arie-Ayulker and Noa

Berrzin-Cohen from the outpatient department. We are extremely grateful to Philip

Tyson and an anonymous reviewer for their helpful comments.

Ziv, Leiser and Levine 4

The present work addresses the issue of social cognition in schizophrenia.

Social cognition is related to the process of drawing inferences about other people's

beliefs and intentions in the social world (Green et al., 2008; Penn, Sanna, & Robert,

2008). In an extensive analysis of research findings, Green et al. (2008) propose that

the term "social cognition" covers five areas: Theory of Mind (ToM), social

perception, social knowledge, attribution bias, and emotion processing (Green, Olivier,

Crawley, Penn, & Silverstein, 2005; Penn, Addington, & Pinkham, 2006). They

maintain that there is convincing evidence suggesting that social cognition is not a

unitary concept. Understanding the factor structure of social-cognitive task measures

may thus be important to better understand these distinct domains of social cognition,

which will, in turn, inform studies of the distinct underlying neurophysiological

circuits and the development of specific, targeted social-cognitive treatments.

The realisation of the importance of measuring more than one aspect of social

cognition has begun to influence studies on schizophrenia (e.g.,Pinkham & Penn,

2006b; Sergi et al., 2007). However, this phase is in its initial stages and none of the

previous studies have measured the social cognition factor structure. The present work

strengthens this approach while focusing on two areas of social cognition: Theory of

Mind (ToM) and recognition and processing of emotion cues and information

(henceforth: RPE: recognition and processing of emotions).

The body of knowledge that has been gathered on social cognition and

mentalising in schizophrenia does not yet permit a satisfactory understanding of the

underlying mechanisms and components involved (Harrington, Siegert, & McClure,

2005; Sprong, Schothorst, Vos, Hox, & England, 2007). This study will specifically

examine the role of executive dysfunction in social cognition impairment. We will

follow the terminology used by Picket (2008) and others, and refer broadly to the

range of cognitive functions as we discuss Executive Functions (EF). If an executive

deficit is involved in impaired ToM in schizophrenia, it is likely that one of two

specific primary EFs are concerned: (1) the ability to disengage from and inhibit

salient information, such as the current reality of a situation, so that less salient

information (e.g., another person’s beliefs) can be considered; and (2) the ability to

manipulate representations of hypothetical situations in order to reason

consequentially (e.g., inferring another person’s beliefs about the current state of

Ziv, Leiser and Levine 5

affairs). The first EF is typically tested by using the Weigl Test (Weigl, 1941), the

Wisconsin Card Sorting Test (Heaton, 1981; Stroop, 1935), or the Stroop Colour-

Word Test (Stroop, 1935). The second EF is tested by evaluating strategic planning

tasks such as the Tower of London (Shallice, 1982), Key Search, or the Zoo Map

(Wilson, Alderman, Burgess, Emslie, & Evans, 1996). We will concentrate on the

second, that is expected to entertain contrasting relations with ToM and RPE, the

facets of social cognition we will be focusing on.

Schizophrenia, ToM, and EF

ToM is defined as the ability to attribute mental states (including beliefs,

intentions, desires, and goals) to the self and others. It also involves the ability to

understand that behaviour is the result of these mental states (Premack & Woodruff,

1978). Effective ToM abilities are important for normal social functioning because

they facilitate the understanding of people’s behaviour (Baron-Cohen, 1995).

There is converging evidence from many sources suggesting that EF plays a

significant role in ToM tasks performance. The development of ToM and success in

false belief inferences was shown to be based in part on that of EF, allowing for the

contribution of planning, response inhibition and cognitive flexibility to ToM function

(Carlson, Moses, & Breton, 2002; Carlson, Moses, & Claxton, 2004; Hughes, 2002;

Sabbagh, Xu, Carlson, Moses, & Lee, 2006; Wellman, Cross, & Watson, 2001).

Further, results from elderly participants indicate that their decreased ability to

understand others' beliefs and desires is related to a decline in executive skills,

especially inhibition, rather than to an inferior ability to mentalise (German &

Hehman, 2006). The extent of performance impairment in belief and desire reasoning

among both the elderly and younger adults has been related to the degree of

processing demand (McKinnon & Moscovitch, 2007). Similar conclusions were

reached with a student population, using a dual-task paradigm that manipulated EF

(inhibition, updating and switching) to assess their implication in ToM tasks (Bull,

Phillips, & Conway, 2008). For a further and more extensive discussion regarding

ToM and EF, see Ziv and Leiser (submitted).

ToM impairment is observed in schizophrenia. Five studies summarising the

schizophrenia research conducted in the last three decades were recently published.

Ziv, Leiser and Levine 6

Three of the studies provided an overview of social cognition: Brüne (2005b),

Harrington et al. (2005), and Penn et al. (2008). The remaining two were broad meta-

analyses of ToM and schizophrenia conducted by Pickup (2008) and Sprong et al.

