INTRODUCTION
Theory of Mind (ToM), defined as a wide range of processes used to infer inner mental states of oneself and others, has become one of the main research areas in studying processes that may underlie difficulties observed in social functioning of patients with schizophrenia (SCZ). This interest is largely driven by the fact that ToM impairments, among other social cognitive deficits in patients, are better predictors of their everyday functioning than deficits in non-social cognition, for example, working memory, learning, or attention (Fett et al., Reference Fett, Viechtbauer, Dominguez, Penn, van Os and Krabbendam2011).
Several different methodologies have been used to examine ToM in SCZ (Montag et al., Reference Montag, Dziobek, Richter, Neuhaus, Lehmann, Sylla and Gallinat2011; Okruszek et al., Reference Okruszek, Bala, Wordecha, Jarkiewicz, Wysokiński, Szczepocka and Marchel2017). A meta-analysis of 50 studies with, overall, 1536 SCZ and 1760 healthy comparison subjects (HC) converged toward large effects for ToM deficits in SCZ (g=0.96; Savla, Vella, Armstrong, Penn, & Twamley, Reference Savla, Vella, Armstrong, Penn and Twamley2013). However, most of these studies treated ToM as a unitary concept, but it is worth noting that ToM is a multifaceted construct, which encompasses a wide range of processes, associated both with cognitive and affective processing of mental states of others. Several accounts from both healthy (Bottiroli, Cavallini, Ceccato, Vecchi, & Lecce, Reference Bottiroli, Cavallini, Ceccato, Vecchi and Lecce2016) and clinical populations (Dennis et al., Reference Dennis, Simic, Bigler, Abildskov, Agostino, Taylor and Yeates2013) support the disjunction between cognitive and affective ToM. While cognitive ToM is linked to the understanding of others’ intentions and beliefs, affective ToM taps into processes associated with attributing emotional states to others. Both types of ToM processes have been shown to be linked to distinct, albeit overlapping, neural networks: while both types of abilities engage temporo-parietal regions, only affective ToM has been linked to ventromedial prefrontal activity (Corradi-Dell’Acqua, Hofstetter, & Vuilleumier, Reference Corradi-Dell’Acqua, Hofstetter and Vuilleumier2014). On the other hand, functional independence of cognitive ToM has also been observed, with repetitive transcranial magnetic stimulation of right dorsolateral prefrontal cortex impacting cognitive, but not affective ToM task performance (Kalbe et al., Reference Kalbe, Schlegel, Sack, Nowak, Dafotakis, Bangard and Kessler2010).
Previous studies have led to conflicting findings, suggesting either specific impairment in affective ToM (Shamay-Tsoory et al., Reference Shamay-Tsoory, Shur, Barcai-Goodman, Medlovich, Harari and Levkovitz2007), or a similar level of impairment in cognitive and affective ToM (Ho et al., Reference Ho, Lui, Hung, Wang, Li, Cheung and Chan2015; Montag et al., Reference Montag, Dziobek, Richter, Neuhaus, Lehmann, Sylla and Gallinat2011) in SCZ. However, both types of the tasks, which have been used so far to dissociate affective and cognitive ToM in SCZ, tapped strongly into visual processing, by using either cartoons (Shamay-Tsoory et al., Reference Shamay-Tsoory, Shur, Barcai-Goodman, Medlovich, Harari and Levkovitz2007) or scenes presented as videos (Montag et al., Reference Montag, Dziobek, Richter, Neuhaus, Lehmann, Sylla and Gallinat2011). Thus, the findings of the studies that were based on them may be confounded by the basic social perception or emotion recognition deficits which are observed in SCZ (Green, Horan, & Lee, Reference Green, Horan and Lee2015; Savla et al., Reference Savla, Vella, Armstrong, Penn and Twamley2013). To address this issue, we used the novel task, which examines both cognitive and affective ToM and is based purely on verbal material, thus minimizing the impact of perceptual processing on the patients’ performance (Pluta, Gawron, Sobańska, Wójcik, & Łojek, Reference Pluta, Gawron, Sobanska, Wójcik and Łojek2017). It has been suggested that affective ToM is more automatic and less prone to neurodegeneration or brain injury than cognitive ToM (Bottiroli et al., Reference Bottiroli, Cavallini, Ceccato, Vecchi and Lecce2016; Dennis et al., Reference Dennis, Simic, Bigler, Abildskov, Agostino, Taylor and Yeates2013). This also is in line with results of developmental studies demonstrating that children understand other people’s emotions earlier than their beliefs (Singer, Reference Singer2006).
