Lesion localization and performance on Theory of Mind tests in stroke survivors: a systematic review

Bomfim, Ana Julia de Lima; Ferreira, Bianca Letícia Cavalmoretti; Rodrigues, Guilherme Riccioppo; Pontes Neto, Octavio Marques; Chagas, Marcos Hortes Nisihara

doi:10.1590/0101-60830000000250

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Review Article • Arc. Clin. Psychiatr. 47 (5) • Sep-Oct 2020 • https://doi.org/10.1590/0101-60830000000250 copy

Lesion localization and performance on Theory of Mind tests in stroke survivors: a systematic review

Authorship SCIMAGO INSTITUTIONS RANKINGS

Abstract

Background:

Theory of Mind (ToM) is the ability to attribute mental states to oneself and others. Individuals with a brain lesion following a stroke exhibit a compromised ability to perform ToM tasks.

Objective:

To analyze studies that evaluated ToM in stroke survivors considering the lesion localization and performance on ToM tests.

Methods:

The searches were carried out until November 28, 2018, using the following search terms: “social cognition” or “Theory of Mind” and “stroke”. Searches were conducted in the PubMed, PsycInfo, Web of Science and Scopus data bases. The initial search led to the retrieval of 425 articles. After the exclusion of duplicates and the analysis of the titles, abstracts and full texts, 20 articles were selected for the present review.

Results:

The studies showed that patients with lesion in the right hemisphere present lower performance on ToM tasks compared to those with lesion in the left hemisphere. In addition, patients with lesion in the right hemisphere presented significant impairment in the performance on ToM tasks compared to healthy individuals. Furthermore, the studies that evaluated lesions in specific regions such as temporal lobe, prefrontal cortex, posterior parietal cortex, and temporo-parietal junction, indicated a significant deficit in ToM performance of these patients compared to healthy individuals.

Discussion:

This review showed that stroke survivors have a poor performance on ToM tasks. The right hemisphere and prefrontal cortex seem to be associated with the deficit of this ability.