(2007). Each of these studies explored the extent of mentalising impairment in

patients with schizophrenia, and all found a robust and serious impairment of ToM

abilities. Sprong et al. (2007) found that, on average, the ToM performance of

participants with schizophrenia was more than one standard deviation below that of

healthy controls. Applying Cohen’s (1988) statistical power analysis typology, they

found that the magnitude of the effect size of patients corresponded to a "large" effect,

and the effect size of mentalising impairments in patients in remission demonstrated a

"medium to large" effect. This finding was not the result of a verbalisation deficiency

(which is also a characteristic of patients suffering from schizophrenia) because tasks

relying on cartoon strips and pointing revealed the same impairment (Leiser &

Bonshtein, 2003; Sarfati, Hardy-Bayle, Brunet, & Widloecher, 1999; Sarfati, Hardy-

Bayle, Besche, & Wildlocher, 1997; Sarfati, Passerieux, & Hardy-Bayle, 2000).

Further, the deficiency in schizophrenia is more severe in individuals with other

psychiatric disorders, such as depressive disorder, unless psychotic features are

present (Bonshtein, Leiser, & Levine, 2006; Penn et al., 2008).

Results relating to specific schizophrenia symptoms have been ambiguous

thus far. Some studies have found connections between ToM impairment and positive

symptoms (Harrington, Langdon, Siegert, & Mc-Clure, 2005; Langdon, Coltheart,

Ward, & Catts, 2002), while others have found associations with negative symptoms

(Bora, Eryavuz, Kayahan, Sungu, & Veznedaroglu, 2006; Langdon, Coltheart, &

Ward, 2006). Several have produced no evidence of any relationship (Brüne, 2005;

Janssen, Krabbendam, Jolles, & Os, 2003). These findings imply that the mentalising

impairment is not just a manifestation of the acute phase of the disorder, but may

instead be a permanent trait. This belief stems from the finding that patients in

remission continue to show impaired abilities (Herold, Tenyi, Lenard, & Trixler, 2002;

Inoue et al., 2006), though the difference between patients in remission and healthy

participants was reduced (Bonshtein et al., 2006). Other studies claim that

performance returns to normal during periods of remission (Concoran, Cahill, & Frith,

1997; Drury, Robinson, & Birchwood, 1998; Pinkham & Penn, 2006a).

Ziv, Leiser and Levine 7

The findings we summarized on the pairwise relations between ToM, EF, and

schizophrenia raise the question of the involvement of EF in the ToM impairment

observed in schizophrenia. In a recent review, Pickup (2008) examined studies either

directly or indirectly addressing the relationship between ToM and EF in

schizophrenia. Overall, Pickup (2008) reported that, relative to controls, patients with

schizophrenia were significantly impaired both on ToM and EF tasks. Further, of the

17 studies reviewed, 14 reported significant correlations between ToM tasks and EF

tasks.

However, having examined the studies closely, Pickup (2008) made some

observations that do not support the summary presented above. First, no correlation

was found when the relationship between EF and ToM abilities was tested with

healthy control participants (as was done in only three studies: Brüne (2005a),

Langdon, Coltheart, Ward, & Catts (2001), and Pinkham & Penn (2006a)). Pickup

therefore suggested that the correlation that was found with the patient population

may be attributable to some other common cause, rather than to an inherent

relationship between EF and ToM. Second, Pickup further pointed out that eight

superior studies (Brüne , 2005a; Harrington, Langdon, Siegert, & Mc-Clure, 2005;

Janssen, Krabbendam, Jolles, & Os, 2003; Langdon, Coltheart, & Ward, 2006;

Langdon et al., 2001; Langdon, Coltheart, Ward, & Catts, 2002; Langdon, Corner,

McLaren, Ward, & Coltheart, 2006; Langdon, Davies, & Coltheart, 2002) that relied

on multivariate statistics revealed that even when EF was controlled for, ToM ability

continued to predict whether an individual had schizophrenia or was a healthy control.

It remains therefore unclear whether impairment in EF is involved in the

deficiency in ToM observed in schizophrenia. There is evidence that impairment to

the inhibitory control component of EF does not adequately account for social-

cognitive deficits in schizophrenia, while less is known of the relations between social

cognition and fluid, analytic reasoning. It also seems reasonable to expect that fluid

reasoning is more involved in tasks such as the False Belief tasks, especially those

relating to second-order false beliefs, than in the more affective component of social

cognition, RPE, to which we now turn our attention.

Ziv, Leiser and Levine 8

Emotion recognition and emotion understanding in schizophrenia

Emotion processing is primarily related to the ability to recognise and use

emotions (Feldman-Barrett & Salovey, 2002; Slater & Lewis, 2002). It includes four

abilities: identifying emotions, facilitating emotions, understanding emotions, and

managing emotions (Mayer, Salovey, Caruso, & Sitarenios, 2001; Salovey & Sluyter,

1997). Of these characteristics, two have been extensively studied in schizophrenia

research: (1) identifying emotions via facial expressions and affective prosody; and

(2) understanding emotions with ironic expressions.