Thus, we hypothesize that, after minimizing the impact of deficient social perception and emotion recognition, by using verbal vignettes only, a lower magnitude of impairments will be found for affective than for cognitive ToM in SCZ.
MATERIALS AND METHODS
Neuropsychological Assessment
ToM tasks consisted of 81 questions (45 mentalizing questions, MQ, and 36 control questions, CQ) within 18 items. Each item consisted of a short verbal vignette, describing categories of social interactions encompassing false beliefs, false attributions, lies, sarcasm, and faux pas. In each item, a correct response to MQ depended on the participant’s understanding of the protagonist’s mental states, while a correct response to CQ depended on a literal understanding of the storyline. To evaluate understanding of affective or cognitive mental states, MQ were further divided into 23 questions referring to the protagonist’s affective mental states (A-ToM) and 22 questions about the protagonist’s cognitive mental states (C-ToM).
Participants received 2 points for each correct answer, 1 point for a partial answer, and 0 points for the lack of or an incorrect answer. The answers were evaluated based on the answer key established during a pilot study on 22 healthy subjects. A full description of the task may be found in Pluta et al. (Reference Pluta, Gawron, Sobanska, Wójcik and Łojek2017). The task performance has been previously shown to differentiate stroke patients from healthy subjects and be associated with both pragmatic competence and executive functioning measures (Pluta et al., Reference Pluta, Gawron, Sobanska, Wójcik and Łojek2017). The sample stimuli are presented in the Appendix.
Description of other tasks which have been applied to enable analysis of the relationship between ToM subcomponents and other neurocognitive (Jędrasik-Styła et al., Reference Jędrasik-Styła, Ciołkiewicz, Styła, Pankowski, Denisiuk, Linke and Wichniak2014) and social cognitive domains (Baron-Cohen, Wheelwright, Hill, Raste, & Plumb, Reference Baron‐Cohen, Wheelwright, Hill, Raste and Plumb2001; Olszanowski et al., Reference Olszanowski, Pochwatko, Kuklinski, Scibor-Rylski, Lewinski and Ohme2015; White, Coniston, Rogers, & Frith, Reference White, Coniston, Rogers and Frith2011) can be found in the Supplementary Material.
Participants
Twenty-four SCZ were recruited to participate in the study from the Department of Old Age Psychiatry and Psychotic Disorders, Medical University of Łódź (Poland). To be included in the study, patients had to be diagnosed with schizophrenia according to ICD-10 criteria and could have no comorbid psychiatric or neurological disorders. Patients were assessed with the Positive and Negative Syndrome Scale (PANSS; Kay, Opler, Lindenmayer, Reference Kay, Opler and Lindenmayer1988) by qualified psychiatrists (A.W./E.S.). Twenty-two HC with no history of psychiatric or neurological treatment were recruited to participate in the study through online advertisements. Each participant signed an informed written consent upon inclusion in the study, and the study protocol was accepted by the Bioethics Committee at the Medical University of Lodz. No differences were found between groups in terms of age (HC: 34.3±12.0 vs. SCZ: 35.5±10.5; t(43)=0.4; p=.72), gender (HC: 11M/10F vs. SCZ: 16M/8F; Chi-squared=1.0; p=.33), or years of education (HC: 14.0±2.4 vs. SCZ: 12.7±2.8; t(43)=1.7; p=.11).
