FULL-LENGTH ORIGINAL RESEARCH

Theory of mind and social functioning in patients with temporal lobe epilepsy *Wei-Han Wang, †‡Yang-Hsin Shih, *‡Hsiang-Yu Yu, *‡Der-Jen Yen, *‡Yung-Yang Lin, *‡Shang-Yeong Kwan, *‡Chien Chen, and §¶#**Mau-Sun Hua Epilepsia, 56(7):1117–1123, 2015 doi: 10.1111/epi.13023

SUMMARY

Wei-Han Wang, Ph.D., is a clinical neuropsychologist specializing in epilepsy at the Taipei Veterans General Hospital (TPEVGH), Taiwan.

Objective: This study aimed to explore the effects of theory of mind (ToM) and related potential risk factors, including cognitive functions, psychiatric status, and seizure-related clinical variables, on social functioning in patients with temporal lobe epilepsy (TLE). Methods: Sixty-seven patients with intractable TLE who were potential candidates for epilepsy surgery and 30 matched controls were included. All participants completed four tasks measuring different levels of ToM (False Belief, Faux Pas Recognition, Implication Stories, and Visual Cartoon), the Symptom Checklist-90-Revised (SCL-90-R), the Social and Occupational Functioning Scale for Epilepsy (SOFSE), and neuropsychological tests. Results: The patients exhibited impairments in both basic and advanced ToM. Multiple regression analyses revealed the following: (1) the SOFSE total score was significantly predicted by the Faux Pas Recognition (FPR), Global Severity Index (GSI) score of the SCL-90-R, and Full-Scale intelligence quotient (IQ) of the Wechsler Adult Intelligence Scale (WAIS), which accounted for 38%, 11%, and 8% of the variance, respectively; and (2) the FPR was a significant predictor of all SOFSE subscales, whereas the GSI score contributed substantially to the Interpersonal Relationships, Communication, and Occupation subscales of the SOFSE. Significance: Advanced ToM, measured by impaired faux pas recognition, is a relatively strong predictor of poor social functioning in surgical candidates for intractable TLE. Identifying ToM impairment may help plan nonpharmacologic treatment for improving social functions in patients with intractable TLE. KEY WORDS: Theory of mind, Social cognition, Social functioning, Epilepsy, Cognitive function.

Epilepsy is a chronic disorder characterized by recurrent seizures, which has significant cognitive and psychosocial consequences for everyday living.1,2 People with epilepsy (PWEs), even those with well-controlled seizures, may face poor interpersonal relationships, reduced social interactions, decreased job opportunities, and problems in daily activities.3,4 The relationship between social cognition and

psychosocial function in PWEs has been gaining considerable attention in recent years. Social cognition refers to how people perceive and interpret social information, and how well they respond to this information.5 A key aspect of social cognition is the ability to conceptualize other people’s thoughts, intentions, and desires, which is known as “theory of mind” (ToM).6

Accepted April 6, 2015; Early View publication May 16, 2015. Departments of *Neurology and †Neurosurgery, Neurological Institute, Taipei Veterans General Hospital, Taipei, Taiwan; ‡National Yang-Ming University, Taipei, Taiwan; Departments of §Neurology; ¶Psychiatry, National Taiwan University Hospital, Taipei, Taiwan; #Neurobiology and Cognitive Science Center, National Taiwan University, Taipei, Taiwan; and **Graduate Institute of Brain and Mind Sciences, National Taiwan University, Taipei, Taiwan Address correspondence to Mau-Sun Hua, Department of Psychology, National Taiwan University, No. 1, Sec. 4, Roosevelt Rd., Taipei 106, Taiwan. E-mail: [email protected] Wiley Periodicals, Inc. © 2015 International League Against Epilepsy

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Key Points • • • •

Patients with intractable TLE exhibit impairments in both basic and advanced ToM. Social functioning difficulties in patients with intractable TLE are multi-determined in nature. Advanced ToM deficits, psychiatric disturbances, and intellectual impairment can significantly contribute to abnormal social functioning. Impaired advanced ToM is a relatively strong predictor of poor social functioning in patients with intractable TLE.

