Skip to main content
Top
Published in: European Archives of Psychiatry and Clinical Neuroscience 8/2014

01-12-2014 | Original Paper

Putting things into perspective: the nature and impact of theory of mind impairment in Huntington’s disease

Authors: Clare M. Eddy, Sridevi Sira Mahalingappa, Hugh E. Rickards

Published in: European Archives of Psychiatry and Clinical Neuroscience | Issue 8/2014

Login to get access

Abstract

In Huntington’s disease (HD), frontostriatal dysfunction may lead to deficits in theory of mind (ToM), in addition to broader cognitive impairment. We investigated relationships between patients’ spatial and social perspective taking performance and executive deficits, self-reported everyday perspective taking, motor symptoms, functional capacity and quality of life. Thirty patients with symptomatic HD and twenty-three healthy controls of similar age and education completed two ToM tasks, a scale assessing everyday interpersonal perspective taking, a novel object-based spatial perspective taking task (SPT) and executive measures. Ratings of quality of life, psychiatric symptoms, motor symptom severity and functional capacity were also taken for patients. When compared to controls, patients exhibited significant deficits in ToM and spatial perspective taking and lower everyday perspective taking scores. Executive deficits were linked to poor understanding of socially inappropriate remarks and errors in mental state attribution. This may be the first study to show that aspects of ToM performance are linked to spatial perspective taking, motor symptom severity and functional capacity in HD. Our findings indicate that patients with HD exhibit evidence of reduced perspective taking in everyday life in addition to poor performance on social and SPTs. They also emphasise the need to better specify the precise cognitive and neural bases for ToM deficits in neurodegenerative conditions. Further research exploring the impact of striatal degeneration on perspective taking abilities will make a valuable contribution to the continued development of functional models of frontostriatal circuitry.
Literature
1.
go back to reference Montoya A, Pelletier M, Menear M, Duplessis E, Richer F, Lepage M (2006) Episodic memory impairment in Huntington’s disease: a meta-analysis. Neuropsychologia 44:1984–1994PubMedCrossRef Montoya A, Pelletier M, Menear M, Duplessis E, Richer F, Lepage M (2006) Episodic memory impairment in Huntington’s disease: a meta-analysis. Neuropsychologia 44:1984–1994PubMedCrossRef
2.
go back to reference Thompson JC, Poliakoff E, Sollom AC, Howard E, Craufurd D, Snowden JS (2010) Automaticity and attention in Huntington’s disease: when two hands are not better than one. Neuropsychologia 48:171–178PubMedCrossRef Thompson JC, Poliakoff E, Sollom AC, Howard E, Craufurd D, Snowden JS (2010) Automaticity and attention in Huntington’s disease: when two hands are not better than one. Neuropsychologia 48:171–178PubMedCrossRef
3.
go back to reference Georgiou N, Bradshaw JL, Phillips JG, Chiu E (1996) The effect of Huntington’s disease and Gilles de la Tourette’s syndrome on the ability to hold and shift attention. Neuropsychologia 34:843–851PubMedCrossRef Georgiou N, Bradshaw JL, Phillips JG, Chiu E (1996) The effect of Huntington’s disease and Gilles de la Tourette’s syndrome on the ability to hold and shift attention. Neuropsychologia 34:843–851PubMedCrossRef
4.
go back to reference Beste C, Saft C, Andrich J, Gold R, Falkenstein M (2008) Response inhibition in Huntington’s disease - a study using ERPs and sLORETA. Neuropsychologia 46:1290–1297PubMedCrossRef Beste C, Saft C, Andrich J, Gold R, Falkenstein M (2008) Response inhibition in Huntington’s disease - a study using ERPs and sLORETA. Neuropsychologia 46:1290–1297PubMedCrossRef
5.
