Skip to main content

Advertisement

SpringerLink
Log in

Analyzing theory of mind impairment in patients with behavioral variant frontotemporal dementia

  • Original Article
  • Published:
Neurological Sciences Aims and scope Submit manuscript

Abstract

Objective

Behavioral variant frontotemporal dementia (bvFTD) and theory of mind (ToM) have common neuroanatomical aspects. This pilot study analyzed the qualitative features of ToM relatively to the site of prefrontal atrophy, aiming to identify a neurobehavioral pattern of bvFTD.

Method

Fourteen bvFTD patients were compared with 14 healthy subjects with similar age, years of schooling, gender distribution, and social background. The faux pas task (FPT) measured the recognition and comprehension of faux pas (FP) and awareness of the factual details on 20 stories. Magnetic resonance assessed prefrontal atrophy.

Results

The bvFTD patients were significantly impaired in FP recognition and comprehension and in attribution of non-existent FP. Qualitative analysis revealed five types of errors: misidentification of characters, misidentification of emotions, excessive cohesiveness to the factual context, delusional interpretations, and non-responses. The FPT recognition and comprehension scores were unrelated to story factual details or other neuropsychological performance. Conversely, the FP comprehension scores related to disease duration, the delusional errors to disease duration and prefrontal orbital atrophy, and the cohesiveness errors to age and prefrontal dorsolateral atrophy.

Conclusions

In bvFTD, ToM is characterized by misinterpretation of mental states and concrete thinking, which is related to disease severity and distinct areas of prefrontal atrophy. This neurobehavioral pattern may be a marker for bvFDT.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  1. Rascovsky K, Hodges JR, Knopman D, Mendez MF, Kramer JH, Neuhaus J, van Swieten JC, Seelaar H, Dopper EG, Onyike CU, Hillis AE, Josephs KA, Boeve BF, Kertesz A, Seeley WW, Rankin KP, Johnson JK, Gorno-Tempini ML, Rosen H, Prioleau-Latham CE, Lee A, Kipps CM, Lillo P, Piguet O, Rohrer JD, Rossor MN, Warren JD, Fox NC, Galasko D, Salmon DP, Black SE, Mesulam M, Weintraub S, Dickerson BC, Diehl-Schmid J, Pasquier F, Deramecourt V, Lebert F, Pijnenburg Y, Chow TW, Manes F, Grafman J, Cappa SF, Freedman M, Grossman M, Miller BL (2011) Sensitivity of revised diagnostic criteria for the behavioural variant of frontotemporal dementia. Brain 134:2456–2477. https://doi.org/10.1093/brain/awr179

    Article  PubMed  PubMed Central  Google Scholar 

  2. Neary D, Snowden JS, Northen B, Goulding PJ (1998) Dementia of frontal lobe type. J Neurol Neurosurg Psychiatry 51:353–361

    Article  Google Scholar 

  3. Johnson JK, Diehl J, Mendez MF, Neuhaus J, Shapira JS, Forman M, Chute DJ, Roberson ED, Pace-Savitsky C, Neumann M, Chow TW, Rosen HJ, Forstl H, Kurz A, Miller BL (2005) Frontotemporal lobar degeneration. Arch Neurol 62:925–930

    PubMed  Google Scholar 

  4. Leyton CE, Hodges JR (2010) Frontotemporal dementias: recent advances and current controversies. Ann Indian Acad Neurol 13:S74–S80

    PubMed  PubMed Central  Google Scholar 

  5. Schroeter ML, Raczka K, Neumann J, von Cramon DY (2007) Neural networks in frontotemporal dementia – a meta-analysis. Neurobiol Aging 36:497–510

    Google Scholar 

  6. Schroeter ML, Lair AR, Chwiesko C, Deuschl C, Scheiner E, Bzdok D, Eickhoff SB, Neumann J (2014) Conceptualizing neuropsychiatric diseases with multimodal data-driven meta-analyses. The case of behavioral variant frontotemporal dementia. Cortex 57:22–37

