Top

Published in:

01-03-2016 | Review

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

Authors: Elizabeth Stewart, Cathy Catroppa, Suncica Lah

Published in: Neuropsychology Review | Issue 1/2016

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.

Available only for authorised users

Amlerova, J., Cavanna, A., Bradac, O., Javurkova, A., Raudenska, J., & Marusic, P. (2014). Emotion recognition and social cognition in temporal lobe epilepsy and the effect of epilepsy surgery. Epilepsy & Behavior, 36, 86–89.CrossRef

Amodio, D., & Frith, C. (2006). Meeting of minds: the medial frontal cortex and social cognition. Nature Reviews Neuroscience, 7(4), 268–277.CrossRefPubMed

Anderson, V., Brown, S., Newitt, H., & Hoile, H. (2011). Long-term outcome from childhood traumatic brain injury: intellectual ability, personality, and quality of life. Neuropsychology, 25(2), 176.CrossRefPubMed

Anderson, V., Catroppa, C., Morse, S., Haritou, F., & Rosenfeld, J. V. (2009). Intellectual outcome from preschool traumatic brain injury: a 5-year prospective, longitudinal study. Pediatrics, 124(6), e1064–e1071.CrossRefPubMed

Anderson, V., & Moore, C. (1995). Age at injury as a predictor of outcome following pediatric head injury: a longitudinal perspective. Child Neuropsychology, 1(3), 187–202.CrossRef

Astington, J. W., & Jenkins, J. M. (1995). Theory of mind development and social understanding. Cognition & Emotion, 9(2–3), 151–165.CrossRef

Astington, J. W., & Jenkins, J. M. (1999). A longitudinal study of the relation between language and theory of mind development. Developmental Psychology, 35, 1311–1320.CrossRefPubMed

Astington, J. W., Pelletier, J., & Homer, B. (2002). Theory of mind and epistemological development: the relation between children’s second-order false-belief understanding and their ability to reason about evidence. New Ideas in Psychology, 20(2), 131–144.CrossRef

Baron-Cohen, S., O’Riordan, M., Jones, R., Stone, V., & Plaisted, K. (1999). A new test of social sensitivity: detection of faux pas in normal children and children with Asperger syndrome. Journal of Autism and Developmental Disorders, 29, 407–418.CrossRefPubMed

Baron‐Cohen, S., Jolliffe, T., Mortimore, C., & Robertson, M. (1997). Another advanced test of theory of mind: evidence from very high functioning adults with autism or Asperger syndrome. Journal of Child Psychology and Psychiatry, 38(7), 813–822.CrossRefPubMed

Baron‐Cohen, S., Wheelwright, S., Hill, J., Raste, Y., & Plumb, I. (2001). The “Reading the Mind in the Eyes” test revised version: a study with normal adults, and adults with Asperger syndrome or high‐functioning autism. Journal of Child Psychology and Psychiatry, 42(2), 241–251.CrossRefPubMed

Bauminger-Zviely, N. (2013). False-belief task Encyclopedia of autism spectrum disorders (pp. 1249–1249): Springer.

Black, L., Schefft, B., Howe, S. R., Szaflarski, J. P., Yeh, H. S., & Privitera, M. D. (2010). The effect of seizures on working memory and executive functioning performance. Epilepsy & Behavior, 17(3), 412–419.CrossRef

Bird, C. M., Castelli, F., Malik, O., Frith, U., & Husain, M. (2004). The impact of extensive medial frontal lobe damage on ‘Theory of Mind’and cognition. Brain, 127(4), 914–928.CrossRefPubMed

Borenstein, M., Hedges, L., Higgins, J., & Rothstein, H. (2005). Comprehensive meta-analysis version 2 (p. 104). Englewood: Biostat.

Borenstein, M., Hedges, L., Higgins, J., & Rothstein, H. (2009). Introduction to meta-analysis. Chichester: Wiley.CrossRef

Broicher, S. D., Kuchukhidze, G., Grunwald, T., Kramer, G., Kurthen, M., & Jokeit, H. (2012). “Tell me how do I feel”–Emotion recognition and theory of mind in symptomatic mesial temporal lobe epilepsy. Neuropsychologia, 50(1), 118–128.CrossRefPubMed

Brune, M. (2005). Emotion recognition, ‘theory of mind’,and social behavior in schizophrenia. Psychiatry Research, 133(2), 135–147.CrossRefPubMed