go back to reference Eddy CM, Rickards HE (2012) Impact of cognitive and behavioural changes on quality of life in Huntington’s disease. Basal Ganglia 2(3):139–142CrossRef Eddy CM, Rickards HE (2012) Impact of cognitive and behavioural changes on quality of life in Huntington’s disease. Basal Ganglia 2(3):139–142CrossRef
6.
go back to reference Wolf RC, Vasic N, Schönfeldt-Lecuona C, Ecker D, Landwehrmeyer GB (2009) Cortical dysfunction in patients with Huntington’s disease during working memory performance. Hum Brain Mapp 30:327–339PubMedCrossRef Wolf RC, Vasic N, Schönfeldt-Lecuona C, Ecker D, Landwehrmeyer GB (2009) Cortical dysfunction in patients with Huntington’s disease during working memory performance. Hum Brain Mapp 30:327–339PubMedCrossRef
7.
go back to reference Henley SM, Novak MJ, Frost C, King J, Tabrizi SJ, Warren JD (2012) Emotion recognition in Huntington’s disease: a systematic review. Neurosci Biobehav Rev 36:237–253PubMedCrossRef Henley SM, Novak MJ, Frost C, King J, Tabrizi SJ, Warren JD (2012) Emotion recognition in Huntington’s disease: a systematic review. Neurosci Biobehav Rev 36:237–253PubMedCrossRef
8.
go back to reference Calder AJ, Keane J, Young AW, Lawrence AD, Mason S, Barker RA (2010) The relation between anger and different forms of disgust: implications for emotion recognition impairments in Huntington’s disease. Neuropsychologia 48:2719–2729PubMedCrossRef Calder AJ, Keane J, Young AW, Lawrence AD, Mason S, Barker RA (2010) The relation between anger and different forms of disgust: implications for emotion recognition impairments in Huntington’s disease. Neuropsychologia 48:2719–2729PubMedCrossRef
9.
go back to reference Eddy CM, Mitchell IJ, Beck SR, Cavanna AE, Rickards HE (2011) Altered subjective fear responses in Huntington’s disease. Parkinsonism Relat Disord 17:386–389PubMedCrossRef Eddy CM, Mitchell IJ, Beck SR, Cavanna AE, Rickards HE (2011) Altered subjective fear responses in Huntington’s disease. Parkinsonism Relat Disord 17:386–389PubMedCrossRef
10.
go back to reference Hayes CJ, Stevenson RJ, Coltheart M (2009) The processing of emotion in patients with Huntington’s disease: variability and differential deficits in disgust. Cogn Behav Neurol 22:249–257PubMedCrossRef Hayes CJ, Stevenson RJ, Coltheart M (2009) The processing of emotion in patients with Huntington’s disease: variability and differential deficits in disgust. Cogn Behav Neurol 22:249–257PubMedCrossRef
11.
go back to reference Snowden JS, Gibbons ZC, Blackshaw A, Doubleday E, Thompson J, Craufurd D (2003) Social cognition in frontotemporal dementia and Huntington’s disease. Neuropsychologia 41:688–701PubMedCrossRef Snowden JS, Gibbons ZC, Blackshaw A, Doubleday E, Thompson J, Craufurd D (2003) Social cognition in frontotemporal dementia and Huntington’s disease. Neuropsychologia 41:688–701PubMedCrossRef
12.
go back to reference Allain P, Havet-Thomassin V, Verny C, Gohier B, Lancelot C, Besnard J, Fasotti L, Le Gall D (2011) Evidence for deficits on different components of theory of mind in Huntington’s disease. Neuropsychology 25:741–751PubMedCrossRef Allain P, Havet-Thomassin V, Verny C, Gohier B, Lancelot C, Besnard J, Fasotti L, Le Gall D (2011) Evidence for deficits on different components of theory of mind in Huntington’s disease. Neuropsychology 25:741–751PubMedCrossRef
13.
go back to reference Brüne M, Blank K, Witthaus H, Saft C (2011) “Theory of mind” is impaired in Huntington’s disease. Mov Disord 26:671–678PubMedCrossRef Brüne M, Blank K, Witthaus H, Saft C (2011) “Theory of mind” is impaired in Huntington’s disease. Mov Disord 26:671–678PubMedCrossRef
14.
go back to reference Eddy CM, Sira Mahalingappa S, Rickards HE (2012) In Huntington’s disease associated with deficits in theory of mind? Acta Neurol Scand 126:376–383PubMedCrossRef Eddy CM, Sira Mahalingappa S, Rickards HE (2012) In Huntington’s disease associated with deficits in theory of mind? Acta Neurol Scand 126:376–383PubMedCrossRef
15.