    Article  PubMed  Google Scholar 

  7. Giovagnoli AR, Erbetta A, Reati F, Bugiani O (2008) Differential neuropsychological patterns in frontotemporal dementia and Alzheimer’s disease in a study of diagnostic concordance. Neuropsychologia 46:1495–1504

    Article  PubMed  Google Scholar 

  8. Frisoni GB, Pizzolato G, Geroldi C, Rossato A, Bianchetti A, Trabucchi M (1995) Dementia of the frontal type: neuropsychological and [99Tc]-HMPAO SPECT features. Int Ger Psychiat Neurol 8:42–48

    CAS  Google Scholar 

  9. Gregory CA, Orrell M, Sahakian B, Hodges J (1997) Can frontotemporal dementia and Alzheimer’s disease be differentiated using a brief battery of tests? Int J Geriatr Psychiatry 12:375–383

    Article  CAS  PubMed  Google Scholar 

  10. Hodges JR, Patterson K, Ward R, Garrard P, Bak T, Perry R, Gregory C (1999) The differentiation of semantic dementia and frontal lobe dementia (temporal and frontal variants of frontotemporal dementia) from early Alzheimer’s disease: a comparative neuropsychological study. Neuropsychology 13:31–40

    Article  CAS  PubMed  Google Scholar 

  11. Mendez MF, Cherrier M, Perryman KM, Pachana N, Miller BL, Cummings JL (1996) Frontotemporal dementia versus Alzheimer’s disease: differential cognitive features. Neurology 47:1189–1194

    Article  CAS  PubMed  Google Scholar 

  12. Pachana NA, Boone BK, Millar BL, Cummings JL, Berman N (1996) Comparisons of neuropsychological functioning in Alzheimer’s disease and frontotemporal dementia. J Int Neuropsychol Soc 2:505–510

    Article  CAS  PubMed  Google Scholar 

  13. Pasquier F, Lebert F, Grymonprez L, Pettit H (1995) Verbal fluency in dementia of frontal lobe type and dementia of Alzheimer type. J Neurol Neurosurg Psychiatry 58:81–84

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Thompson JC, Stopford CL, Snowden JS, Neary D (2005) Qualitative neuropsychological performance characteristics in frontotemporal dementia and Alzheimer’s disease. J Neurol Neurosurg Psychiatry 76:920–927

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Walker AJ, Meares S, Sachdev PS, Brodaty H (2005) The differentiation of mild frontotemporal dementia from Alzheimer’s disease and healthy aging by neuropsychological tests. Int Psychogeriatr 17:57–68

    Article  PubMed  Google Scholar 

  16. Siri S, Benaglio I, Frigerio G, Binetti G, Cappa SF (2001) A brief neuropsychological assessment for the differential diagnosis between frontotemporal dementia and Alzheimer’s disease. Eur J Neurol 8:125–132

    Article  CAS  PubMed  Google Scholar 

  17. Perri R, Koch G, Carlesimo et al (2004) Alzheimer’s disease and frontal variant of frontotemporal dementia. J Neurol 10:1238–1244

    Google Scholar 

  18. Davies RR, Hodges JR, Kril JJ, Patterson K, Halliday GM, Xuereb JH (2005) The pathological basis of semantic dementia. Brain 128:1984–1995

    Article  PubMed  Google Scholar 

  19. Henry JD, Phillips LH, von Hippel C (2014) A meta-analytic review of theory of mind difficulties in behavioural-variant frontotemporal dementia. Neuropsychologia 56:53–62

    Article  PubMed  Google Scholar 

  20. Shamay-Tsoory SG, Harari H, Aharon-Peretz J, Levkovitz Y (2010) The role of the orbitofrontal cortex in affective theory of mind deficits in criminal offenders with psychopathic tendencies. Cortex 46:668–677

    Article  PubMed  Google Scholar 

  21. Völlm BA, Taylor ANW, Richardson P, Corcoran R, Stirling J, McKie S, Deakin JF, Elliott R (2006) Neuronal correlates of theory of mind and empathy: a functional magnetic resonance imaging study in a nonverbal task. Neuroimage 29:90–98