Temporal lobe epilepsy (TLE), a common type of focal epilepsy, is characterized by epileptogenic discharges arising from temporal regions. A growing body of evidence has demonstrated that TLE may impair ToM by affecting regions of the underlying neural network of ToM.5–9 However, the relationship between ToM deficits and abnormal social functioning remains unclear in patients with TLE. Social functioning has been widely defined as the capacity of a person to function in different societal roles such as homemaker, worker, or student.10 Our previous study found that cognitive impairments and psychiatric disturbances can have adverse effects on social functioning in TLE.11 In addition, a strong relationship between seizure-related clinical variables (such as epilepsy duration and seizure frequency) and psychosocial difficulties has been documented.12,13 Taken together, the relative contribution of each of the ToM deficits and other risk factors, as mentioned earlier, to abnormal social functioning in TLE awaits further investigation. Several studies have indicated that ToM is a composite function, which involves joint attention, memory, language, executive functions, and complex perceptual recognition (such as face processing).8,14–16 To identify the component skills that might be adversely affected, a number of neuropsychological tests measuring these cognitive functions should be included when assessing ToM. In view of the preceding reasons, we employed four standardized ToM tasks, neuropsychological tests, and the Social and Occupational Functioning Scale for Epilepsy (SOFSE)11 to explore the effects of ToM abilities and related potential risk factors, including cognitive functions, psychiatric status, and seizure-related clinical variables, on social functioning in patients with TLE.

Methods Subjects This study was approved by the institutional ethics committee of the Taipei Veterans General Hospital (TPEVGH), one of the largest medical centers in Taiwan. At enrollment, Epilepsia, 56(7):1117–1123, 2015 doi: 10.1111/epi.13023

written informed consent was obtained from all participants. Sixty-seven adult inpatients with TLE were recruited from the Neurological Institute at TPEVGH. All patients were diagnosed with medically refractory epilepsy by experienced epileptologists, according to the criteria defined by the International League Against Epilepsy (ILAE).17 Clinical data, including age at seizure onset, epilepsy duration, and seizure frequency, were collected through a semistructured questionnaire by the epileptologists, who interviewed the patient and at least one witness to the seizures (usually a relative of the patient). In addition, the number of antiepileptic drugs used was obtained from medical records. None of the patients had undergone brain surgery before recruitment. For determining whether a patient was a candidate for epilepsy surgery, each patient underwent an extensive presurgical evaluation, including long-term video–electroencephalography (EEG) monitoring, structural (magnetic resonance imaging; MRI), and functional (positron emission tomography [PET] and/or single-photon emission computed tomography [SPECT]) brain imaging studies, neuropsychological testing, and intracarotid amobarbital testing. Patients with abnormal MRI findings outside the temporal regions and a history (or current diagnosis) of neurodevelopmental disorders (such as autism spectrum disorder or attention-deficit/hyperactivity disorder), neurodegenerative diseases, major depression, anxiety disorders (including social phobia), mental retardation, physical limitations, and severe systemic disease were excluded. On these bases, a total of 67 TLE patients were recruited. Structural MRI indicated medial temporal lobe sclerosis in 36 patients. Other lesions (such as dysplasias, brain tumors, or atrophic lesions) were detected in the medial temporal region in nine patients and in the lateral temporal area in seven patients. Finally, 15 patients had cryptogenic epilepsy with interictal epileptiform discharges originating in the temporal lobes. Thirty healthy controls (HCs) were selected and underwent neuropsychological testing. Participants were excluded if there was a history of psychiatric disorders, mental retardation, severe systemic disease, or any neurologic disease relevant to cognitive impairment. ToM tasks Four standardized ToM tasks in Chinese were used to measure ToM ability: the False Belief (FB) test, Faux Pas Recognition (FPR) test, Implication Stories (IS) test, and Visual Cartoon (VC) test.18 The internal consistency coefficients (Cronbach’s a) of the tasks were 0.50 for the firstorder FB test, 0.67 for the second-order FB test, 0.91 for the FPR test, 0.93 for the IS test, 0.87 for the VC test in implicit form, and 0.92 for the VC test in explicit form. Moreover, based on a sample of 32 healthy adults, test–retest reliability for the tasks ranged from 0.86 to 0.94.18 Following the procedure of Li et al.,5 we employed the FB test to assess basic ToM, and used the FPR, IS, and VC tests to evaluate