Keywords:
Social cognition; Theory of Mind; stroke

Authors/Year	Sample	Sex (M:F)	Age	Education (years)	Lesion site	Time post stroke	ToM assessment tool	Main findings
Apperly et al., 2004²⁰20. Apperly IA, Samson D, Chiavarino C, Humphreys GW. Frontal and temporo-parietal lobe contributions to theory of mind: neuropsychological evidence from a false-belief task with reduced language and executive demands. J Cogn Neurosci. 2004;16(10):1773-84.	12	SP: 10:2	SP: 55.2 (±13.5)	–	Frontal Parietal temporal lobes.	8 (±4.2) years	False Belief Tasks	Lesions in the temporoparietal region impair the ability to perform the False Beliefs task.
Besharati et al., 2016¹⁶16. Besharati S, Forkel SJ, Kopelman M, Solms M, Jenkinson PM, Fotopoulou A, et al. Mentalizing the body: spatial and social cognition in anosognosia for hemiplegia. Brain. 2016;139(3):971-85.	45	AHP: 6:9 HP: 8:7 HC: 9:7	AHP: 73.00 (±22.0) HP: 68.00 (±27.0) HC: 71.00 (±7.0)	AHP: 12.00 (± 3.0) HP: 12.00 (±3.0) HC: 13.00 (±6.0)	Right hemisphere	–	Adapted Stories inference of beliefs, intentions and emotions	Anosognosia group performed worse than both control groups when having to perform tasks from a third versus a first person perspective.
Champagne-Lavau et al., 2009²⁶26. Champagne-Lavau M, Joanette Y. Pragmatics, theory of mind and executive functions after a right-hemisphere lesion: Different patterns of deficits. J Neurolinguistics. 2009;22(5):413-26.	30	RHL: 6:9 HC: 7:8	RHL: 60.9 (±11.7) HC: 60.7 (±12.8)	RHL: 11.7 (±3.1) HC: 11.7(±3.2)	Right hemisphere	1-4 months	False belief task	Patients with right frontal and internal capsule lesions presented pragmatic and ToM deficits compared to HC group.
Griffin et al., 2006¹⁹19. Griffin R, Friedman O, Ween J, Winner E, Happé F, Brownell H. Theory of mind and the right cerebral hemisphere: Refining the scope of impairment. Laterality. 2006;11(3):195-225.	31	RHL: 6:5 HC: 7:13	RHL: 61.0 HC: 66.0	RHL:14.0 HC: 15.0	Right hemisphere	–	A graded (first order, second order) ToM task with non-mentalistic control questions	RHL patients differed from non-brain-damaged controls in the ability to attribute second order intentional states.
Hamilton et al., 2017³3. Hamilton J, Radlak B, Morris PG, Phillips LH. Theory of Mind and Executive Functioning Following Stroke. Arch Clin Neuropsychol. 2017;32(5):507-18.	70	RHL: 7:8 LHL: 7:8 HC: 18:22	RHL: 67.80 (±14.1) LHL: 67.73 (±9.9) HC: 66.63 (±12.7)	RHL: 11.73 (±3.0) LHL:10.87 (±2.2) HC: 12.13(± 3.5)	Left hemisphere and Right hemisphere	RHL: 71.0 (±32.4) days LHL: 77.47 (±32.4) days	RMET and Eyes control task	The results showed that stroke participants with RHL were significantly more impaired on the visual RMET than those with LHL, who performed similarly to healthy controls.
Happé et al., 1999¹⁷17. Happé F, Brownwll H, Winner E. Acquired theory of mind impairments following stroke. Cognition. 1999;70(3):211-40.	38	RHL: 5:9 LHL: 4:1 HC: 9:10	RHL: 64 LHL: 67 HC: 73	RHL: 13.4 LHL: 12.6 HC: 14.6	Right hemisphere and Left hemisphere	RHL: 4 months to 23 years LHL: 12 months to 21 years	ToM stories and non- mental stories.	RHL patients showed evidence of ToM impairment compared to LHL patients and healthy controls.
Humphreys and Bedford, 2011²³23. Humphreys GW, Bedford J. The relations between joint action and theory of mind: a neuropsychological analysis. Exp Brain Res. 2011;211(34):357-69.	24	PPC/TP: 4:2FL: 6:0 LC: 6:0 HC: 4:2	PPC/TPJ: 68.33(±6.3) FL: 63.5 (±14.2) LC: 56.16 (±14.2) HC: 67.5	–	Posterior parietal cortex and Temporoparietal junction	–	Social Simon	Patients with brain injuries present impairment on ToM tasks related to the capacity to respond to social stimuli.
Mah et al., 2004²⁷27. Mah L, Arnold MC, Grafman J. Impairment of social perception associated with lesions of the prefrontal cortex. Am J Psychiatry. 2004;161(7):1247-55.	64	SP: 30:3 HC: 23:8	SP: 52.5 (±7.5) HC: 54.5 (±9.8)	SP: 14.1 (±2.5) HC: 14.9 (±2.0)	Prefrontal cortex	–	Interpersonal Perception Task	All patients showed poorer insight into their deficits, relative to healthy volunteers.
Martin and Mcdonald, 2006²¹21. Martin I, Mcdonald S. That can't be right! What causes pragmatic language impairment following right hemisphere damage? Brain Impairment. 2006;7(3):202-11.	42	RHL: 13:8 HC: 6:15	RHL: 69.2 (±14.8) HC: 68.5 (±14.7)	–	Right hemisphere	5.7 months	Test of ToM and Pragmatic Ability	Patients with RHL demonstrated significant difficulty on tasks that used the social context to interpret pragmatic inferences.
Pluta et al., 2017⁴4. Pluta A, Gawron N, Sobańska M, Wójcik AD, Łojek E. The nature of the relationship between neurocognition and theory of mind impairments in stroke patients. Neuropsychology. 2017;31(6):666-81.	80	RHL: 15:14 LHL: 12:12 BL: 5:0 HC: 9:13	RHL: 57.7 (±13) LHL: 60.2 (±10) BL: 45.5 (±19.8) HC: 55.4 (±10)	RHL: <12: 18/ >12: 9 LHL: <12: 10 / >12: 14 BL: <12: 3 / >12: 2 HC: <12: 12 / >12: 10	Left hemisphere, right hemisphere and bilateral	RHL: 24.8 (±35.4) months LHL: 28.4 (±28.1) months BL: 13 (±15.5) months	18 short vignettes (false beliefs, sarcasm, white lie)	The results showed that there were no differences between RHD, LHD, and BD patients in any of the ToM tasks. Patient group demonstrated impaired performance on all ToM tasks compared to a control group.
