Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress 2023 EHA Congress 2023 ASCO Annual Meeting
Clinical Collections
Advances in Alzheimer’s

At a glance: The ONWARDS insulin icodec trials

A round-up of the ONWARDS phase 3 clinical trials evaluating the novel weekly insulin icodec in people with diabetes.
ADVANCED SEARCH
Log in
Top
Alzheimer's Research & Therapy
Published in: Alzheimer's Research & Therapy 1/2016

Open Access 01-12-2016 | Research

Cognitive and affective theory of mind in dementia with Lewy bodies and Alzheimer’s disease

Authors: Camille Heitz, Vincent Noblet, Clélie Phillipps, Benjamin Cretin, Natacha Vogt, Nathalie Philippi, Jennifer Kemp, Xavier de Petigny, Mathias Bilger, Catherine Demuynck, Catherine Martin-Hunyadi, Jean-Paul Armspach, Frédéric Blanc

Published in: Alzheimer's Research & Therapy | Issue 1/2016

Login to get access

Abstract

Background

Theory of mind (ToM) refers to the ability to attribute mental states, thoughts (cognitive component) or feelings (affective component) to others. This function has been studied in many neurodegenerative diseases; however, to our knowledge, no studies investigating ToM in dementia with Lewy bodies (DLB) have been published. The aim of our study was to assess ToM in patients with DLB and to search for neural correlates of potential deficits.

Methods

Thirty-three patients with DLB (DLB group) and 15 patients with Alzheimer’s disease (AD group), all in the early stage of the disease, as well as 16 healthy elderly control subjects (HC group), were included in the study. After a global cognitive assessment, we used the Faux Pas Recognition (FPR) test, the Reading the Mind in the Eyes (RME) test and Ekman’s Facial Emotion Recognition test to assess cognitive and affective components of ToM. Patients underwent cerebral 3-T magnetic resonance imaging, and atrophy of grey matter was analysed using voxel-based morphometry. We performed a one-sample t test to investigate the correlation between each ToM score and grey matter volume and a two-sample t test to compare patients with DLB impaired with those non-impaired for each test.

Results

The DLB group performed significantly worse than the HC group on the FPR test (P = 0.033) and the RME test (P = 0.015). There was no significant difference between the AD group and the HC group or between the DLB group and the AD group. Some brain regions were associated with ToM impairments. The prefrontal cortex, with the inferior frontal cortex and the orbitofrontal cortex, was the main region, but we also found correlations with the temporoparietal junction, the precuneus, the fusiform gyrus and the insula.