go back to reference 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 125:752–764PubMedCrossRef 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 125:752–764PubMedCrossRef
16.
go back to reference 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, adults with Asperger’s syndrome or high-functioning autism. J Child Psychol Psychiatry 42:241–251PubMedCrossRef 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, adults with Asperger’s syndrome or high-functioning autism. J Child Psychol Psychiatry 42:241–251PubMedCrossRef
17.
go back to reference Duff K, Paulsen JS, Beglinger LJ, Langbehn DR, Stout JC, Predict-HD Investigators of the Huntington Study Group (2010) Frontal behaviours before the diagnosis of Huntington’s disease and their relationship to markers of disease progression: evidence of early lack of awareness. J Neuropsychiatry Clin Neurosci 22:196–207PubMedCentralPubMedCrossRef Duff K, Paulsen JS, Beglinger LJ, Langbehn DR, Stout JC, Predict-HD Investigators of the Huntington Study Group (2010) Frontal behaviours before the diagnosis of Huntington’s disease and their relationship to markers of disease progression: evidence of early lack of awareness. J Neuropsychiatry Clin Neurosci 22:196–207PubMedCentralPubMedCrossRef
18.
go back to reference Henry JD, Phillips LH, Crawford JR, Ietswaart M, Summers F (2006) Theory of mind following traumatic brain injury: the role of emotion recognition and executive dysfunction. Neuropsychologia 44:1623–1628PubMedCrossRef Henry JD, Phillips LH, Crawford JR, Ietswaart M, Summers F (2006) Theory of mind following traumatic brain injury: the role of emotion recognition and executive dysfunction. Neuropsychologia 44:1623–1628PubMedCrossRef
19.
go back to reference Saltzman J, Strauss E, Hunter M, Archibald S (2000) Theory of mind and executive functions in normal human aging and Parkinson’s disease. J Int Neuropsychol Soc 6:781–788PubMedCrossRef Saltzman J, Strauss E, Hunter M, Archibald S (2000) Theory of mind and executive functions in normal human aging and Parkinson’s disease. J Int Neuropsychol Soc 6:781–788PubMedCrossRef
20.
go back to reference Fine C, Lumsden J, Blair RJ (2001) Dissociation between ‘theory of mind’ and executive functions in a patient with early left amygdala damage. Brain 124:287–298PubMedCrossRef Fine C, Lumsden J, Blair RJ (2001) Dissociation between ‘theory of mind’ and executive functions in a patient with early left amygdala damage. Brain 124:287–298PubMedCrossRef
21.
go back to reference Shamay-Tsoory SG, Aharon-Peretz J (2007) Dissociable prefrontal networks for cognitive and affective theory of mind: a lesion study. Neuropsychologia 45:3054–3067PubMedCrossRef Shamay-Tsoory SG, Aharon-Peretz J (2007) Dissociable prefrontal networks for cognitive and affective theory of mind: a lesion study. Neuropsychologia 45:3054–3067PubMedCrossRef
22.
go back to reference Shamay-Tsoory SG, Aharon-Peretz J, Perry D (2009) Two systems for empathy: a double dissociation between emotional and cognitive empathy in inferior frontal gyrus versus ventromedial prefrontal lesions. Brain 132:617–627PubMedCrossRef Shamay-Tsoory SG, Aharon-Peretz J, Perry D (2009) Two systems for empathy: a double dissociation between emotional and cognitive empathy in inferior frontal gyrus versus ventromedial prefrontal lesions. Brain 132:617–627PubMedCrossRef
23.
go back to reference Kessler K, Rutherford H (2010) The two forms of visuo-spatial perspective taking are differently embodied and subserve different spatial prepositions. Front Psychol 1:213 Kessler K, Rutherford H (2010) The two forms of visuo-spatial perspective taking are differently embodied and subserve different spatial prepositions. Front Psychol 1:213
24.
go back to reference Davis MH (1980) A multidimensional approach to individual differences in empathy. JSAS Cat Sel Doc Psychol 10:85 Davis MH (1980) A multidimensional approach to individual differences in empathy. JSAS Cat Sel Doc Psychol 10:85