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  23. Giovagnoli AR (2015) The importance of theory of mind in epilepsy. Epilepsy Behav 39:145–153

    Article  Google Scholar 

  24. Shaw P, Lawrence EJ, Radbourne C, Bramham J, Polkey CE, David AS (2004) The impact of early and late damage to the human amygdala on “theory of mind” reasoning. Brain 127:1535–1548

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  26. Rowe AD, Bullock PR, Polkey CE, Morris RG (2001) “Theory of mind” impairments and their relationship to executive functioning following frontal lobe excisions. Brain 124:600–616

    Article  CAS  PubMed  Google Scholar 

  27. Stuss DT, Gallup GG Jr, Alexander MP (2001) The frontal lobes are accessory for “theory of mind”. Brain 124:279–286

    Article  CAS  PubMed  Google Scholar 

  28. Stone VE, Baron-Cohen S, Knight RT (1998) Frontal lobe contributions to theory of mind. J Cogn Neurosci 10:640–656

    Article  CAS  PubMed  Google Scholar 

  29. Saxe R, Wexler A (2005) Making sense of another mind. Neuropsychologia 43:1391–1399

    Article  PubMed  Google Scholar 

  30. Bodden ME, Dodel R, Kalbe E (2010) Theory of mind in Parkinson’s disease and related basal ganglia disorders: a systematic review. Mov Disord 25:13–27

    Article  PubMed  Google Scholar 

  31. Parente A, Manfredi V, Tarallo A, Salsano E, Erbetta A, Pareyson D, Giovagnoli AR (2013) Selective theory of mind impairment and cerebellar atrophy: a case report. J Neurol 260:2166–2169

    Article  PubMed  Google Scholar 

  32. Gregory C, Lough S, Stone V, Erzinclioglu S, Martin L, Baron-Cohen S, Hodges JR (2002) Theory of mind in patients with frontal variant frontotemporal dementia and Alzheimer’s disease: theoretical and practical implications. Brain 125:752–764

    Article  PubMed  Google Scholar 

  33. Torralva T, Kipps CM, Hodges JR, Clark L, Bekinschtein T, Roca M, Calcagno ML, Manes F (2007) The relationship between affective decision-making and theory of mind in the frontal variant of fronto-temporal dementia. Neuropsychologia 45:342–349

    Article  PubMed  Google Scholar 

  34. Lough S, Kipps CM, Treise C, Watson P, Blair JR, Hodges JR (2006) Social reasoning, emotion and empathy in frontotemporal dementia. Neuropsychologia 44:950–958

    Article  PubMed  Google Scholar 

  35. Eslinger PJ, Moore P, Troiani V, Antani S, Cross K, Kwok S, Grossman M (2007) Oops! Resolving social dilemmas in frontotemporal dementia. J Neurol Neurosurg Psychiatry 78:457–460

    Article  PubMed  PubMed Central  Google Scholar 

  36. Ramanan S, de Souza LC, Moreau N, Sarazin M, Teixeira AL, Allen Z, Guimarães HC, Caramelli P, Dubois B, Hornberger M, Bertoux M (2017) Determinants of theory of mind performance in Alzheimer’s disease: a data-mining study. Cortex 88:8–18. https://doi.org/10.1016/j.cortex.2016.11.014

    Article  PubMed  Google Scholar 

  37. Samson D, Apperly IA, Humphreys GW (2007) Error analysis reveal contrasting deficits in “theory of mind”: neuropsychological evidence from 3-option false belief task. Neuropsychologia 45:2561–2569

    Article  PubMed  Google Scholar 

  38. Maylor EA, Moulson JM, Muncer AM, Taylor LA (2002) Does performance on theory of mind tasks decline in old age? Br J Psychol 93:465–485

    Article  PubMed  Google Scholar 

  39. Surian L, Siegal M (2001) Sources of performance on theory of mind tasks in right hemisphere-damaged patients. Brain Lang 78:224–232