Bull, R., Phillips, L. H., & Conway, C. A. (2008). The role of control functions in mentalizing: dual-task studies of theory of mind and executive function. Cognition, 107(2), 663–672.CrossRefPubMed

Caplan, R., Sagun, J., Siddarth, P., Gurbani, S., Koh, S., Gowrinathan, R., & Sankar, R. (2005). Social competence in pediatric epilepsy: insights into underlying mechanisms. Epilepsy & Behavior, 6(2), 218–228.CrossRef

Carlson, S. M., & Moses, L. J. (2001). Individual differences in inhibitory control and children’s theory of mind. Child Development, 72(4), 1032–1053.CrossRefPubMed

Carlson, S. M., Moses, L. J., & Breton, C. (2002). How specific is the relation between executive function and theory of mind? Contributions of inhibitory control and working memory. Infant and Child Development, 11(2), 73–92.CrossRef

Cavallini, E., Lecce, S., Bottiroli, S., Palladino, P., & Pagnin, A. (2013). Beyond false belief: theory of mind in young, young-old, and old-old adults. The International Journal of Aging and Human Development, 76(3), 181–198.CrossRefPubMed

Cohen, J. D. (1988). Statistical power analysis for the behavioral sciences. Hillsdale: Lawrence Earlbaum Associates.

Culhane-Shelburne, K., Chapieski, L., Hiscock, M., & Glaze, D. (2002). Executive functions in children with frontal and temporal lobe epilepsy. Journal of the International Neuropsychological Society, 8(05), 623–632.CrossRefPubMed

Downs, S. H., & Black, N. (1998). The feasibility of creating a checklist for the assessment of the methodological quality both of randomised and non-randomised studies of health care interventions. Journal of Epidemiology and Community Health, 52(6), 377–384.PubMedCentralCrossRefPubMed

Dumontheil, I., Apperly, I. A., & Blakemore, S. J. (2010). Online usage of theory of mind continues to develop in late adolescence. Developmental Science, 13(2), 331–338.CrossRefPubMed

Eddy, C. M., Rickards, H. E., & Cavanna, A. E. (2011). The cognitive impact of antiepileptic drugs. Therapeutic Advances in Neurological Disorders, 4(6), 385–407.PubMedCentralCrossRefPubMed

Egger, M., Smith, G. D., Schneider, M., & Minder, C. (1997). Bias in meta-analysis detected by a simple, graphical test. BMJ, 315(7109), 629–634.PubMedCentralCrossRefPubMed

Engel, J. (2001). A proposed diagnostic scheme for people with epileptic seizures and with epilepsy: report of the ILAE Task Force on Classification and Terminology. Epilepsia, 42(6), 796–803.CrossRefPubMed

Farrant, A., Morris, R. G., Russell, T., Elwes, R., Akanuma, N., Alarcón, G., & Koutroumanidis, M. (2005). Social cognition in frontal lobe epilepsy. Epilepsy & Behavior, 7(3), 506–516.CrossRef

Fiske, S., & Taylor, S. (1991). Social cognition (2nd ed., pp. 16–15). NY: McGraw-Hill.

Fiske, S. T., & Taylor, S. E. (2013). Social cognition: From brains to culture: Sage.

Fournier, N., Calverley, K., Wagner, J., Poock, J., & Crossley, M. (2008). Impaired social cognition 30 years after hemispherectomy for intractable epilepsy: the importance of the right hemisphere in complex social functioning. Epilepsy & Behavior, 12(3), 460–471.CrossRef

Frith, C. D. (2007). The social brain? Philosophical Transactions of the Royal Society, B: Biological Sciences, 362(1480), 671–678.PubMedCentralCrossRef

Frith, C. D., & Frith, U. (1999). Interacting minds-a biological basis. Science, 286(5445), 1692–1695.CrossRefPubMed

Gallagher, H. L., & Frith, C. D. (2003). Functional imaging of ‘theory of mind’. Trends in Cognitive Sciences, 7(2), 77–83.CrossRefPubMed

Gallagher, H. L., Happé, F., Brunswick, N., Fletcher, P. C., Frith, U., & Frith, C. D. (2000). Reading the mind in cartoons and stories: an fMRI study of ‘theory of mind’ in verbal and nonverbal tasks. Neuropsychologia, 38(1), 11–21.

Gelžinienė, G., Jurkevičienė, G., Marmienė, V., Adomaitienė, V., & Endzinienė, M. (2010). Executive functions in adolescents with idiopathic generalized epilepsy. Medicina (Kaunas, Lithuania), 47(6), 313–319.

