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Theory of Mind in Patients with Epilepsy: a Systematic Review and Meta-analysis

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Abstract

The ability to understand our own thoughts, intentions, beliefs and emotions and those of others (Theory of Mind; ToM) is a high-order social cognitive skill that is vital for social interaction and which has been found to be impaired in patients with epilepsy. Studies examining ToM in patients with epilepsy, however, have yielded inconsistent findings. The main aim of this study is to determine whether the magnitude of ToM deficits varies as a function of the site of epilepsy focus and/or the type of ToM task used. Electronic databases searches included Psychinfo, Medline/PubMed and EMBASE. Studies were included if they examined a group of patients with epilepsy and a group of healthy controls, reported original research, were published in the English language in peer reviewed journals, and used one of five empirically validated measures of ToM: False Belief, Reading the Mind in the Eyes Task (RMET), Faux-pas, Strange Stories, Cartoon ToM vignettes. Twelve studies were identified, ten included adults and two included children with epilepsy. Findings revealed marked ToM deficits in adults with focal seizures emanating from core brain regions underpinning ToM: temporal and frontal lobes (frontal lobe epilepsy, FLE; temporal lobe epilepsy, TLE), but not in adults with focal seizures outside the temporal and frontal lobes (extra-TLE/FLE). ToM deficits were also observed in children with generalised seizures (idiopathic generalised epilepsy, IGE). ToM deficits were documented across ToM tasks. In conclusion, ToM deficits represent a robust finding in adults with frontal and temporal epilepsy, but are also found in children with generalised seizures. Further research into ToM is needed, especially in children with epilepsy as early ToM may have cumulative, negative effects on development of social skills that continues into adulthood.

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Authors and Affiliations

  1. School of Psychology, The University of Sydney, Brennan McCallum (A18), Sydney, NSW, 2006, Australia

    Elizabeth Stewart & Suncica Lah

  2. ARC Centre of Excellence in Cognition and its Disorders, Sydney, NSW, Australia

    Elizabeth Stewart & Suncica Lah

  3. Murdoch Children’s Research Institute, Royal Children’s Hospital, Melbourne, Australia

    Cathy Catroppa

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  2. Cathy Catroppa
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Appendix 1

Appendix 1

Details of Quality Rating Items

The following 17 items from the Downs and Black checklist (1998) were employed to assess quality of included studies: 1. Is the hypothesis/aim/objective of the study clearly described? 2. Are the main outcomes to be measured clearly described in the Introduction or Methods section? 3. Are the characteristics of the patients included in the study described clearly? 5. Are the distributions of principal confounders in each group of subjects to be compared described clearly? 6. Are the main findings of the study described clearly? 7. Does the study provide estimates of the random variability in the data for the main outcomes? 9. Have the characteristics of patients lost to follow-up been described? 10. Have actual probability values been reported (for example, 0.035 rather than < 0.05) for the main outcomes except where the probability value is less than 0.001? 11. Were the subjects asked to participate in the study representative of the entire population from which they were recruited? 16. If any of the results of the study were based on ‘data dredging’, was this made clear? 18. Were the statistical tests used to assess the main outcomes appropriate? 20. Were the main outcome measures used accurate (valid and reliable)? 21. Were the patients in different groups recruited from the same population? 22. Were study subjects recruited over the same period of time? 25. Was there adequate adjustment for confounding in the analyses from which the main findings were drawn? 26. Were losses of patients to follow-up taken into account? 27: Did the study have sufficient power to detect a clinically important effect where the probability value for a difference being due to chance is less than 5 %?

Details of Theory of Mind Tasks

Five types of ToM tasks were included in this review. These tasks were selected based on a recent review by Henry et al. (2015), which identified the empirically validated and psychometrically sound behavioural measures of ToM.

False Belief Tasks

Participants are read aloud short stories about a character who has a mistaken belief (i.e., a belief that is inconsistent with their own beliefs and/or or out of line with reality). The participant must correctly infer the mental state of the character by using their cognitive ToM skills. In the simplest version of these tasks, participants must make inferences about the mistaken beliefs of a character with regard to real events (first-order false belief). In more complicated versions of the task, participants must make meta-cognitive inferences: attributing the false belief of one person based on the thoughts of another (second-order false belief). First-order and second-order false belief are commonly grouped together to measure false belief (i.e., ToM) performance. Numerous versions of this task have been developed, which are mostly based on the initial task done by (Wimmer and Perner 1983). This task assesses early cognitive ToM (Henry et al. 2015).

Reading the Mind in the Eyes Test (RMET)

Participants are presented with a series of photographs of the eye regions of faces and are asked to select the emotion label that best depicts how a character is feeling. The Reading in the Mind in the Eyes Task (RMET), designed by Baron-Cohen, is the most commonly used of these measures and contains 36 photographs, presented sequentially with four emotion labels for each (Baron‐Cohen et al. 2001). Adaptations of this task have been created for participants from different cultural groups (Jiang et al. 2014). The RMET assesses early affective ToM (Henry et al. 2015).

Faux-Pas Tasks

Participants are read aloud stories that contain a social faux-pas (i.e., scenario in which a character says or does something unintended that may impact upon another characters feelings). Following each story, participants are asked a series of questions that assess their ability to detect the faux-pas (i.e., Did someone say something they shouldn’t have said or something awkward? Who said something they shouldn’t have said or something awkward?); their cognitive ToM (Why do you think he or she said it?); and their affective ToM (How do you think X felt when Y said that?). Each participant obtains a total ToM score by summing responses across questions on the faux-pas stories. They also obtain a score representing their ability to detect the faux pas (Faux-pas hits; calculated by summing responses to the question 1 on each story). Participants are also read control stories that do not contain faux-pas’ and are asked the first comprehension question to assess their ability to rule out non-existent faux-pas and obtain a score representing their ability to rule out non-existant faux-pas (Faux-pas correct rejections; calculated by summing responses to the first question asked on each of the non faux-pas stories). This task assessed advanced ToM (cognitive and affective components) (Henry et al. 2015).

Strange Stories

Participants are read aloud stories involving an interaction between two people, in which characters say or do something that they do not literally mean. The stories contain jokes, metaphors, double bluff, mistakes, persuasion, white lies and/or deception. Participants are asked a series of questions assessing their ability to comprehend the implicit meaning of the story (What it true, what X said?) and then to make inferences about characters’ thoughts, beliefs, intentions and emotional states (Why did X say it?). The original version of this task contains 24 short stories, however shortened versions have been used in recent studies (Happé 1994). This task assesses advanced ToM (cognitive and affective components) (Henry et al. 2015).

Cartoon ToM Tasks

Participants are shown a series of single frame cartoons in which humour depends on what a character mistakenly thought or did not know. Participants are typically asked two questions. 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. Some studies have only used the implicit form of the question, however, to receive a correct response, participants must accurately infer what is funny in the story with reference to the thoughts, beliefs, intentions and feelings of characters. This task assesses advanced ToM (cognitive and affective component).

Table 7

Table 7 Studies excluded from meta-analysis
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Stewart, E., Catroppa, C. & Lah, S. Theory of Mind in Patients with Epilepsy: a Systematic Review and Meta-analysis. Neuropsychol Rev 26, 3–24 (2016). https://doi.org/10.1007/s11065-015-9313-x

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