Overall, patients presented moderate levels of both positive (PANSS-Positive: 19.5±5.5) and negative (PANSS-Negative: 23.0±7.4) symptoms of schizophrenia at the time of the study. All of the patients were medicated. All but one of the patients were treated with antipsychotics, either atypical (n=18) or a combination of typical and atypical (n=5). The mean chlorpromazine (CPZ) equivalent dose was 672±342 mg. Four patients were receiving antidepressant treatment, and four patients were medicated with benzodiazepines.
Statistical Analysis
For the analysis of the ToM task performance, a percentage of correct responses for each condition was calculated. Repeated-measures analysis of variance was then performed with Condition (Control, Affective, Cognitive) as a within-subject factor and Group (Patients, Controls) as a between-subject factor. All of the results were Greenhouse-Geisser corrected.
To examine the relationship between the performance in each condition of the ToM task and performance in other social cognitive tasks, Spearman rho values were calculated. Because for each external variable three correlation coefficients were calculated (control/affective/ cognitive), the threshold for correlation was corrected accordingly, thus producing p=.0167 significance threshold.
RESULTS
Verbal ToM: The main effects of the group (F(1,43)=27.2; p<.001) and the type of task (F(2,43)=44.6; p<.001) were observed with overall higher performance in HC (88±8%) than in SCZ (71±13%), and with higher accuracy for control stories (88±10%) than for affective (77±16%) or cognitive ToM scores (73±19%).
Furthermore, an interaction between group and the type of the task was found (F(2,43)=6.2; p=.005). Investigation of this effect revealed that while in HC no differences were found between cognitive and affective ToM accuracy (t(20)=0.4; p=.72; COG: 85±13% vs. AFF: 86±7%), in SCZ (t(23)=2.1; p=.045; COG: 62±17% vs. AFF: 68±17%) affective ToM was less impaired than cognitive ToM. Accuracy for control condition was higher than for ToM conditions both in HC (CON: 94±6%; CON vs. AFF: t(20)=6.1; p<.001; CON vs. COG: t(20)=3.9; p=.001) and in SCZ (CON: 83±10%; CON vs. AFF: t(23)=6.8; p<.001; CON vs. COG: t(23)=8.3; p<.001).
Other Tasks
Patients performed worse than controls across all of the B-CATS tests (Digit Symbol: SCZ:36.0±10.9 vs. HC:57.6±12.6; t(43)=6.2; p<.001; Category Fluency: SCZ:19.3±5.2 vs. HC:29.6±5.4; t(43)=6.2; p<.001; TMT-B: SCZ:117.0±92.3 vs. HC:59.4±34.5 t(43)=2.7; p=.010).
A main effect of the group was found for each of the additional tasks, which have been used to examine social cognitive processes in both groups. Patients were less successful than controls in recognizing basic emotion on the basis of facial displays (HC:43.6±3.4 vs. SCZ:37.3±7.8; t(42)=3.4; p=.001) and in attributing complex mental states on the basis of the picture of the eyes (HC:27.1±3.0 vs. SCZ:21.5±5.0; t(42)=4.5; p<.001). Furthermore, patients had problems in both classifying the actions (HC:10.4±1.8 vs. SCZ:7.5±2.1; t(41)=4.8; p<.001) and in selecting a specific alternative (HC:5.2±1.1 vs. SCZ:3.8±1.8; t(41)=3.0; p=.005) in the Frith-Happe task.
Correlations
In SCZ, both C-ToM (rho=0.56; p=.005) and A-ToM (rho=0.49; p=.0166) were correlated with performance in the Frith-Happe task alternative selection task. No correlations were found between ToM and B-CATS subtests.
In HC, A-ToM was correlated with RMET score (rho=0.60; p=.004) and with TMT-B time (rho=−0.65; p<.001).
DISCUSSION
The aim of this study was to analyze the pattern of affective and cognitive ToM abilities in patients with schizophrenia by using a single paradigm depicting everyday social interactions, which examined both types of processes within a single task. We found that, while patients showed deficient performance in all conditions of the verbal ToM task, the magnitude of the deficits was larger for cognitive than for affective ToM. A recent comprehensive review of mechanisms of social cognitive deficits in SCZ (Green et al., Reference Green, Horan and Lee2015) provides a conceptual framework to understand this finding. Distinct sets of abilities are required to successfully perform each type of task.