Genizi, J., Shamay-Tsoory, S. G., Shahar, E., Yaniv, S., & Aharon-Perez, J. (2012). Impaired social behavior in children with benign childhood epilepsy with centrotemporal spikes. Journal of Child Neurology, 27(2), 156–161.CrossRefPubMed

Giovagnoli, A. R. (2014). The importance of theory of mind in epilepsy. Epilepsy & Behavior, 39, 145–153.CrossRef

Giovagnoli, A. R., Canafoglia, L., Reati, F., Raviglione, F., & Franceschetti, S. (2009). The neuropsychological pattern of Unverricht–Lundborg disease. Epilepsy Research, 84(2), 217–223.CrossRefPubMed

Giovagnoli, A. R., Franceschetti, S., Reati, F., Parente, A., Maccagnano, C., Villani, F., & Spreafico, R. (2011). Theory of mind in frontal and temporal lobe epilepsy: cognitive and neural aspects. Epilepsia, 52(11), 1995–2002.CrossRefPubMed

Giovagnoli, A. R., Parente, A., Villani, F., Franceschetti, S., & Spreafico, R. (2013). Theory of mind and epilepsy: what clinical implications? Epilepsia, 54(9), 1639–1646.CrossRefPubMed

Gomez-Ibañez, A., Urrestarazu, E., & Viteri, C. (2014). Recognition of facial emotions and identity in patients with mesial temporal lobe and idiopathic generalized epilepsy: an eye-tracking study. Seizure, 23(10), 892–898.CrossRefPubMed

Happé, F. (1994). An advanced test of theory of mind: understanding of story characters’ thoughts and feelings by able autistic, mentally handicapped, and normal children and adults. Journal of Autism and Developmental Disorders, 24(2), 129–154.CrossRefPubMed

Henry, J., Cowan, D., Lee, T., & Sachdev, P. (2015). Recent trends in testing social cognition. Current Opinion in Psychiatry, 28(2), 133–140.PubMed

Henry, J. D., Phillips, L. H., Crawford, J. R., Ietswaart, M., & Summers, F. (2006). Theory of mind following traumatic brain injury: the role of emotion recognition and executive dysfunction. Neuropsychologia, 44(10), 1623–1628.CrossRefPubMed

Higgins, J., & Green, S. (2008). Cochrane handbook for systematic reviews of interventions. Version 5.0.1.: The Cochrane Collaboration.

Hrabok, M., Dykeman, J., Sherman, E. M. S., & Wiebe, S. (2013). An evidence-based checklist to assess neuropsychological outcomes of epilepsy surgery: How good is the evidence? Epilepsy & Behavior, 29(3), 443–448.CrossRef

Hughes, C. (1998). Executive function in preschoolers: links with theory of mind and verbal ability. British Journal of Developmental Psychology, 16(2), 233–253.CrossRef

Hynes, C. A., & Mar, R. A. (2009). A case study of long-term cognitive and social functioning following a right temporal lobectomy in infancy. Neurocase, 15(1), 37–46.CrossRef

Jiang, Y., Hu, Y., Wang, Y., Zhou, N., Zhu, L., & Wang, K. (2014). Empathy and emotion recognition in patients with idiopathic generalized epilepsy. Epilepsy & Behavior, 37, 139–144.CrossRef

Kalbe, E., Schlegel, M., Sack, A. T., Nowak, D. A., Dafotakis, M., Bangard, C., & Kessler, J. (2010). Dissociating cognitive from affective theory of mind: a TMS study. Cortex, 46(6), 769–780.CrossRefPubMed

Kaland, N., Møller-Nielsen, A., Smith, L., Mortensen, E. L., Callesen, K., & Gottlieb, D. (2005). The strange stories test. European Child & Adolescent Psychiatry, 14(2), 73–82.CrossRef

Kim, Y. T., Kwon, D. H., & Chang, Y. (2011). Impairments of facial emotion recognition and theory of mind in methamphetamine abusers. Psychiatry Research, 186(1), 80–84.CrossRefPubMed

Kirsch, H. E. (2006). Social cognition and epilepsy surgery. Epilepsy & Behavior, 8(1), 71–80.CrossRef

Kwan, P., & Brodie, M. J. (2001). Neuropsychological effects of epilepsy and antiepileptic drugs. The Lancet, 357(9251), 216–222.CrossRef