Roca et al., 2013¹⁴14. Roca M, Gleichgerrcht E, Abáñez A, Torralva T, Manes F. Cerebellar stroke impairs executive functions but not theory of mind. J Neuropsychiatry Clin Neurosci. 2013;25(1):E48-9.	11	9:2	50.6 (±12.1)	12.5 (±2.9)	–	–	The Faux Pas task	Patients with cerebellar strokes did not show impairment on the test.
Shamay-Tsoory et al., 2005¹⁵15. Shamay-Tsoory SG, Tomer R, Berger BD, Goldsher DMD, Aharon-Peretz JMD. Impaired “affective theory of mind” is associated with right ventromedial prefrontal damage. Cogn Behav Neurol. 2005;18(1):55-67.	52	FL: 20:6 PL: 8:5 HC: 10:3	FL: 34.12 (±14.0) PL: 40.46 (±5.38) HC: 34.12 (±12.59)	FL: 12.46 (±1.9) PL: 12.9 (±2.1) HC: 14.4 (±3.4)	Prefrontal cortex and posterior lesions	6 months, except one patient who was assessed 3 months after trauma	false belief task, detection of irony and identifying social faux pas	Lesions in the right ventromedial area were associated with more severe ToM deficit compared with patients with posterior lesions and normal control subjects.
Siegal et al., 1996¹³13. Siegal M, Carrington J, Radel M. Theory of mind and pragmatic understanding following right hemisphere damage. Brain Lang. 1996;53(1): 40-50.	28	RHL: 7:10 LHL: 8:3	RHL: 69.2 (±10.9) LHL: 70.3 (±9.7)	RHL: 8.6 LHL: 8.2	Right hemisphere and Left hemisphere	RHL: 1-24 months LHL: 1-68 months	False belief and True Belief task	Patients with RHL have difficulties understanding the false beliefs tasks.
Surian and Siegal, 2001¹⁸18. Surian L, Siegal M. Sources of performance on theory of mind tasks in right hemisphere-damaged patients. Brain Lang. 2001;78(2):224-32.	64	RHL: 9:7 LHL: 8:8 HC: 13:19	RHL: 62.3 (±12.3) LHL: 62.8 (±15.5) HC: 64.5	RHL: 7.3 (±3.1) LHL: 7.6 (±2.5) HC: 7.3	Right hemisphere and Left hemisphere	RHL: 9.9 months (±13.7) LHL: 8.6 months (±8.1)	False Belief and True Belief stories.	The performances on the ToM tasks of the RHL and LHL groups did not differ significantly from controls
Tompkins et al., 2008⁷7. Tompkins CA, Scharp VL, Fassbinder W, Meigh KM, Armstrong EM. A different story on “theory of mind” deficit in adults with right hemisphere brain damage. Aphasiology. 2008;22(1):42-61.	60	RHL: 3:9 HC: 9:19	RHL: 64.4 HC: 60.4	RHL: 14.6 (±3.2) HC: 13.9 (±2.2)	Right hemisphere	65.7 (±52.2) months	Narrative stimuli that targeted either a mental or a non-mental causal inference.	The group with RHL did not show impairment on the test.
Weed et al., 2010²²22. Weed E, McGregor W, Nielsen JF, Roepstorff A, Frith U. Theory of Mind in adults with right hemisphere damage: What's the story? Brain Lang. 2010;113(2):65-72.	21	RHL: 8:3 HC: 4:6	RHL: 65.0 HC: 65.0	–	Right hemisphere	3.09 (±1.7) months	Animated films with moving geometric shapes	RHL group displayed impaired ability to discriminate between film categories and exhibited bias when attributing mental states to others.
Wilkos et al., 2015²⁴24. Wilkos E, Brown TJ, Slawinska K, Kucharska KA. Social cognitive and neurocognitive deficits in inpatients with unilateral thalamic lesions – Pilot study. Neuropsychiatr Dis Treat. 2015;11:1031-8.	19	SP: 5:3 HC: 6:5	SP: 63.7 (±7.9) HC: 49.6 (±12.2)	–	Unilateral Thalamic	3 weeks	RMET	Compared to healthy controls, patients showed significantly worse performance on RMET task.
Winner et al., 1998²⁵25. Winner E, Brownell H, Happé F, Blum A, Pincus D. Distinguishing lies from jokes: Theory of mind deficits and discourse interpretation in right hemisphere brain-damaged patients. Brain Lang. 1998;62(1):89-106.	33	RHL: 6:7 HC: 14:6	RHL: 59.5 (±12.2) HC: 66.5 (±8.2)	RHL: 14.5 (±2.6) HC: 14.2 (±2.4)	Right hemisphere	5.6 (±5.2) years	Sixteen short lie or joke stories	RHL patients performed significantly worse than control subjects on one of two measures of second-order belief.
Xi et al., 2013²⁸28. Xi C, Zhu Y, Zhu C, Song D, Wang Y, Wang K. Deficit of theory of mind after temporal lobe cerebral infarction. Behav Brain Funct. 2013;9:15.	39	TLCI: 16:3 HC: 13:7	TLCI: 55.16 (±14.0) HC: 56 (±6.7)	SP: 10.11 (±3.3) HC: 10.95 (± 2.3)	Temporal lobe	36.42 days (±8.9)	Recognition of faux pas and RMET tasks	TLCI group performed significantly worse on tasks compared to HC group.
Yeh et al., 2014⁸8. Yeh ZT, Tsai CF. Impairment on theory of mind and empathy in patients with stroke. Psychiatry Clin Neurosci. 2014;68(8):612-20.	74	LHL: 8:6 RHL: 9:11 HC: 22:18	LHL: 57.79 (±10.8) RHL: 63.85 (±11.5) HC: 60.20 (±11.87)	LHL: 9.64 (±3.5) RHL: 8.70 (±4.6) HC: 9.10 (±3.5)	Left hemisphere and Right hemisphere	LHL: 18.18 (±6.5) months RHL: 20.45 (±7.9) months	The Faux Pas task	Patients with stroke were significantly impaired in both cognitive and affective ToM compared to a control group.

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[1] Address for correspondence: Ana Julia de Lima Bomfim. Federal University of São Carlos, Department of Psychology. Rodovia Washington Luís, km 235 – 13565-905 – São Carlos, SP, Brazil. Telephone +55 (16) 99721-2482. Fax: +55 (16) 3306-6675. E-mail: anaajullia@hotmail.com