A decade ago, Mandal, Pandey, and Prasad (1998) conducted a general review

of previous studies and found evidence that schizophrenia patients are strongly

impaired in the ability to recognise other people’s emotions based on their facial

expressions, gestures, or voices. This result was repeatedly found in later studies

(Brüne, 2005a; Hooker & Park, 2003). The duration of schizophrenia is closely

related to this impaired ability, and chronic patients suffering from marked negative

symptoms are more impaired than less chronic patients (Brüne, 2005a; Mueser et al.,

1996; Penn, Spaulding, Reed, & Sullivan, 1996).

Inferring the emotions involved in a social situation (like that a boy who was

tripped by his classmate will feel angry) is a more complicated process than merely

identifying facial expressions (Shamay-Tsoory, Tomer, & peretz, 2005), because it

requires a reasoning process.

The same holds for irony. The ironic meaning of a sentence is derived from

the difference between the literal meaning of the sentence and the speaker’s meaning

(Winner, 1988), that must be inferred. For example, someone who was embarrassed

by his friend may state: “you have acted like a gentleman”. The listener must

understand the difference between the literal meaning, "acted like a gentleman", and

the implicit intention, "you have acted badly". As Dennis, Purvis, Barnes, Wilkinson,

and Winner (2001) stress, the speaker intends for the listener to identify and

understand the deliberate falseness of his expression. Irony is typically used in

situations that include negative affect, such as contempt, scorn, or disapproval, and is

often used to convey criticism (Sperber & Wilson, 1986). While understanding of

irony involves an additional process relative to identifying emotions from facial

Ziv, Leiser and Levine 9

expressions, Shamay-Tsoory et al. (2005) found that both abilities are mediated by the

right prefrontal lobe.

The impaired understanding of irony in schizophrenia is well-established

(Langdon & Coltheart, 2004; Langdon, Coltheart et al., 2002; Langdon, Davies, &

Coltheart, 2002; Shamay-Tsoory & Aharon-Peretz, 2007; Shamay-Tsoory, Aharon-

Peretz, & Levkovitz, 2006; Shamay-Tsoory et al., 2007; Shuliang, Yanjie, Chan, &

Jianxin, 2008). The relationship between ToM understanding and irony understanding

has also been studied, though the findings are conflicting. Mo, Su, Chan, and Liu

(2008) found no support for the claim that insensitivity to irony in patients with

schizophrenia was associated with a deficient ToM, whereas Langdon and Coltheart

(2004) claimed that an intact ToM is a prerequisite for the interpretation of irony.

Studies of patients with localised lesions revealed dissociable prefrontal

networks for ToM and irony (Shamay-Tsoory & Aharon-Peretz, 2007; Shamay-

Tsoory, Tibi-Elhanany, & Aharon-Peretz, 2006). Based on these dissociable networks,

Shamay-Tsoory, Aharon-Peretz, and Levkovitz (2006) distinguish between cognitive

ToM, that primarily relates to traditional ToM tasks, and affective ToM, that relates to

RPE. This distinction corresponds to two of the social cognition areas identified by

Green et al. (2008): ToM and emotion processing. Shamay-Tsoory et al. (2005) argue

in favour of the relationship between ToM and irony, claiming that the understanding

of irony requires an integration of both components, (cognitive) ToM and emotion

processing.

The present study

We aimed to address two main objectives. First, we explored the factor

structure of two of the social cognition areas, ToM understanding and emotion

processing, as well as their associations with fluid, analytic reasoning. This analysis is

useful in elucidating the distinction and commonalities between these areas, and their

respective relations with the ability to reason analytically. Second, we studied the

independent contribution of each of the social cognition areas in order to discriminate

between schizophrenia patients and controls. This was intended to shed light on the

on-going debate regarding whether schizophrenia is domain-specific (Brune, 2005b;

Bryson, Bell, & Lysaker, 1997; Harrington, Siegert et al., 2005; Langdon et al., 1997)

Ziv, Leiser and Levine 10

or whether the impairment is fundamentally domain-general (e.g., as in the lack of

‘cognitive coordination’ proposed by Phillips and Silverstein (2003)). The two social

cognitive areas behaving as a single factor would suggest that the impairment in

schizophrenia is domain-general. The domain-specific hypothesis would be supported

by evidence that they function as two distinct factors.

Correspondingly, two experiments were constructed. In the first experiment,

we factor-analysed healthy participants performing a range of cognitive and affective

social cognition tests, and an analytic reasoning task. In keeping with the distinction

between the cognitive and emotional facets of social cognition posited in the literature

("ToM" and "emotion processing" in the list by Green et al. (2008), "cognitive ToM"

and "affective ToM", in the terms of Shamay-Tsoory, Aharon-Peretz, and Levkovitz

(2006)), we expected to find that the tasks would be divided into two factors. In the

second experiment, we compared the performance of schizophrenia patients and a

matching control group on the same cognitive and affective social cognition tests,

while controlling for analytic reasoning. We expected the performance of

schizophrenic patients to be impaired on both the cognitive and the affective social

cognition tasks. We also used logistic regression analyses to determine whether the

impairments in the cognitive and the affective aspects of social cognition dissociated

in the patients. Understanding the factor structure of social-cognitive task measures

may be important to better understand these distinct domains of social

cognition, which may, in turn, inform studies of the distinct underlying

neurophysiological circuits and the development of specific, targeted social-cognitive

treatments.