Ladegaard, N., Larsen, E. R., Videbech, P., & Lysaker, P. H. (2014). Higher-order social cognition in first-episode major depression. Psychiatry Research, 216(1), 37–43.CrossRefPubMed

Lew, A. R., Lewis, C., Lunn, J., Tomlin, P., Basu, H., Roach, J., & Martland, T. (2015). Social cognition in children with epilepsy in mainstream education. Developmental Medicine & Child Neurology, 57(1), 53–59.CrossRef

Li, Y., Chiu, M., Yeh, Z., Liou, H., Cheng, T., & Hua, M. (2013). Theory of mind in patients with temporal lobe epilepsy. Journal of the International Neuropsychological Society, 19(05), 594–600.CrossRefPubMed

Martín-Rodríguez, J. F., & León-Carrión, J. (2010). Theory of mind deficits in patients with acquired brain injury: a quantitative review. Neuropsychologia, 48(5), 1181–1191.CrossRefPubMed

Miller, M. B., Sinnott-Armstrong, W., Young, L., King, D., Paggi, A., Fabri, M., & Gazzaniga, M. S. (2010). Abnormal moral reasoning in complete and partial callosotomy patients. Neuropsychologia, 48(7), 2215–2220.PubMedCentralCrossRefPubMed

Milligan, K., Astington, J. W., & Dack, L. A. (2007). Language and theory of mind: meta‐analysis of the relation between language ability and false‐belief understanding. Child Development, 78(2), 622–646.CrossRefPubMed

Mo, S., Su, Y., Chan, R. C., & Liu, J. (2008). Comprehension of metaphor and irony in schizophrenia during remission: the role of theory of mind and IQ. Psychiatry Research, 157(1), 21–29.CrossRefPubMed

Moher, D., Liberati, A., Tetzlaff, J., & Altman, D. G. (2009). Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Annals of Internal Medicine, 151(4), 264–269.CrossRefPubMed

Mutter, B., Alcorn, M. B., & Welsh, M. (2006). Theory of mind and executive function: working-memory capacity and inhibitory control as predictors of false-belief task performance. Perceptual and Motor Skills, 102(3), 819–835.CrossRefPubMed

Nolan, M. A., Redoblado, M. A., Lah, S., Sabaz, M., Lawson, J. A., Cunningham, A. M., & Bye, A. M. (2003). Intelligence in childhood epilepsy syndromes. Epilepsy Research, 53(1), 139–150.CrossRefPubMed

Olson, I. R., McCoy, D., Klobusicky, E., & Ross, L. A. (2012). Social cognition and the anterior temporal lobes: a review and theoretical framework. Social cognitive and affective neuroscience, 8(2), 123–133.

Olson, I. R., Plotzker, A., & Ezzyat, Y. (2007). The enigmatic temporal pole: a review of findings on social and emotional processing. Brain, 130(7), 1718–1731.CrossRefPubMed

Onishi, K. H., & Baillargeon, R. (2005). Do 15-month-old infants understand false beliefs? Science, 308(5719), 255–258.PubMedCentralCrossRefPubMed

Park, S., & Kwon, S. (2008). Cognitive effects of antiepileptic drugs. Journal of Clinical Neurology, 4(3), 99–106.PubMedCentralCrossRefPubMed

Perner, J., & Lang, B. (1999). Development of theory of mind and executive control. Trends in Cognitive Sciences, 3(9), 337–344.CrossRefPubMed

Pickup, G. J. (2008). Relationship between theory of mind and executive function in schizophrenia: a systematic review. Psychopathology, 41(4), 206–213.CrossRefPubMed

Pons, F., Harris, P. L., & de Rosnay, M. (2004). Emotion comprehension between 3 and 11 years: developmental periods and hierarchical organization. European Journal of Developmental Psychology, 1(2), 127–152.CrossRef

Rantanen, K., Eriksson, K., & Nieminen, P. (2012). Social competence in children with epilepsy—a review. Epilepsy & Behavior, 24(3), 295–303.CrossRef

Rajkumar, A. P., Yovan, S., Raveendran, A. L., & Russell, P. S. (2008). Can only intelligent children do mind reading: the relationship between intelligence and theory of mind in 8 to 11 years old. Behavioral and Brain Functions, 4(51), 1–7.

Richard-Mornas, A., Mazzietti, A., Koenig, O., Borg, C., Convers, P., & Thomas-Antérion, C. (2014). Emergence of hyper empathy after right amygdalohippocampectomy. Neurocase, 20(6), 666–670.

