Social reasoning, emotion and empathy in frontotemporal dementia

INTRODUCTION Social cognition is crucial for human interaction, and is markedly impaired in the frontal variant of frontotemporal dementia (fvFTD). The relationship of various aspects of social functioning, however, remains controversial in this group. METHODS Patients with fvFTD (n = 18), and matched controls (n = 13), were tested using tasks designed to assess their Theory of Mind (ToM), moral reasoning, emotion recognition and executive function. Caregivers documented changes in empathy compared to premorbid functioning. RESULTS We found marked impairments in the abilities of fvFTD patients, relative to controls, in ability to mentalise (ToM), which was evident on a cartoon test, but not on a story-based ToM task. Knowledge of social rules was intact, but moral reasoning was defective, and was due, in part, to an inability to rate the seriousness of moral and conventional transgressions appropriately. Executive function was impaired in this group, and compromised aspects of moral reasoning, but ToM performance was independent of this. Emotion recognition was globally impaired in fvFTD, but was particularly so for anger and disgust which may partly explain the difficulty these patients have with identifying social violations. Empathy, as rated by carers, was also shown to be abnormal. CONCLUSION It appears that social reasoning is disrupted in a number of ways in fvFTD, and the findings provide a basis for the understanding and further study of abnormal behaviour in this disease. The results are discussed in light of neuroimaging findings in studies of social cognition and the locus of pathology in fvFTD.

[1]  F. Happé An advanced test of theory of mind: Understanding of story characters' thoughts and feelings by able autistic, mentally handicapped, and normal children and adults , 1994, Journal of autism and developmental disorders.

[2]  C. Cliffordson The hierarchical structure of empathy: dimensional organization and relations to social functioning. , 2002, Scandinavian journal of psychology.

[3]  Jill Keane,et al.  Face and emotion processing in frontal variant frontotemporal dementia , 2002, Neuropsychologia.

[4]  E. Rolls,et al.  Face and voice expression identification in patients with emotional and behavioural changes following ventral frontal lobe damage , 1996, Neuropsychologia.

[5]  J. Kril,et al.  Clinicopathological Staging of Frontotemporal Dementia Severity: Correlation with Regional Atrophy , 2004, Dementia and Geriatric Cognitive Disorders.

[6]  R. Dolan,et al.  An fMRI study of intentional and unintentional (embarrassing) violations of social norms. , 2002, Brain : a journal of neurology.

[7]  Mark H. Davis,et al.  A Multidimensional Approach to Individual Differences in Empathy , 1980 .

[8]  Sarah Crawford,et al.  The effects of anterior lesions on performance on a story comprehension test: left anterior impairment on a theory of mind-type task , 2000, Neuropsychologia.

[9]  C. Frith,et al.  Functional imaging of ‘theory of mind’ , 2003, Trends in Cognitive Sciences.

[10]  Jordan Grafman,et al.  Functional Networks in Emotional Moral and Nonmoral Social Judgments , 2002, NeuroImage.

[11]  C. Frith,et al.  The appreciation of visual jokes in people with schizophrenia: a study of ‘mentalizing’ ability , 1997, Schizophrenia Research.

[12]  Guy B. Williams,et al.  Neural correlates of semantic and behavioural deficits in frontotemporal dementia , 2005, NeuroImage.

[13]  B L Miller,et al.  Patterns of brain atrophy in frontotemporal dementia and semantic dementia , 2002, Neurology.

[14]  K. Zilles,et al.  Mind Reading: Neural Mechanisms of Theory of Mind and Self-Perspective , 2001, NeuroImage.

[15]  R. R.James Brief Report : Morality in the Autistic Child , 2006 .

[16]  J. Hodges,et al.  Staging disease severity in pathologically confirmed cases of frontotemporal dementia , 2003, Neurology.

[17]  T. Robbins,et al.  Specific cognitive deficits in mild frontal variant frontotemporal dementia. , 1999, Brain : a journal of neurology.

[18]  Jennifer S. Beer,et al.  Hemispheric Dominance for Emotions, Empathy and Social Behaviour: Evidence from Right and Left Handers with Frontotemporal Dementia. , 2001, Neurocase.

[19]  L Cipolotti,et al.  Impaired social response reversal. A case of 'acquired sociopathy'. , 2000, Brain : a journal of neurology.

[20]  M. Dewey Autism and Asperger syndrome: Living with Asperger's syndrome , 1991 .