25.
go back to reference Klöppel S, Stonnington CM, Petrovic P, Mobbs D, Tüscher O, Craufurd D et al (2010) Irritability in pre-clinical Huntington’s disease. Neuropsychologia 48:549–557PubMedCentralPubMedCrossRef Klöppel S, Stonnington CM, Petrovic P, Mobbs D, Tüscher O, Craufurd D et al (2010) Irritability in pre-clinical Huntington’s disease. Neuropsychologia 48:549–557PubMedCentralPubMedCrossRef
26.
go back to reference Stone VE, Baron-Cohen S, Knight RT (1998) Frontal lobe contributions to theory of mind. J Cogn Neurosci 10:640–656PubMedCrossRef Stone VE, Baron-Cohen S, Knight RT (1998) Frontal lobe contributions to theory of mind. J Cogn Neurosci 10:640–656PubMedCrossRef
27.
go back to reference Folstein MF, Folstein SE, McHugh PR (1975) Mini-mental state. A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12:189–198PubMedCrossRef Folstein MF, Folstein SE, McHugh PR (1975) Mini-mental state. A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12:189–198PubMedCrossRef
28.
go back to reference Lezak M (1995) Neuropsychological assessment. Oxford University Press, New York Lezak M (1995) Neuropsychological assessment. Oxford University Press, New York
29.
go back to reference Cooper JA, Sagar HJ, Jordan N, Harvey NS, Sullivan EV (1991) Cognitive impairment in early untreated Parkinson’s disease and its relationship to motor disability. Brain 114:2095–2122PubMedCrossRef Cooper JA, Sagar HJ, Jordan N, Harvey NS, Sullivan EV (1991) Cognitive impairment in early untreated Parkinson’s disease and its relationship to motor disability. Brain 114:2095–2122PubMedCrossRef
30.
go back to reference Werheid K, Hoppe C, Thöne A, Müller U, Müngersdorf M, von Yves Cramon D (2002) The adaptive digit ordering test: clinical application, reliability, and validity of a verbal working memory test. Arch Clin Neuropsychol 17:547–565PubMedCrossRef Werheid K, Hoppe C, Thöne A, Müller U, Müngersdorf M, von Yves Cramon D (2002) The adaptive digit ordering test: clinical application, reliability, and validity of a verbal working memory test. Arch Clin Neuropsychol 17:547–565PubMedCrossRef
31.
go back to reference Reitan RM, Wolfson D (1985) The Halstead–Reitan neuropsychological test battery: therapy and clinical interpretation. Neuropsychological Press, Tucson Reitan RM, Wolfson D (1985) The Halstead–Reitan neuropsychological test battery: therapy and clinical interpretation. Neuropsychological Press, Tucson
32.
go back to reference Stroop JR (1935) Studies of interference in serial verbal reactions. J Exp Psychol 18:643–662CrossRef Stroop JR (1935) Studies of interference in serial verbal reactions. J Exp Psychol 18:643–662CrossRef
33.
go back to reference Lezak MD, Howieson DB, Loring DW (2004) Neuropsychological assessment. Oxford University Press, New York Lezak MD, Howieson DB, Loring DW (2004) Neuropsychological assessment. Oxford University Press, New York
34.
go back to reference Stone VE, Baron-Cohen S, Knight RT (1998) Frontal lobe contributions to theory of mind. J Cogn Neurosci 10:640–656CrossRef Stone VE, Baron-Cohen S, Knight RT (1998) Frontal lobe contributions to theory of mind. J Cogn Neurosci 10:640–656CrossRef
35.
go back to reference Piaget J, Inhelder B (1967) The child’s conception of space. Norton & Co, New York Piaget J, Inhelder B (1967) The child’s conception of space. Norton & Co, New York
36.
go back to reference Huntington Study Group (1996) Unified Huntington’s Disease Rating Scale: reliability and consistency. Mov Disord 11:136–142CrossRef Huntington Study Group (1996) Unified Huntington’s Disease Rating Scale: reliability and consistency. Mov Disord 11:136–142CrossRef
37.
go back to reference Ware JE Jr, Sherbourne CD (1992) The MOS 36-item short form health survey (SF-36) I. Conceptual framework and item selection. Med Care 30:473–483PubMedCrossRef Ware JE Jr, Sherbourne CD (1992) The MOS 36-item short form health survey (SF-36) I. Conceptual framework and item selection. Med Care 30:473–483PubMedCrossRef