Experiment 1

Method

Seventy-five healthy participants (40 males, 35 females) with no history of

psychiatric disorders were recruited from the community. Their mean age was 29.86

(SD=10.69), with mean years of education 13.5 (SD=2.12). All of the participants

completed all of the tasks. The order of the tasks was counterbalanced across

participants.

Ziv, Leiser and Levine 11

Task Assessment

ToM Assessment (False Belief Stories)

This task was based on six ToM false belief stories (Frith & Corcoran, 1996)

that test the ability of participants to identify trickery and deal with first- and second-

order false beliefs. In first-order stories, the character has a mistaken belief about

reality. In second-order stories, there is a mistaken belief about the beliefs of another

character. The stories are simple and short. At the end of each story, two questions are

presented to the participants. The first can only be answered if the mental state of the

character is inferred. More specifically, to realize that a given belief is mistaken, the

participants must know the correct belief. The second question serves as a control and

to answer it, only the situation must be understood, while the use of ToM is

unnecessary. The second question ensures that the participant is cooperating,

understands the situation, and remembers the plot. For example, in one of the first-

order stories the subject is told about "Betty that put her chocolate in the drawer and

left the room. In her absence, her brother moved the chocolate to his closet". The

following two questions are: "A. Where will Betty search for her chocolate?" and "B.

Where did her brother put the chocolate?"

The second-order stories include an episode about "Dan who plans to visit

with Ruth an exhibition that should take place in Tel Aviv. While purchasing a

newspaper for their train journey Dan sees an advertisement, announcing that the

exhibition was moved to Haifa. On the way to the tickets office, Ruth sees the same

advertisement." The following two questions are: "A. To which city does Dan think

Ruth buy the tickets." and "B. What is the new location of the exhibition?" An

experimenter read all the questions to each participant and marked the participant’s

answer on the questionnaire sheet. The participant's score was the proportion of

correct answers.

Emotion Inference Questionnaire (EIQ)

For this novel task, participants were asked to infer an emotion related to a

relatively simple social situation presented in a short sentence. The following are

examples of the scenarios presented to participants: “In the course of giving a talk, Gil

Ziv, Leiser and Levine 12

began to stutter and his voice trembled. Did he feel embarrassed?”; “ Your mom’s

garden is blooming like her close friend’s garden. Will your mom be jealous of her

friend?” and “The neighbour's son did not get any presents for his birthday. Will he

be sad?” (see Appendix). In order to successfully complete this task, participants had

to grasp the situation and identify the emotion congruent with the situation. The

questions were forced-choice (yes/no). The questionnaire included 24 sentences

related to seven emotions: three basic emotions (happiness, sadness, and anger), and

four advanced emotions (insult, jealousy, embarrassment, and guilt). Each emotion

was represented by four sentences, two of which required a “yes” answer and two a

“no” answer. The scale yield cronbach's alpha =0.92.

Irony Understanding

This task was devised by Ackerman (1981) and translated into Hebrew by

Lapidot, Most, Pik, and Schneider (1998). The task consists of two versions (ironic

and neutral) of eight short stories. The sixteen stories were presented in randomised

order. The stories all involve some interaction between two characters. At the end of

each interaction, one of the characters makes a comment directed at the other. The

verbal comment was the same in both versions, but the intonation was manipulated. In

the ironic version, the comment was uttered with an ironic intonation, whereas the

neutral utterances were spoken with a neutral intonation. Consequently, the literal

meaning of the speaker’s comment in the ironic version was positive, though the

speaker’s true meaning was negative. In the neutral version, on the other hand, both

the literal meaning and the speaker’s intended meaning were positive. To illustrate, an

ironic version item described Joe, who came to work but sat down to rest instead of

beginning to work. His boss noticed his behaviour and said, “Joe, don’t work too

hard!” The neutral version was the same but the intonation was sincere and serious.

Each story was followed by two questions. The first question assessed the

participant’s understanding of the content by asking, “Did Joe work hard?” The

second question examined whether the participant appreciated the true meaning of the

speaker by asking, “Did the manager believe Joe was working hard?” The participant

received a score for the irony question only when both answers were correct. To

control for memory load, we discarded the question if the participant failed to answer

the content question correctly. Two scores were given to participants for this task: one

Ziv, Leiser and Levine 13

for the proportion of correct answers on understanding the irony, and one for the

proportion of correct answers on the control questions. Participants who made more

than two errors on the neutral version items were excluded and replaced. There was

therefore almost no variance in the scores on the neutral versions, and only those on

the irony versions of the stories will be used.