[21]  A. Lawrence,et al.  Functional neuroanatomy of emotions: A meta-analysis , 2003, Cognitive, affective & behavioral neuroscience.

[22]  Sasha Bozeat,et al.  Which neuropsychiatric and behavioural features distinguish frontal and temporal variants of frontotemporal dementia from Alzheimer's disease? , 2000, Journal of neurology, neurosurgery, and psychiatry.

[23]  J. Perner,et al.  Development of theory of mind and executive control , 1999, Trends in Cognitive Sciences.

[24]  R. Blair,et al.  A cognitive developmental approach to morality: investigating the psychopath , 1995, Cognition.

[25]  D. Perrett,et al.  Dissociable neural responses to facial expressions of sadness and anger. , 1999, Brain : a journal of neurology.

[26]  A. Calder Facial Emotion Recognition after Bilateral Amygdala Damage: Differentially Severe Impairment of Fear , 1996 .

[27]  Carol Gregory,et al.  Dissociation of Social Cognition and Executive Function in Frontal Variant Frontotemporal Dementia. , 2001, Neurocase.

[28]  Helen Tager-Flusberg,et al.  The relationship of theory of mind and executive functions to symptom type and severity in children with autism , 2004, Development and Psychopathology.

[29]  Joshua D. Greene,et al.  How (and where) does moral judgment work? , 2002, Trends in Cognitive Sciences.

[30]  R. Blair,et al.  Dissociation between 'theory of mind' and executive functions in a patient with early left amygdala damage. , 2001, Brain : a journal of neurology.

[31]  Uta Frith,et al.  Theory of mind , 2001, Current Biology.

[32]  Tim Shallice,et al.  The Hayling and Brixton Tests , 1997 .

[33]  C. Polkey,et al.  "Theory of mind" impairments and their relationship to executive functioning following frontal lobe excisions. , 2001, Brain : a journal of neurology.

[34]  R. Knight,et al.  Frontal Lobe Contributions to Theory of Mind , 1998, Journal of Cognitive Neuroscience.

[35]  S. Baron-Cohen,et al.  The Empathy Quotient: An Investigation of Adults with Asperger Syndrome or High Functioning Autism, and Normal Sex Differences , 2004, Journal of autism and developmental disorders.

[36]  R. Faber,et al.  Frontotemporal lobar degeneration: a consensus on clinical diagnostic criteria. , 1999, Neurology.

[37]  C. Frith,et al.  Development and neurophysiology of mentalizing. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[38]  D. Neary,et al.  Social cognition in frontotemporal dementia and Huntington’s disease , 2003, Neuropsychologia.

[39]  K. Perryman,et al.  Neuropsychiatric features of frontotemporal dementia: evaluation of consensus criteria and review. , 2002, The Journal of neuropsychiatry and clinical neurosciences.

[40]  E. Rolls,et al.  Changes in emotion after circumscribed surgical lesions of the orbitofrontal and cingulate cortices. , 2003, Brain : a journal of neurology.

[41]  R. Blair,et al.  Brief report: Morality in the autistic child , 1996, Journal of autism and developmental disorders.

[42]  L. Moses,et al.  Individual differences in inhibitory control and children's theory of mind. , 2001, Child development.

[43]  Clinical and neuropathological criteria for frontotemporal dementia. The Lund and Manchester Groups. , 1994, Journal of neurology, neurosurgery, and psychiatry.

[44]  HighWire Press Philosophical Transactions of the Royal Society of London , 1781, The London Medical Journal.

[45]  C. Frith,et al.  Reading the mind in cartoons and stories: an fMRI study of ‘theory of mind’ in verbal and nonverbal tasks , 2000, Neuropsychologia.

[46]  E. Rolls The orbitofrontal cortex and reward. , 2000, Cerebral cortex.

[47]  Paul J. Eslinger,et al.  Neurological and Neuropsychological Bases of Empathy , 1998, European Neurology.

[48]  Istvan Molnar-Szakacs,et al.  Watching social interactions produces dorsomedial prefrontal and medial parietal BOLD fMRI signal increases compared to a resting baseline , 2004, NeuroImage.

[49]  S. Baron-Cohen,et al.  Theory of mind in patients with frontal variant frontotemporal dementia and Alzheimer's disease: theoretical and practical implications. , 2002, Brain : a journal of neurology.