Successful performance in an affective ToM task is highly dependent on the ability to use one’s own emotional experience generated while tracking the story, whereas cognitive ToM is strongly linked with social knowledge and reasoning abilities. Thus, an affective ToM condition may be perceived more as a reflexive process, when compared to cognitive ToM. It has been proposed that while effortful reflective social cognitive processes are strongly impacted in schizophrenia, some of the reflexive processes may be intact in patients (Green et al., Reference Green, Horan and Lee2015). In line with this framework, affective ToM, which is more automatic and based on reflexive processes, may differentiate patients from healthy comparison subjects to a lesser extent than cognitive ToM.
Just a handful of previous studies have separately examined cognitive and affective ToM in SCZ. First, Shamay-Tsoory et al. (Reference Shamay-Tsoory, Shur, Barcai-Goodman, Medlovich, Harari and Levkovitz2007) and Ho et al. (Reference Ho, Lui, Hung, Wang, Li, Cheung and Chan2015) used the “Yoni task,” which is a cartoon-based task that requires participants to infer either emotional or non-emotional mental states in the presented character. The first of these studies found a decreased number of errors on affective as compared to cognitive ToM in HC during the task, but no such pattern in SCZ (Shamay-Tsoory et al., Reference Shamay-Tsoory, Shur, Barcai-Goodman, Medlovich, Harari and Levkovitz2007). However, a subsequent study, which examined both types of ToM in first-episode SCZ, their unaffected siblings, and HC found no group by condition interaction with higher performance in affective as compared to cognitive ToM conditions in all three groups of participants. Furthermore, as was stressed by the authors of the latter study, the Yoni task, which is purely cartoon-based, may not be an appropriate tool for examination of “cold” (cognitive) and “hot” (affective) ToM abilities (Ho et al., Reference Ho, Lui, Hung, Wang, Li, Cheung and Chan2015).
Montag et al. (Reference Montag, Dziobek, Richter, Neuhaus, Lehmann, Sylla and Gallinat2011) used the Movie for Assessment of Social Cognition (MASC) methodology, which is a more ecologically valid task as compared to the Yoni task, to examine affective and cognitive mental state attribution in 80 SCZ and 80 HC. The authors found impairments of similar magnitude for both ToM domains in SCZ and attributed this effect to significantly higher demands of MASC in terms of mental state attribution as compared to the Yoni task (Montag et al., Reference Montag, Dziobek, Richter, Neuhaus, Lehmann, Sylla and Gallinat2011).
In line with both Ho et al. (Reference Ho, Lui, Hung, Wang, Li, Cheung and Chan2015) and Montag et al. (Reference Montag, Dziobek, Richter, Neuhaus, Lehmann, Sylla and Gallinat2011), we found deficient performance across ToM domains in patients as compared to controls. However, unlike the aforementioned studies, our vignettes, which were limited to a verbal description of the situation, did not engage lower-level social cognitive processes. In line with our hypothesis, we found significant (albeit modest) decrease in cognitive ToM as compared to more automatic affective ToM in patients group.
Unlike previous studies, which have linked specific domains of ToM with either positive (Montag et al., Reference Montag, Dziobek, Richter, Neuhaus, Lehmann, Sylla and Gallinat2011; Okruszek et al., Reference Okruszek, Bala, Wordecha, Jarkiewicz, Wysokiński, Szczepocka and Marchel2017) or negative (Shamay-Tsoory et al., Reference Shamay-Tsoory, Shur, Barcai-Goodman, Medlovich, Harari and Levkovitz2007) symptoms of schizophrenia, we did not document such a relationship. Furthermore, while performance in the affective condition of the task was related to the task that taps into mental state decoding, no such effect was observed in patients. On the other hand, performance in both conditions of Verbal-ToM (V-ToM) was linked to performance during the alternative selection task in the Frith-Happe task. Successful performance in Frith-Happe tasks is dependent on the number of ToM abilities, which combine both automatic mentalizing processes and explicit mental state inference. Thus, it may be hypothesized that the correlation between the performance in both tasks may reflect general ToM impairment in patients.