Matrix Reasoning

The matrix reasoning test, a WAIS-R subtest, is a standard measure of

nonverbal abstract problem solving, inductive reasoning, and spatial reasoning

abilities. The materials consist of 25 cards. On each card, a combination of figures is

presented. The participants’ task is to analyse the relationship between the figures

based on several variables (e.g., colour and spatial orientation), and to select a figure

that best fits the sequence from a set of options given at the bottom of the card. The

cards displayed are increasingly difficult, as answering them requires consideration of

an increasing number of variables, such as colour × size or colour × size × spatial

orientation.

Procedure

Participants were tested individually. An experimenter read the questions out

loud and marked the participant’s answer on a questionnaire sheet for each of the

tasks. Filler questions were interspersed as a control. The participant's score was

based on the proportion of correct answers on each task.

Results

A principal components factor analysis was conducted including all task

expect of the irony control task that yielded a ceiling effect. The number of factors

was not restricted. Two factors were extracted using principal-axes factoring and the

criteria of eigenvalue >1.0; they were optimised using varimax with Kaiser

normalisation rotation. The two factors account for 75.7% of the variance in the data.

Table 1 presents the loading upon rotation of the five tasks on the two factors. The

variables that loaded on the first factor were matrix reasoning, ToM1, and ToM2.

Those that loaded on the second factor were EIQ and understanding of irony. No

Ziv, Leiser and Levine 14

cross-loadings had weights above 0.20, and the two factors are not correlated (r=-

0.07).

Insert Table 1

Discussion

The results of Experiment 1 reveal a two-factor structure. The first factor

included ToM1, ToM2, and matrix reasoning; the second factor included EIQ and

understanding of irony. Delving into the first factor, we see that both ToM tasks (first-

and second-order) and matrix reasoning share the same underlying features. Matrix

reasoning is a WAIS-R subtest used to measure nonverbal abstract problem solving,

inductive reasoning, and spatial reasoning abilities. Matrix reasoning is strongly

related to advanced analytic abilities. The common pattern of loading of ToM1 and

ToM2 and Matrix reasoning suggests that both ToM tasks are related to a cognitive-

based factor and require analytic skills to successfully tackle the questions. EIQ and

irony understanding load on a second factor. Green et al.’s (2008) typology proposes

that social cognition covers five areas, including ToM and emotion processing. The

current findings suggest that these two areas are related to distinct factors.

These results are in line with the growing body of recent evidence that distinguishes

between cognitive and affective aspects of interpersonal skills, such as the

differentiation between cognitive ToM and affective ToM (Shamay-Tsoory, Aharon-

Peretz et al., 2006; Shamay-Tsoory et al., 2007). Recent neurophysiological findings

also support this distinction. Shamay-Tsoory, Aharon-Peretz, & Perry (2009) found

that subjects with ventromedial prefrontal damage showed impaired cognitive

empathy and ToM2 abilities while still exhibiting intact emotion recognition. Patients

with inferior frontal gyrus lesions, on the other hand, presented deficits in emotion

recognition while maintaining cognitive empathy and ToM2 abilities.

We nex turn to Experiment 2 in order to identify which factors and tasks were

significantly more difficult for schizophrenia patients than for healthy controls.

Ziv, Leiser and Levine 15

Experiment 2

Experiment 2 was designed to provide an analysis of the impairment of

schizophrenia patients regarding the two-factor structure. An additional goal of

Experiment 2 was to create a map of the significant inter-correlations of performance

on the tasks for both patients and controls.

Method

Participants and Design

Thirty patients with schizophrenia (21 males, 9 females), diagnosed according

to the DSM-IV (American Psychiatric Association, 1994), participated in this study.

Participants were treated in a day-care clinic at the Mental Health Centre in Beer

Sheva, Israel. They provided informed consent before participating. Patients’

psychopathology was measured using the Positive and Negative Syndrome Scale

(PANSS; Kay et al., 1989). The researchers rating psychopathology were blind to the

patients’ performance on the tasks used in the study. All of the patients were being

treated with antipsychotic medication. The patients’ mean age at onset of the disorder

was 23.5 years (range: 13–60 years; SD=11 years), with a mean duration of illness of

13.2 years (range: 1–35 years; SD=10.3 years). A similar number of healthy controls

(16 males, 14 females) with no history of psychiatric disorders were recruited from

the community. All participants performed the tasks presented in Experiment 1: ToM

false belief stories (first- and second-order), EIQ, irony understanding, and matrix

reasoning. Materials and procedure were identical to those of Experiment 1. Patients

and controls were matched according to age and education. Demographic

characteristics of the participants, including their psychopathology ratings, are shown

in Table 2.

Insert Table 2

Results

A mixed-design ANOVA Group × Task was used to analyse the data. The

score for each task was treated as a within-participant variable, and the group

(schizophrenia patient versus control) was a between-participants variable. There is

Ziv, Leiser and Levine 16

little purpose in comparing the means across tasks, as the questions were

heterogeneous and not matched for difficulty. Our interest lies in the differential

effect of schizophrenia on the tasks.