Saxe, R., & Kanwisher, N. (2003). People thinking about thinking people: the role of the temporo-parietal junction in “theory of mind”. NeuroImage, 19(4), 1835–1842.CrossRefPubMed

Saxe, R., & Wexler, A. (2005). Making sense of another mind: the role of the right temporo-parietal junction. Neuropsychologia, 43(10), 1391–1399.CrossRefPubMed

Schacher, M., Winkler, R., Grunwald, T., Kraemer, G., Kurthen, M., Reed, V., & Jokeit, H. (2006). Mesial temporal lobe epilepsy impairs advanced social cognition. Epilepsia, 47(12), 2141–2146.CrossRefPubMed

Shaw, P., Lawrence, E., Bramham, J., Brierley, B., Radbourne, C., & David, A. (2007). A prospective study of the effects of anterior temporal lobectomy on emotion recognition and theory of mind. Neuropsychologia, 45(12), 2783–2790.CrossRefPubMed

Shaw, P., Lawrence, E., Radbourne, C., Bramham, J., Polkey, C., & David, A. (2004). The impact of early and late damage to the human amygdala on ‘theory of mind’ reasoning. Brain, 127(7), 1535–1548.

Sodian, B., & Kristen, S. (2010). Theory of mind Towards a theory of thinking (pp. 189–201): Springer.

Song, H. J., Onishi, K. H., Baillargeon, R., & Fisher, C. (2008). Can an agent’s false belief be corrected by an appropriate communication? Psychological reasoning in 18-month-old infants. Cognition, 109(3), 295–315.PubMedCentralCrossRefPubMed

Sosa, J. T. R., Ojeda, M. A., & del Rosario, L. R. (2011). Theory of mind, facial recognition and emotional processing in schizophrenia. Revista de Psiquiatría y Salud Mental (English Edition), 4(1), 28–37.

Stone, V., Baron-Cohen, S., Calder, A., Keane, J., & Young, A. (2003). Acquired theory of mind impairments in individuals with bilateral amygdala lesions. Neuropsychologia, 41(2), 209–220.

Sullivan, J. E., & Dlugos, D. J. (2004). Idiopathic generalized epilepsy. Current Treatment Options in Neurology, 6(3), 231–242.CrossRefPubMed

Suurmeijer, T. P., Reuvekamp, M. F., & Aldenkamp, B. P. (2001). Social functioning, psychological functioning, and quality of life in epilepsy. Epilepsia, 42(9), 1160–1168.CrossRefPubMed

Wang, W. H., Shih, Y. H., Yu, H. Y., Yen, D. J., Lin, Y. Y., Kwan, S. Y., Hua, M. S. (2015). Theory of mind and social functioning in patients with temporal lobe epilepsy. Epilepsia, 56(7), 1117–1123.

Wellman, H. M., Cross, D., & Watson, J. (2001). Meta-analysis of theory-of-mind development: The truth about false belief. Child development, 72(3), 655–684.

Wimmer, H., & Perner, J. (1983). Beliefs about beliefs: representation and constraining function of wrong beliefs in young children’s understanding of deception. Cognition, 13(1), 103–128.CrossRefPubMed

Title: Theory of Mind in Patients with Epilepsy: a Systematic Review and Meta-analysis
Authors: Elizabeth Stewart
Cathy Catroppa
Suncica Lah
Publication date: 01-03-2016
Publisher: Springer US
Published in: Neuropsychology Review / Issue 1/2016
Print ISSN: 1040-7308
Electronic ISSN: 1573-6660
DOI: https://doi.org/10.1007/s11065-015-9313-x

At a glance: The STEP trials

Springer Medicine

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

Abstract

At a glance: The STEP trials

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 1/2016

The Combined Effect of Neuropsychological and Neuropathological Deficits on Instrumental Activities of Daily Living in Older Adults: a Systematic Review

Multisensory Stimulation to Improve Low- and Higher-Level Sensory Deficits after Stroke: A Systematic Review

Editorial

A Comparison of Structural Brain Imaging Findings in Autism Spectrum Disorder and Attention-Deficit Hyperactivity Disorder

A Systematic Review and Meta-analysis of Neuroimaging in Oppositional Defiant Disorder (ODD) and Conduct Disorder (CD) Taking Attention-Deficit Hyperactivity Disorder (ADHD) Into Account