38.
go back to reference Craufurd D, Thompson JC, Snowden JS (2001) Behavioural changes in Huntington’s disease. Neuropsychiatry Neuropsychol Behav Neurol 14:219–226PubMed Craufurd D, Thompson JC, Snowden JS (2001) Behavioural changes in Huntington’s disease. Neuropsychiatry Neuropsychol Behav Neurol 14:219–226PubMed
39.
go back to reference Stone VE, Baron-Cohen S, Calder A, Keane J, Young A (2003) Acquired theory of mind impairments in individuals with bilateral amygdala lesions. Neuropsychologia 41:209–220PubMedCrossRef Stone VE, Baron-Cohen S, Calder A, Keane J, Young A (2003) Acquired theory of mind impairments in individuals with bilateral amygdala lesions. Neuropsychologia 41:209–220PubMedCrossRef
40.
go back to reference Lambrey S, Doeller C, Berthoz A, Burgess N (2012) Imagining being somewhere else: neural basis of changing perspective in space. Cereb Cortex 22:166–174PubMedCrossRef Lambrey S, Doeller C, Berthoz A, Burgess N (2012) Imagining being somewhere else: neural basis of changing perspective in space. Cereb Cortex 22:166–174PubMedCrossRef
41.
go back to reference Ho AK, Robbins AO, Barker RA (2006) Huntington’s disease patients have selective problems with insight. Mov Disord 21(3):385–389PubMedCrossRef Ho AK, Robbins AO, Barker RA (2006) Huntington’s disease patients have selective problems with insight. Mov Disord 21(3):385–389PubMedCrossRef
42.
go back to reference Clark VP, Lai S, Wallace Deckel A (2002) Altered functional MRI responses in Huntington’s disease. NeuroReport 13:703–706PubMedCrossRef Clark VP, Lai S, Wallace Deckel A (2002) Altered functional MRI responses in Huntington’s disease. NeuroReport 13:703–706PubMedCrossRef
43.
go back to reference Novak MJU, Warren JD, Henley SMD, Draganski B, Frackowiak RS, Tabrizi SJ (2012) Altered brain mechanisms of emotion processing in premanifest Huntington’s disease. Brain 135:1165–1179PubMedCentralPubMedCrossRef Novak MJU, Warren JD, Henley SMD, Draganski B, Frackowiak RS, Tabrizi SJ (2012) Altered brain mechanisms of emotion processing in premanifest Huntington’s disease. Brain 135:1165–1179PubMedCentralPubMedCrossRef
44.
go back to reference Blekher T, Weaver MR, Marshall J, Hui S, Jackson JG, Stout JC, Beristain X, Wojcieszek J, Yee RD, Foroud TM (2009) Visual scanning and cognitive performance in prediagnostic and early stage Huntington’s disease. Mov Disord 24:533–540PubMedCentralPubMedCrossRef Blekher T, Weaver MR, Marshall J, Hui S, Jackson JG, Stout JC, Beristain X, Wojcieszek J, Yee RD, Foroud TM (2009) Visual scanning and cognitive performance in prediagnostic and early stage Huntington’s disease. Mov Disord 24:533–540PubMedCentralPubMedCrossRef
45.
go back to reference van Asselen M, Júlio F, Januário C, Campos EB, Almeida I, Cavaco S, Castelo-Branco M (2012) Scanning patterns of faces do not explain impaired emotion recognition in huntington disease: evidence for a high level mechanism. Front Psychol 3:31PubMedCentralPubMed van Asselen M, Júlio F, Januário C, Campos EB, Almeida I, Cavaco S, Castelo-Branco M (2012) Scanning patterns of faces do not explain impaired emotion recognition in huntington disease: evidence for a high level mechanism. Front Psychol 3:31PubMedCentralPubMed
Metadata
Title
Putting things into perspective: the nature and impact of theory of mind impairment in Huntington’s disease
Authors
Clare M. Eddy
Sridevi Sira Mahalingappa
Hugh E. Rickards
Publication date
01-12-2014
Publisher
Springer Berlin Heidelberg
Published in
European Archives of Psychiatry and Clinical Neuroscience / Issue 8/2014
Print ISSN: 0940-1334
Electronic ISSN: 1433-8491
DOI
https://doi.org/10.1007/s00406-014-0498-4

Other articles of this Issue 8/2014

European Archives of Psychiatry and Clinical Neuroscience 8/2014 Go to the issue