Overall, we found the expected significant main effect for schizophrenia,

F(1,57)=25.50; p<0.0001, as participants in the control group performed significantly

better than those in the schizophrenia group. We also observed a significant

interaction effect, F(5,285)=9.835; p<0.0001.

Table 3 presents follow-up t-test analyses (with Bonferroni adjustment of the

alpha to 0.05/6=0.00625) contrasting the performance of schizophrenic patients and

control group for each task. Both groups performed at similar levels on the irony-

control questions, indicating that patients and controls alike could handle a simple

conversation that did not include emotionally complicated phrases or analytic

understanding. The difference in performance between the groups was larger for the

matrix and ToM2 tasks, and slightly less pronounced for the Emotional Inference,

ToM1, and Irony Understanding tasks as reflected by the power analysis values. All

the differences were significant, except for two -- ToM1, and irony-control.

Insert Table 3

We computed the correlations between the main tasks (see Table 4).

Examining the correlation matrix for the patients group, we observe a significant

correlation between ToM1 and ToM2, as well as between matrix reasoning and ToM2.

The first correlation reflects the shared processes common to ToM1 and ToM2; the

second correlation indicates the need for analytic abilities when confronting ToM2

questions. The correlation between matrix reasoning and ToM1 trends in the same

direction (p=0.09), though it does not reach significance.

Insert Table 4

Proceeding to the right side and the data for the control group, the correlations

between the matrix task and ToM2 and between ToM1 and ToM2 are more marked.

In addition, the correlation between the matrix task and ToM1 is now significant.

Lastly, a correlation between ToM2 and the irony understanding task emerges. The

control group reflects the cognitive mechanisms required for the tasks, and a

Ziv, Leiser and Levine 17

comparison of the two tables may provide information regarding the deteriorated

mechanism in the patient group. Table 5 presents the correlations between the PANSS

evaluation dimensions and the tasks. Significant relationships were only found when

the negative psychological symptoms assessed by the PANSS were correlated with

the matrix, ToM2, and irony tasks (all these correlations are negative).

Insert Table 5

We used logistic regression to identify the task performances that discriminate

between patients and controls. The predictor variables were the five tasks (matrix

reasoning, ToM1, ToM2, EIQ and irony). Three of them – matrix, ToM2, and irony --

were found to distinguish patients from controls, even when all other tasks that

showed significant impairment in the patients' performance were taken into account.

The log L-R (likelihood-reduction) χ2 statistic -- that tests the significance of the

decrease in predictive power if a variable is removed from the full model-- is

significant for all three tasks (matrix: χ2 =43.8, p=0.003; ToM2: χ2 =10.646, p=0.01;

irony: χ2 =20.486, p=0.008).

General Discussion

Analysing the performance of healthy subjects on five tasks, Experiment 1

revealed that the tasks (first- and second-order ToM, EIQ and irony understanding,

and matrix reasoning) divide into two distinct factors that correspond to the two areas

of the social cognition ability, Theory of Mind (ToM), and EIQ. This pattern of

factors is also in accord with the findings of Shamay-Tsoory et al. (2007) and

Shamay-Tsoory & Tibi-Elhanany et al. (2006) regarding the distinction between

cognitive ToM and affective ToM, that are supported by recent neurophysiological

brain studies (Shamay-Tsoory et al., 2009).

Experiment 2 compared schizophrenia patients and healthy controls. The

patients and the control groups answered the irony-control questions with equal

accuracy. This shows that individuals with schizophrenia have adequate abilities

when it comes to comprehending a simple conversation that rarely demands advanced

cognitive or affective abilities. Experiment 2 confirmed the serious performance

impairment of patients with schizophrenia on all five tasks: ToM1, ToM2, EIQ, irony,

Ziv, Leiser and Levine 18

and matrix (and not on the irony-control task). These results are congruent with those

of Pickup (2008) and in line with previous studies showing that patients with

schizophrenia demonstrate impaired performance on all tasks involving EF and RPE

(emotion recognition, and the ability to appreciate the mental states of others) (Brüne,

2005b; Evans, Chua, McKenna, & Wilson, 1997; Langdon & Coltheart, 2004;

Langdon, Coltheart et al., 2002; Langdon, Davies et al., 2002; Pickup & Frith, 2001;

Poole, Tobias, & Vinogradov, 2000; Shamay-Tsoory & Aharon-Peretz, 2007;

Shamay-Tsoory, Aharon-Peretz et al., 2006; Shamay-Tsoory et al., 2007; Shuliang et

al., 2008). However, while Brüne (2005a), Langdon, Coltheart, Ward, and Catts

(2001), and Pinkham and Penn (2006a) failed to find significant correlations between

the ability to reason analytically and their ToM measures, we did find a significant

and positive correlation between matrix reasoning scores and performance on ToM2.

Our findings regarding the marked negative correlation between the negative

psychological symptoms assessed by the PANSS and performance on the tasks are in

line with the findings of Shamay-Tsoory et al. (2007), who also found significant

negative correlations between ToM measures and negative symptom ratings, but

differ from those Brüne (2005a), who failed to find significant correlations of this

type.