Conclusions

This study is the first one to show early impairments of ToM in DLB. The two cognitive and affective components both appear to be affected in this disease. Among patients with ToM difficulties, we found atrophy in brain regions classically involved in ToM, which reinforces the neuronal network of ToM. Further studies are now needed to better understand the neural basis of such impairment.
Appendix
Available only for authorised users
Literature
1.
Shamay-Tsoory SG, Aharon-Peretz J, Perry D. Two systems for empathy: a double dissociation between emotional and cognitive empathy in inferior frontal gyrus versus ventromedial prefrontal lesions. Brain. 2009;132:617–27.CrossRefPubMed
2.
Kemp J, Despres O, Sellal F, Dufour A. Theory of mind in normal ageing and neurodegenerative pathologies. Ageing Res Rev. 2012;11:199–219.CrossRefPubMed
3.
Carrington SJ, Bailey AJ. Are there theory of mind regions in the brain? A review of the neuroimaging literature. Hum Brain Mapp. 2009;30:2313–35.CrossRefPubMed
4.
Poletti M, Enrici I, Adenzato M. Cognitive and affective theory of mind in neurodegenerative diseases: neuropsychological, neuroanatomical and neurochemical levels. Neurosci Biobehav Rev. 2012;36:2147–64.CrossRefPubMed
5.
Sebastian CL, Fontaine NM, Bird G, Blakemore SJ, Brito SA, McCrory EJ, et al. Neural processing associated with cognitive and affective theory of mind in adolescents and adults. Soc Cogn Affect Neurosci. 2012;7:53–63.PubMedCentralCrossRefPubMed
6.
Kalbe E, Schlegel M, Sack AT, Nowak DA, Dafotakis M, Bangard C, et al. Dissociating cognitive from affective theory of mind: a TMS study. Cortex. 2010;46:769–80.CrossRefPubMed
7.
Baron-Cohen S, Ring HA, Wheelwright S, Bullmore ET, Brammer MJ, Simmons A, et al. Social intelligence in the normal and autistic brain: an fMRI study. Eur J Neurosci. 1999;11:1891–8.CrossRefPubMed
8.
Frith CD, Corcoran R. Exploring ‘theory of mind’ in people with schizophrenia. Psychol Med. 1996;26:521–30.CrossRefPubMed
9.
Gregory C, Lough S, Stone V, Erzinclioglu S, Martin L, Baron-Cohen S, et al. Theory of mind in patients with frontal variant frontotemporal dementia and Alzheimer’s disease: theoretical and practical implications. Brain. 2002;125:752–64.CrossRefPubMed
10.
Henry JD, Phillips LH, von Hippel C. A meta-analytic review of theory of mind difficulties in behavioural-variant frontotemporal dementia. Neuropsychologia. 2014;56:53–62.CrossRefPubMed
11.
Youmans G, Bourgeois M. Theory of mind in individuals with Alzheimer-type dementia. Aphasiology. 2010;24:515–34.CrossRef
12.
Funkiewiez A, Bertoux M, de Souza LC, Levy R, Dubois B. The SEA (Social Cognition and Emotional Assessment): a clinical neuropsychological tool for early diagnosis of frontal variant of frontotemporal lobar degeneration. Neuropsychology. 2012;26:81–90.CrossRefPubMed
13.
Bodden ME, Dodel R, Kalbe E. Theory of mind in Parkinson’s disease and related basal ganglia disorders: a systematic review. Mov Disord. 2010;25:13–27.CrossRefPubMed
14.
Bodden ME, Mollenhauer B, Trenkwalder C, Cabanel N, Eggert KM, Unger MM, et al. Affective and cognitive theory of mind in patients with ’Parkinson’s disease. Parkinsonism Relat Disord. 2010;16:466–70.CrossRefPubMed
15.
Roca M, Torralva T, Gleichgerrcht E, Chade A, Arevalo GG, Gershanik O, et al. Impairments in social cognition in early medicated and unmedicated Parkinson disease. Cogn Behav Neurol. 2010;23:152–8.CrossRefPubMed
16.
Allain P, Havet-Thomassin V, Verny C, Gohier B, Lancelot C, Besnard J, et al. Evidence for deficits on different components of theory of mind in Huntington’s disease. Neuropsychology. 2011;25:741–51.CrossRefPubMed
17.
Meier SL, Charleston AJ, Tippett LJ. Cognitive and behavioural deficits associated with the orbitomedial prefrontal cortex in amyotrophic lateral sclerosis. Brain. 2010;133:3444–57.CrossRefPubMed
18.
Kluger BM, Heilman KM. Dysfunctional facial emotional expression and comprehension in a patient with corticobasal degeneration. Neurocase. 2007;13:165–8.CrossRefPubMed
19.