Several limitations of our study must be pointed out. First, all of the participants from the patient group were medicated at the time of the study. While we did not find a significant correlation between CPZ equivalents and any V-ToM measures, medication still could have affected the cognitive processes underlying ToM abilities. Additionally, we did not perform a detailed neuropsychological examination of various cognitive functions; accordingly, we cannot exclude the possibility that the differences in cognitive ToM were in fact caused by a basic non-social neurocognitive function impairment.
However, several studies (Carlson and Moses, Reference Carlson and Moses2001; Wang et al., Reference Wang, Shi, Roberts, Jiang, Shen, Wang and Wang2015) have indeed shown a positive correlation between ToM and inhibition (investigated in our study with the use of TMT-B). These studies argued that, to understand another person’s mental states, one’s own dominant perspective has to be inhibited. However, in our study the correlation between TMT-B and V-ToM was not significant in the patient group, and, therefore, this interpretation is rather unlikely. Furthermore, our main task was based on the verbal comprehension of the stories, thus the fact that, due to the extensive social cognitive testing, verbal IQ was not assessed in the study is another limitation of the current study.
Additionally, the task which included both affective and cognitive ToM questions within the same scenario minimizes the methodological differences in assessment of both types of ToM abilities. However, construction of the task may lead to answers to one type of question impacting the responses to the other. Finally, although the V-ToM task has been previously applied with neuropsychiatric populations (Pluta et al., Reference Pluta, Gawron, Sobanska, Wójcik and Łojek2017), and each of three subscales has shown satisfactory internal consistency in a current sample (Cronbach’s α>=0.8 for each of three scales), its psychometric values require further investigation.
The results of the current study add to the previous literature, by further establishing that ToM deficits in SCZ are a multifaceted problem and both cognitive and affective ToM should be examined during the assessment of social cognitive functioning in schizophrenia. Furthermore, as various ToM subcomponents may be differentially affected in SCZ, it may be suggested that strategies which are tailored to address the specific ToM impairments observed in patients may be more beneficial than broad-scope interventions aimed at improving social cognition in schizophrenia.
ACKNOWLEDGMENTS
The authors declare that there are no conflicts of interest in relation to the subject of this study. Ł.O. was supported by Foundation for Polish Science Start (074.2016) program.
Supplementary Material
To view supplementary material for this article, please visit https://doi.org/10.1017/S1355617717000960
Appendix A. Exemplary items from ToM task.
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1. John prepares a dinner and accidentally pours some tomato sauce on himself. Within a moment, his sister enters the kitchen and, noticing the red liquid on John’s face and a knife on the table, says: “I will bring the bandage.”
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1. What is the sister feeling when she spots John? [A-ToM]
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2. Why, According to John’s sister, does she want to bring a bandage? [C-ToM]
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3. Did John cut himself? [CQ]
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2. Peter has a date with Katrina. He likes her very much, and he would like to make a good impression. They arrange a meeting in a horse club because Katrina is very good at horse riding. While she is sitting on a horse encouraging him to do the same, Peter, who is a good actor, touches his chest and says: “I just got a terrible heartache. . . .”
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1. Why did he say that? [A-ToM]
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2. What does, according to Peter, Katie think about his behavior? [C-ToM]
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3. Did Peter have heartache in fact? [CQ]
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4. Where did they meet? [CQ]
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3. Martha and Kate meet at a party. Looking at Kate’s protruding abdomen, Martha says, “I can see that pregnancy does you good. Am I right to say, by the looks of your belly, that you are in your seventh month?” Confused, Kate replies, “Martha, I am NOT pregnant…”
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1. Did anyone say anything improper? [C-ToM]
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2. Why did Martha congratulate Kate? [C-ToM]
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3. How was Kate feeling when she heard Martha’s congratulations? [A-ToM]
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4. Is Kate pregnant? [CQ]
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5. Where were the friends? [CQ]