Negative symptoms signify a lack of certain abilities in schizophrenia patients

when compared to healthy individuals. The significant correlations between negative

symptoms and ToM2, irony understanding and matrix reasoning indicate a deficiency

in the mechanisms underlying these abilities.

What ability is involved? The extent of the difference between the patients

group and the control group was the largest for the matrix and ToM2 tasks.

Performance on these two tasks is correlated, in both the patients and control groups.

This fits well with the finding in Experiment 1 that ToM1 and ToM2 relate to the

same factor as matrix reasoning, while irony and emotion inference relate to another.

A natural interpretation is that the false-belief tasks require significant analytical

competence, and that ToM ability is related to the quality of fluid mental abilities.

The ToM2 and irony tasks were found to be correlated within the control

group. Mo et al. (2008) did not find this correlation, though they did produce related

findings, namely, that metaphor understanding was correlated with ToM2. For their

Ziv, Leiser and Levine 19

part, Langdon and collaborators (Langdon, Coltheart et al. (2002), Langdon, Davies et

al. (2002), and Langdon and Coltheart (2004)) found a significant correlation between

metaphor comprehension and ToM1. Mo et al. (2008) proposed that the relationship

between metaphor and ToM may be explained using the Relevance Theory of Sperber

and Wilson (1986, 1998). This theory holds that non-literal speech comprehension is

related to the understanding of mental states, such as those assessed by the false-belief

tasks. The significant correlation we found between ToM2 and irony supports this

notion to some extent, as irony is also a form of non-literal speech understanding.

The results of Experiment 2 provide important complements to the two-factor

structure found in Experiment 1 with healthy participants. The logistic regression

showed that matrix reasoning, ToM2, and irony all made significant independent

contributions to discrimination between patients and controls, even when all other

tasks that reveal significant impairment in the patients' performance are taken into

account. This suggests that: (1) the understanding of irony (as assessed in this study)

and ToM dissociate in schizophrenic patients; and (2) poor analytic reasoning

(indexed by matrix reasoning) does not completely explain the patients' difficulty with

second-order ToM and the understanding of irony.

Taken together, these results suggest several conclusions for social cognition

with respect to schizophrenia. First, the two areas of social cognition ability, Theory

of Mind and RPE, are related to distinct factors. This finding corresponds to Green et

al.’s (2008) typology. Second, while the mechanism needed for answering ToM

questions (especially of second-order) is significantly related to fluid intelligence, the

ability to reason analytically does not entirely account for the difficulties manifested

by schizophrenic patients on this task. The impaired social cognition skills of

individuals with schizophrenia appear to be due to the combination of several

deteriorated mechanisms, including both the ability to think analytically and the

ability to process emotional cues and information. Individuals with schizophrenia

suffer from several specific cognitive impairments that not only relate to the semantic

network or the inhibitory control ability, as proposed by Brüne (2005a), but also to the

interaction of these abilities with the cognitive impairment of analytical reasoning and

emotion processing. Accordingly, when discussing social cognition in relation to

schizophrenia, it is critical to stress both the emotional components and the

Ziv, Leiser and Levine 20

cognitive/analytic components. This is extremely important, because it implies that

patients could benefit from the development of specific clinical rehabilitation

programs that would address these varied and distinct impairments. Moreover, the

current results also support the study of separate neurophysiological circuits, as has

been done extensively by Shamay-Tsoory and colleagues (2007; 2006; 2009; 2006).

In closing, we wish to stress the importance and the necessity of future studies

that will validate and extend the results presented in this paper. We hypothesised that

the social cognition areas of ToM understanding and emotion processing were divided

into a two-factor structure. The results clearly support this claim. However, this

conclusion should be taken with caution, as an experimenter read all the tasks to the

participants and may have provided them with prosodic cues. This might account for

the irony task and the emotion inference tasks loading on the same factor. Future

studies should clarify the role of prosodic cues by using both written and oral stories

in modified irony tasks. More importantly, there is a need for broader studies that will

clarify whether all the areas of social cognition identified by Green et al (2005)

correspond to distinct factors when indexed by a range of suitable tasks, and how this

factor structure is modulated by schizophrenia.

Ziv, Leiser and Levine 21

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Ziv, Leiser and Levine 27

Appendix – Emotion Inferencing Questionnaire

During the break ToM ran in the garden. One of his classmates tripped him and he fell.

Will he be angry with the other boy?

Tomorrow Lisa will have a long day at school. Her mother will prepare her a

sandwich for lunch. Will Lisa be angry with her mother?

Dan asked his friend to help him study for a test. Instead, the friend went to sleep.

Will Dan be angry with his friend?

On the way to the local grocery, Rina does some shopping for her neighbours as well.

Will they be angry with her?

Your friend wrote a love letter for a girl and was rejected by her. Will he feel hurt?

The neighbour's son cleaned the garden and received from his mother his favourite

chocolate. Will he feel hurt?

Nir bought a birthday present for his friend with the money he saved. However, the

friend tossed it to the garbage in front of his eyes. Will Nir be hurt?