Duval C, Bejanin A, Piolino P, Laisney M, de La Sayette V, Belliard S, et al. Theory of mind impairments in patients with semantic dementia. Brain. 2012;135:228–41.PubMedCentralCrossRefPubMed
20.
Ghosh BC, Calder AJ, Peers PV, Lawrence AD, Acosta-Cabronero J, Pereira JM, et al. Social cognitive deficits and their neural correlates in progressive supranuclear palsy. Brain. 2012;135:2089–102.PubMedCentralCrossRefPubMed
21.
Roca M, Manes F, Gleichgerrcht E, Ibanez A, de Toledo MEG, Marenco V, et al. Cognitive but not affective theory of mind deficits in mild relapsing-remitting multiple sclerosis. Cogn Behav Neurol. 2014;27:25–30.CrossRefPubMed
22.
23.
Perri R, Monaco M, Fadda L, Caltagirone C, Carlesimo GA. Neuropsychological correlates of behavioral symptoms in Alzheimer’s disease, frontal variant of frontotemporal, subcortical vascular, and Lewy body dementias: a comparative study. J Alzheimers Dis. 2014;39:669–77.PubMed
24.
Modinos G, Obiols JE, Pousa E, Vicens J. Theory of mind in different dementia profiles. J Neuropsychiatry Clin Neurosci. 2009;21:100–1.CrossRefPubMed
25.
McKeith IG, Dickson DW, Lowe J, Emre M, O’Brien JT, Feldman H, et al. Diagnosis and management of dementia with Lewy bodies: third report of the DLB Consortium. Neurology. 2005;65:1863–72.CrossRefPubMed
26.
American Psychiatric Association. Diagnostic and statistical manual of mental disorders. 5th ed. Washington, DC: American Psychiatric Publishing; 2013.
27.
Dubois B, Feldman HH, Jacova C, DeKosky ST, Barberger-Gateau P, Cummings J, et al. Research criteria for the diagnosis of Alzheimer’s disease: revising the NINCDS-ADRDA criteria. Lancet Neurol. 2007;6:734–46.CrossRefPubMed
28.
Movement Disorder Society Task Force on Rating Scales for Parkinson’s Disease. The Unified Parkinson’s Disease Rating Scale (UPDRS): status and recommendations. Mov Disord. 2003;18:738–50.CrossRef
29.
Ferman TJ, Smith GE, Boeve BF, Ivnik RJ, Petersen RC, Knopman D, et al. DLB fluctuations: specific features that reliably differentiate DLB from AD and normal aging. Neurology. 2004;62:181–7.CrossRefPubMed
30.
Walker MP, Ayre GA, Cummings JL, Wesnes K, McKeith IG, O’Brien JT, et al. The Clinician Assessment of Fluctuation and the One Day Fluctuation Assessment Scale: two methods to assess fluctuating confusion in dementia. Br J Psychiatry. 2000;177:252–6.CrossRefPubMed
31.
Folstein MF, Folstein SE, McHugh PR. “Mini-mental state”: a practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res. 1975;12:189–98.CrossRefPubMed
32.
Grober E, Buschke H. Genuine memory deficits in dementia. Dev Neuropsychol. 1987;3:13–36.CrossRef
33.
34.
Barbeau E, Didic M, Tramoni E, Felician O, Joubert S, Sontheimer A, et al. Evaluation of visual recognition memory in MCI patients. Neurology. 2004;62:1317–22.CrossRefPubMed
35.
Deloche G, Hannequin D. DO 80: Test de dénomination orale d’images. Paris: Les Editions du Centre de Psychologie Appliquée (ECPA); 1997.
36.
Dubois B, Slachevsky A, Litvan I, Pillon B. The FAB: a Frontal Assessment Battery at bedside. Neurology. 2000;55:1621–6.CrossRefPubMed
37.
Tombaugh TN. Trail Making Test A and B: normative data stratified by age and education. Arch Clin Neuropsychol. 2004;19:203–14.CrossRefPubMed
38.
Wechsler D. Wechsler Adult Intelligence Scale. 4th ed. San Antonio, TX: Pearson; 2008.
39.
Cardebat D, Doyon B, Puel M, Goulet P, Joanette Y. Formal and semantic lexical evocation in normal subjects. Performance and dynamics of production as a function of sex, age and educational level. Acta Neurol Belg. 1990;90:207–17.PubMed
40.
Mahieux-Laurent F, Fabre C, Galbrun E, Dubrulle A, Moroni C, groupe de réflexion sur les praxies du CMRR Ile-de-France Sud. Validation of a brief screening scale evaluating praxic abilities for use in memory clinics: evaluation in 419 controls, 127 mild cognitive impairment and 320 demented patients [in French]. Rev Neurol (Paris). 2009;165:560–7.
41.
Rey A. Manuel du Test de copie et de reproduction de mémoire de figures géométriques complexes. Paris: Centre de Psychologie Appliquée; 1959.
42.
Rapport LJ, Millis SR, Bonello PJ. Validation of the Warrington theory of visual processing and the Visual Object and Space Perception Battery. J Clin Exp Neuropsychol. 1998;20:211–20.CrossRefPubMed