1119 ToM and Social Functioning in TLE advanced ToM abilities. To minimize the load on memory, all ToM materials were presented to participants during the administration.5,18 The FB test comprises eight stories, based on the paradigm used in the studies by Wimmer and Perner.19 Each story is followed by a test question to assess whether participants can recognize that the characters have beliefs about the world that are different from their own perspectives. In addition, two control questions (e.g., “Where is the object really?” and “Where was the object in the beginning?”) were used to ensure that participants had understood and remembered the contents. Participants needed to pass both control questions to qualify for scoring on each trial. For each story, one point is given for each correct answer with a false belief. The total score for the FB test ranges from 0 to 8. The FPR test consists of 10 stories, all of which describe a situation where a speaker says something that is socially inappropriate.20 Each story is followed by three test questions intended to evaluate whether participants recognized the inappropriateness of the speaker’s remarks and realized that these remarks could have negative consequences for the listener that the speaker did not intend (a “faux pas”). A control question ensured that the participants had understood the story and were paying attention. After passing the control question, one point is given for each correct answer to the test questions. The total score for the FPR test ranges from 0 to 30. The IS test comprises five short stories with implied meaning, such as a joke, white lie, or pretend situation.21 Each story is followed by two questions to assess whether participants could understand the implied meaning in the story. The total score for the IS test ranges from 0 to 10. The VC test includes 10 funny cartoon pictures. Participants are shown the pictures one at a time, with two types of questions intended to assess their abilities to infer the characters’ mental states. The first question is open-ended (implicit form), asking participants why the picture is funny; the second question is presented in a more explicit manner (explicit form), asking what the motives of the character in each picture are. The total score for each type of question ranges from 0 to 20. Measurements of cognitive functions The Taiwanese version of the Wechsler Adult Intelligence Scale-Third edition (WAIS-III)22 was used to evaluate intellectual function. The Logic Memory subtest of the Taiwanese version of the WAIS-III23 and the Working Memory Index of the WAIS-III were employed to assess memory function. The Verbal Comprehension Index (VCI) score of the WAIS-III was used to evaluate verbal function. The Modified Card Sorting Test24 and the Semantic Association of Verbal Fluency,25 which consists of three different semantic categories (fruit, fish, and vegetables), were used to measure executive function. Spatial-perceptual function

was evaluated through the Perceptual Organization Index score of the WAIS-III. Finally, the Processing Speed Index score of the WAIS-III was used to assess psychomotor speed. Measurement of social functioning Social functioning was assessed by the Social and Occupational Functioning Scale for Epilepsy (SOFSE),11 which is a functional-based measurement and comprises 30 items in six dimensions: interpersonal relationships, communication, social engagement, leisure activities, instrumental living skill, and occupation. This test has demonstrated adequate psychometric properties: test–retest reliability (correlation coefficients range from 0.72 to 0.89), internal consistency (alpha coefficients range from 0.70 to 0.84), and criterion validity.11 The SOFSE total score is calculated as the mean of all dimension scores. The total scores for SOFSE including all dimensions ranges from 0 to 100, with higher values reflecting better social functioning.11 Inventory of psychiatric status The Taiwanese version of the Symptom Checklist-90Revised (SCL-90-R),26 which was originally developed by Derogatis,27 was employed to evaluate patients’ general psychiatric status. We used the Global Severity Index (GSI) as a measure of overall psychopathology. Higher GSI scores indicate more severe disturbance in a given psychopathologic dimension. Statistical analysis The TLE and HC groups were compared using an independent-sample t-test for parametric variables and a chisquare (v2) test for categorical variables. If the data violated the assumption of homogeneity of variance, the adjusted t and degree of freedom values of the WelchAspin test were used. Moreover, multiple regression analyses were performed to explore the relation between risk factors (independent variables) and SOFSE total and subscale scores (dependent variables). A stepwise multiple regression was used initially to determine the most significant independent variables (including ToM abilities, cognitive functions, psychiatric status, and seizure-related variables) that were expected to explain the association with the SOFSE total score. Determinants that were significantly associated with the outcome in the stepwise model (p-value < 0.05) were then included as potential covariates in a multiple regression analysis. As dependent variables, the six subscale scores of the SOFSE were processed separately; thus six separate multiple regression analyses were performed. The WAIS-III Full-Scale IQ (FSIQ) score was used in all regression analyses instead of its four composite index scores. Data processing and analysis were carried out using SPSS Version 12 (SPSS Inc., Chicago, IL, U.S.A.). Epilepsia, 56(7):1117–1123, 2015 doi: 10.1111/epi.13023

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Results Demographic and clinical seizure characteristics Sixty-seven patients were eligible for this study. As shown in Table 1, demographic variables did not differ between TLE and HC groups (p = 0.15–0.97). ToM and background neuropsychological findings The mean scores for each test are summarized in Table 2. In the FB and FPR tests, every participant correctly answered the control questions. As shown in Table 2, the independent-sample t-test revealed that patients with TLE had lower scores than the HC group on all four ToM tasks (p < 0.001). Except for the tests of executive (p = 0.06– 0.21) and spatial perceptual (p = 0.06) functions, group differences were also found in the other neurocognitive measures (p-values were either equal to 0.008 or

Theory of mind and social functioning in patients with temporal lobe epilepsy.

This study aimed to explore the effects of theory of mind (ToM) and related potential risk factors, including cognitive functions, psychiatric status,...
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