    Article  CAS  PubMed  Google Scholar 

  40. Bibby H, McDonald S (2005) Theory of mind after traumatic brain injury. Neuropsychologia 43:99–114

    Article  PubMed  Google Scholar 

  41. Carlson SM, Moses LJ (2001) Individual differences in inhibitory control and children’s theory of mind. Child Dev 72:1032–1053

    Article  CAS  PubMed  Google Scholar 

  42. McKinnon MC, Moscovitch M (2007) Domain-general contributions to social reasoning: theory of mind and deontic reasoning re-explored. Cognition 102:179–218

    Article  PubMed  Google Scholar 

  43. Channon S, Crawford S (2002) The effects of anterior lesions on performance on a story comprehension test: left anterior impairment on a theory of mind-type task. Neuropsychologia 38:1006–1017

    Article  Google Scholar 

  44. Fine C, Lumsden J, Blair RJR (2001) Dissociation between “theory of mind” and executive functions in a patient with early left amygdala damage. Brain 124:287–298

    Article  CAS  PubMed  Google Scholar 

  45. Bird CM, Castelli F, Malik O, Frith U, Husain M (2004) The impact of extensive medial frontal lobe damage on “theory of mind” and cognition. Brain 127:914–928

    Article  PubMed  Google Scholar 

  46. Baron-Cohen S, O’Riordan M, Stone V, Jones R, Plaisted K (1999) Recognition of faux pas by normally developing children and children with Asperger syndrome or high-functioning autism. J Autism Dev Disord 29:407–418

    Article  CAS  PubMed  Google Scholar 

  47. Hughes CB, Berg L, Danzinger WL (1982) A new clinical scale for the staging of dementia. Br J Psychiatry 140:566–567

    Article  CAS  PubMed  Google Scholar 

  48. Galton CJ, Patterson K, Xuereb JH, Hodges JR (2000) Atypical and typical presentation of Alzheimer’s disease: a clinical, neuropsychological, neuroimaging and pathological study of 13 cases. Brain 123:484–498

    Article  PubMed  Google Scholar 

  49. Tamraz JC, Comair YG (2000) Atlas of regional anatomy of the brain using MRI with functional correlation. Springer-Verlag Berlin Heidelberg, New York, pp 1–330

    Google Scholar 

  50. Jurado MB, Rosselli M (2007) The elusive nature of executive functions. Neuropsychol Rev 17:213–233

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

The authors are grateful to the subjects who kindly cooperated in the neuropsychological assessment.

Author information

Authors and Affiliations

  1. Unit of Neurology – Neuropathology, Department of Diagnostics and Applied Technology, Fondazione IRCCS Istituto Neurologico Carlo Besta, Milan, Italy

    Anna Rita Giovagnoli, Chiara Paterlini & Orso Bugiani

  2. Charles Matthews Neuropsychology Laboratory, Department of Neurology, University of Wisconsin School of Medicine and Public Health, Madison, WI, USA

    Brian Bell

  3. W.S. Middleton Memorial Veterans Hospital, Madison, WI, USA

    Brian Bell

  4. Unit of Neuroradiology, Department of Diagnostics and Applied Technology, Fondazione IRCCS Neurological Institute Carlo Besta, Milan, Italy

    Alessandra Erbetta

Authors
  1. Anna Rita Giovagnoli
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Brian Bell
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Alessandra Erbetta
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Chiara Paterlini
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Orso Bugiani
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Anna Rita Giovagnoli.

Ethics declarations

All of the research procedures were conducted in accord with the Helsinki Declaration of 1975. The subjects gave their informed consent to the clinical and instrumental evaluations.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Giovagnoli, A.R., Bell, B., Erbetta, A. et al. Analyzing theory of mind impairment in patients with behavioral variant frontotemporal dementia. Neurol Sci 40, 1893–1900 (2019). https://doi.org/10.1007/s10072-019-03911-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10072-019-03911-6

Keywords

Search

Navigation