43.
Stone VE, Baron-Cohen S, Knight RT. Frontal lobe contributions to theory of mind. J Cogn Neurosci. 1998;10:640–56.CrossRefPubMed
44.
Baron-Cohen S, Wheelwright S, Hill J, Raste Y, Plumb I. The “Reading the Mind in the Eyes” Test revised version: a study with normal adults, and adults with Asperger syndrome or high-functioning autism. J Child Psychol Psychiatry. 2001;42:241–51.CrossRefPubMed
45.
Ekman P, Friesen W. Pictures of facial affect. Palo Alto, CA: Consulting Psychologists Press; 1975.
46.
Bertoux M, Volle E, Funkiewiez A, de Souza LC, Leclercq D, Dubois B. Social Cognition and Emotional Assessment (SEA) is a marker of medial and orbital frontal functions: a voxel-based morphometry study in behavioral variant of frontotemporal degeneration. J Int Neuropsychol Soc. 2012;18:972–85.CrossRefPubMed
47.
Ruffman T, Henry JD, Livingstone V, Phillips LH. A meta-analytic review of emotion recognition and aging: implications for neuropsychological models of aging. Neurosci Biobehav Rev. 2008;32:863–81.CrossRefPubMed
48.
Shamay-Tsoory SG, Tomer R, Berger BD, Goldsher D, Aharon-Peretz J. Impaired “affective theory of mind” is associated with right ventromedial prefrontal damage. Cogn Behav Neurol. 2005;18:55–67.CrossRefPubMed
49.
Shamay-Tsoory SG, Aharon-Peretz J. Dissociable prefrontal networks for cognitive and affective theory of mind: a lesion study. Neuropsychologia. 2007;45:3054–67.CrossRefPubMed
50.
Cuerva AG, Sabe L, Kuzis G, Tiberti C, Dorrego F, Starkstein SE. Theory of mind and pragmatic abilities in dementia. Neuropsychiatry Neuropsychol Behav Neurol. 2001;14:153–8.PubMed
51.
Zaitchik D, Koff E, Brownell H, Winner E, Albert M. Inference of beliefs and emotions in patients with Alzheimer’s disease. Neuropsychology. 2006;20:11–20.CrossRefPubMed
52.
Fernandez-Duque D, Baird JA, Black SE. False-belief understanding in frontotemporal dementia and Alzheimer’s disease. J Clin Exp Neuropsychol. 2009;31:489–97.CrossRefPubMed
53.
Castelli I, Pini A, Alberoni M, Liverta-Sempio O, Baglio F, Massaro D, et al. Mapping levels of theory of mind in Alzheimer’s disease: a preliminary study. Aging Ment Health. 2011;15:157–68.CrossRefPubMed
54.
Laisney M, Bon L, Guiziou C, Daluzeau N, Eustache F, Desgranges B. Cognitive and affective theory of mind in mild to moderate Alzheimer’s disease. J Neuropsychol. 2013;7:107–20.CrossRefPubMed
55.
Narme P, Mouras H, Roussel M, Devendeville A, Godefroy O. Assessment of socioemotional processes facilitates the distinction between frontotemporal lobar degeneration and Alzheimer’s disease. J Clin Exp Neuropsychol. 2013;35:728–44.CrossRefPubMed
56.
Aboulafia-Brakha T, Christe B, Martory MD, Annoni JM. Theory of mind tasks and executive functions: a systematic review of group studies in neurology. J Neuropsychol. 2011;5:39–55.CrossRefPubMed
57.
Beyer MK, Larsen JP, Aarsland D. Gray matter atrophy in Parkinson disease with dementia and dementia with Lewy bodies. Neurology. 2007;69:747–54.CrossRefPubMed
58.
Whitwell JL, Weigand SD, Shiung MM, Boeve BF, Ferman TJ, Smith GE, et al. Focal atrophy in dementia with Lewy bodies on MRI: a distinct pattern from Alzheimer’s disease. Brain. 2007;130:708–19.PubMedCentralCrossRefPubMed
59.
Zhong J, Pan P, Dai Z, Shi H. Voxelwise meta-analysis of gray matter abnormalities in dementia with Lewy bodies. Eur J Radiol. 2014;83:1870–4.CrossRefPubMed
60.
Stuss DT, Levine B. Adult clinical neuropsychology: lessons from studies of the frontal lobes. Annu Rev Psychol. 2002;53:401–33.CrossRefPubMed
61.
Platek SM, Keenan JP, Gallup Jr GG, Mohamed FB. Where am I? The neurological correlates of self and other. Brain Res Cogn Brain Res. 2004;19:114–22.CrossRefPubMed
62.
Adenzato M, Cavallo M, Enrici I. Theory of mind ability in the behavioural variant of frontotemporal dementia: an analysis of the neural, cognitive, and social levels. Neuropsychologia. 2010;48:2–12.CrossRefPubMed
63.
Baglio F, Castelli I, Alberoni M, Blasi V, Griffanti L, Falini A, et al. Theory of mind in amnestic mild cognitive impairment: an fMRI study. J Alzheimers Dis. 2012;29:25–37.PubMed