One of your classmates read his homework answer. Your teacher is enthusiastic about

the answer and praises your friend. Will the friend feel insulted?

The neighbour's son did not get any present for his birthday. Will he be sad?

Rinat won the first prize in the lottery. Will she be sad?

Mica was the only boy that was not invited to the birthday party. Will Mica be sad?

Ben achieved the best grade in the math test in his class. Will he be sad?

Your friend was chosen as "student of the month" and won a prize. Will he be happy?

The bicycle of the neighbour's daughter was stolen yesterday. Will she be happy?

You friend returned home hungry after a long and intensive basketball training. His

older brother made him supper. Will he be happy?

Ziv, Leiser and Levine 28

Ruth broke the flower vase in the living room. Her mother shouted at her. Will she be

happy?

Your friend studied for the test with her twin sister and received a lower grade than

her. Will she be jealous of her sister?

Solomon bought a brand-new car like his cousin. Will he be jealous of him?

Your younger brother asked your parents to buy him a toy he saw at his friend’s house.

However, your parents refused. Will your younger brother be jealous of his friend?

Your mom’s garden is blooming like her close friend’s garden. Will your mom be

jealous of her friend?

While ToM gave a talk, he started to stutter and his voice trembled. Will he feel

embarrassed?

Sera went with her parents to have dinner in a restaurant. When they entered the

restaurant, they found out that their table was not prepared even though they made

reservations in advance. The parents got angry and shouted at the manager and a fuss

broke out. Will Sera be embarrassed?

Miriam was angry with her friend. When she met her, she yelled at her and offended

her more than she previously intended. Will she feel guilty?

During a basketball game, the players from the rival team pushed Danni the entire

time. After the break, Danny decided to push them back. Will he feel guilty?

Ziv, Leiser and Levine 29

Table 1

Loadings on the two factors upon varimax rotation of the 5 tasks

Factor 1 Factor 2

Matrix 0.72 -0.16

ToM1 0.71 0.19

ToM2 0.75 -0.05

EIQ 0.18 0.76

Irony 0.04 0.74

Ziv, Leiser and Levine 30

Table 2

Demographic characteristics of schizophrenic patients and healthy controls

_____________________________________________________________________

Schizophrenia Healthy Statistics

Patients Controls

_____________________________________________________________________

N 30 30

Gender ratio (M:F) (21:9) (16:14)

Age (years) 37.83 + 11.32 35.56 + 12.64 P=0.46, n.s.

Education (years) 11.43 + 2.17 12.06 + 1.11 P=0.16, n.s.

Age at onset (years) 24.28 + 11.08

Duration of illness

(years) 13.20 + 13.37

PANSS positive subscale 19.16 + 7.18

PANSS negative subscale 17.01 + 5.17

PANSS general subscale 39.96 + 9.48

PANSS total sum* 58.12 + 16.53

_____________________________________________________________________

* Total score – 18 points

Ziv, Leiser and Levine 31

Table 3

t-test analyses (with Bonferroni adjustment) for all tasks

Task Controls Patients Effect Observed Power

Mean SD Mean SD t(58) P

Matrix 0.72 0.18 0.36 0.18 7.719** 0.000 1.00

EIQ 0.97 0.04 0.88 0.15 2.811** 0.006 0.83

ToM1 0.98 0.06 0.91 0.17 2.304 0.024 ----

ToM2 0.90 0.18 0.65 0.40 3.088** 0.003 0.98

Irony 0.95 0.08 0.85 0.16 3.085** 0.003 0.78

Irony-

Control

0.88 0.14 0.89 0.15 0.351 0.726 ----

Ziv, Leiser and Levine 32

Table 4 – Correlations between the tasks

Patients Control

Matrix EIQ ToM1 ToM2 Matrix EIQ ToM1 ToM2

EIQ 0.15 EIQ 0.27

ToM1 0.31 0.13 ToM1 0.50** 0.34

ToM2 0.36* 012 0.41* ToM2 0.60** 0.18 0.50**

Irony 0.30 (-.11) (-0.08) 0.20 Irony 0.31 0.16 0.13 0.52**

*p<0.05 **p<0.01

Ziv, Leiser and Levine 33

Table 5 – Correlations between PANSS evaluations and tasks. (Significant

correlations are in bold.)

Matrix EIQ ToM1 ToM2 Irony

Positive (-0.192)

p=0.358

(-0.014)

p=0.944

(-0.173)

p=0.407

(-0.191)

p=0.36

(-0.293)

p=0.155

Negative (-0.524)

p=0.007

(-0.083)

p=0.692

(-0.277)

p=0.180

(-0.553)

p=0.004

(-0.423)

p=0.035

General (-0.202)

p=0.331

(-0.287)

p=0.165

(-0.244)

p=0.239

(-0.192)

p=0.562

(-0.192)

p=0.917

Total (-0.363)

p=0.074

(-0.197)

p=0.344

(-0.302)

p=0.142

(-0.326)

p=0.112

(-0.272)

p=0.188