64.
Hynes CA, Baird AA, Grafton ST. Differential role of the orbital frontal lobe in emotional versus cognitive perspective-taking. Neuropsychologia. 2006;44:374–83.CrossRefPubMed
65.
Shamay-Tsoory SG, Harari H, Aharon-Peretz J, Levkovitz Y. The role of the orbitofrontal cortex in affective theory of mind deficits in criminal offenders with psychopathic tendencies. Cortex. 2010;46:668–77.CrossRefPubMed
66.
Bodden ME, Kubler D, Knake S, Menzler K, Heverhagen JT, Sommer J, et al. Comparing the neural correlates of affective and cognitive theory of mind using fMRI: Involvement of the basal ganglia in affective theory of mind. Adv Cogn Psychol. 2013;9:32–43.PubMedCentralCrossRefPubMed
67.
Geraci A, Surian L, Ferraro M, Cantagallo A. Theory of mind in patients with ventromedial or dorsolateral prefrontal lesions following traumatic brain injury. Brain Inj. 2010;24:978–87.CrossRefPubMed
68.
Lee TM, Ip AK, Wang K, Xi CH, Hu PP, Mak HK, et al. Faux pas deficits in people with medial frontal lesions as related to impaired understanding of a speaker’s mental state. Neuropsychologia. 2010;48:1670–6.CrossRefPubMed
69.
Kalbe E, Grabenhorst F, Brand M, Kessler J, Hilker R, Markowitsch HJ. Elevated emotional reactivity in affective but not cognitive components of theory of mind: a psychophysiological study. J Neuropsychol. 2007;1:27–38.CrossRefPubMed
70.
Schurz M, Radua J, Aichhorn M, Richlan F, Perner J. Fractionating theory of mind: a meta-analysis of functional brain imaging studies. Neurosci Biobehav Rev. 2014;42:9–34.CrossRefPubMed
71.
Uddin LQ, Molnar-Szakacs I, Zaidel E, Iacoboni M. rTMS to the right inferior parietal lobule disrupts self-other discrimination. Soc Cogn Affect Neurosci. 2006;1:65–71.PubMedCentralCrossRefPubMed
72.
Decety J, Lamm C. The role of the right temporoparietal junction in social interaction: how low-level computational processes contribute to meta-cognition. Neuroscientist. 2007;13:580–93.CrossRefPubMed
73.
Cavanna AE, Trimble MR. The precuneus: a review of its functional anatomy and behavioural correlates. Brain. 2006;129:564–83.CrossRefPubMed
74.
Fusar-Poli P, Placentino A, Carletti F, Landi P, Allen P, Surguladze S, et al. Functional atlas of emotional faces processing: a voxel-based meta-analysis of 105 functional magnetic resonance imaging studies. J Psychiatry Neurosci. 2009;34:418–32.PubMedCentralPubMed
75.
Gallagher HL, Happe F, Brunswick N, Fletcher PC, Frith U, Frith CD. Reading the mind in cartoons and stories: an fMRI study of ‘theory of mind’ in verbal and nonverbal tasks. Neuropsychologia. 2000;38:11–21.CrossRefPubMed
76.
Nelson PT, Jicha GA, Kryscio RJ, Abner EL, Schmitt FA, Cooper G, et al. Low sensitivity in clinical diagnoses of dementia with Lewy bodies. J Neurol. 2010;257:359–66.PubMedCentralCrossRefPubMed
Metadata
Title
Cognitive and affective theory of mind in dementia with Lewy bodies and Alzheimer’s disease
Authors
Camille Heitz
Vincent Noblet
Clélie Phillipps
Benjamin Cretin
Natacha Vogt
Nathalie Philippi
Jennifer Kemp
Xavier de Petigny
Mathias Bilger
Catherine Demuynck
Catherine Martin-Hunyadi
Jean-Paul Armspach
Frédéric Blanc
Publication date
01-12-2016
Publisher
BioMed Central
Published in
Alzheimer's Research & Therapy / Issue 1/2016
Electronic ISSN: 1758-9193
DOI
https://doi.org/10.1186/s13195-016-0179-9

Other articles of this Issue 1/2016

Alzheimer's Research & Therapy 1/2016 Go to the issue

Research

Changes in cerebral glucose metabolism after 3 weeks of noninvasive electrical stimulation of mild cognitive impairment patients

Review

Drug development in Alzheimer’s disease: the path to 2025

Research

Prospective longitudinal course of cognition in older subjects with mild parkinsonian signs

Research

Mini Mental State Examination and Logical Memory scores for entry into Alzheimer’s disease trials

Research

Recent global trends in the prevalence and incidence of dementia, and survival with dementia

Research

Transcranial direct current stimulation as a memory enhancer in patients with Alzheimer’s disease: a randomized, placebo-controlled trial