Social Mind Representation: Where Does It Fail in Frontotemporal Dementia?

We aimed at investigating social disability and its cerebral correlates in frontotemporal dementia (FTD). To do so, we contrasted answers of patients with early-stage FTD and of their relatives on personality trait judgment and on behavior prediction in social and emotional situations. Such contrasts were compared to control contrasts calculated with answers of matched controls tested with their relatives. In addition, brain metabolism was measured in patients with positron emission tomography and the [18F]fluorodeoxyglucose method. Patients turned out to be as accurate as controls in describing their relative's personality, but they failed to predict their relative's behavior in social and emotional circumstances. Concerning the self, patients were impaired both in current personality assessment and in prediction of their own behavior. Those two self-evaluation measures did not correlate. Only patients' anosognosia for social behavioral disability was found to be related to decreased metabolic activity in the left temporal pole. Such results suggest that anosognosia for social disability in FTD originates in impaired processing of emotional autobiographical information, leading to a self-representation that does not match current behavior. Moreover, we propose that perspective-taking disability participates in anosognosia, preventing patients from correcting their inaccurate self-representation based on their relative's perspective.

[1]  S. Klein,et al.  Self-Knowledge of an Amnesic Patient : Toward a Neuropsychology of Personality and Social Psychology , 2001 .

[2]  Joel H Kramer,et al.  Patterns of Cognitive and Emotional Empathy in Frontotemporal Lobar Degeneration , 2005, Cognitive and behavioral neurology : official journal of the Society for Behavioral and Cognitive Neurology.

[3]  Karl Herholz,et al.  Predominant ventromedial frontopolar metabolic impairment in frontotemporal dementia , 2003, NeuroImage.

[4]  K. Boone,et al.  A study of the Lund‐Manchester research criteria for frontotemporal dementia , 1997, Neurology.

[5]  Tetsuya Matsuda,et al.  Brain activation associated with evaluative processes of guilt and embarrassment: an fMRI study , 2004, NeuroImage.

[6]  Ian Nimmo-Smith,et al.  Anosognosia for Plegia: Specificity, Extension, Partiality and Disunity of Bodily Unawareness , 2004, Cortex.

[7]  Sandra Weintraub,et al.  Self-awareness and self-monitoring of cognitive and behavioral deficits in behavioral variant frontotemporal dementia, primary progressive aphasia and probable Alzheimer’s disease , 2008, Brain and Cognition.

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

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

[10]  Y. Joanette,et al.  [Formal and semantic lexical evocation in normal subjects. Performance and dynamics of production as a function of sex, age and educational level]. , 1990, Acta neurologica Belgica.

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

[12]  R. Robinson,et al.  Specificity of changes in cerebral blood flow in patients with frontal lobe dementia. , 1994, Journal of neurology, neurosurgery, and psychiatry.

[13]  F. Pasquier,et al.  Perception of emotion in frontotemporal dementia and Alzheimer disease. , 1999, Alzheimer disease and associated disorders.

[14]  J. Lowe,et al.  The new neuropathology of degenerative frontotemporal dementias , 2009, Acta Neuropathologica.

[15]  T. Gilovich,et al.  The spotlight effect in social judgment: an egocentric bias in estimates of the salience of one's own actions and appearance. , 2000, Journal of personality and social psychology.

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

[17]  M. Freedman,et al.  Frontotemporal lobar degeneration , 1998, Neurology.

[18]  Howard J. Rosen,et al.  Recognition of Emotion in the Frontal and Temporal Variants of Frontotemporal Dementia , 2004, Dementia and Geriatric Cognitive Disorders.

[19]  Kristi A. Costabile,et al.  Preserved Knowledge of Self in a Case of Alzheimer's Dementia , 2003 .

[20]  Karl Herholz,et al.  Neural correlates of anosognosia for cognitive impairment in Alzheimer's disease , 2006, Human brain mapping.

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

[22]  B. Berger,et al.  Characterization of Empathy Deficits following Prefrontal Brain Damage: The Role of the Right Ventromedial Prefrontal Cortex , 2003, Journal of Cognitive Neuroscience.

[23]  Dana Samson,et al.  Left temporoparietal junction is necessary for representing someone else's belief , 2004, Nature Neuroscience.

[24]  J. Decety,et al.  What you believe versus what you think they believe: a neuroimaging study of conceptual perspective‐taking , 2003, The European journal of neuroscience.

[25]  G. Glover,et al.  Reflecting upon Feelings: An fMRI Study of Neural Systems Supporting the Attribution of Emotion to Self and Other , 2004, Journal of Cognitive Neuroscience.

[26]  J. Constantinidis,et al.  Pick’s Disease , 1974 .

[27]  A. Alavi,et al.  Language comprehension and regional cerebral defects in frontotemporal degeneration and Alzheimer's disease , 1998, Neurology.

[28]  A. Meltzoff.  Origins of theory of mind, cognition and communication. , 1999, Journal of communication disorders.

[29]  R. Leiguarda,et al.  Anosognosia in Alzheimer's disease: a study of associated factors. , 1995, The Journal of neuropsychiatry and clinical neurosciences.

[30]  N. Anderson.  Likableness ratings of 555 personality-trait words. , 1968, Journal of personality and social psychology.

[31]  Dana Samson,et al.  Seeing it my way: a case of a selective deficit in inhibiting self-perspective. , 2005, Brain : a journal of neurology.

[32]  J. Gee,et al.  Neural basis for sentence comprehension deficits in frontotemporal dementia , 2003, Brain and Language.

[33]  Gereon R Fink,et al.  Differential remoteness and emotional tone modulate the neural correlates of autobiographical memory. , 2003, Brain : a journal of neurology.

[34]  N. Costes,et al.  Emotional Responses to Pleasant and Unpleasant Olfactory, Visual, and Auditory Stimuli: a Positron Emission Tomography Study , 2000, The Journal of Neuroscience.

[35]  J. Decety,et al.  How Would You Feel versus How Do You Think She Would Feel? A Neuroimaging Study of Perspective-Taking with Social Emotions , 2004, Journal of Cognitive Neuroscience.

[36]  Matthew Brett,et al.  The neural basis of autobiographical and semantic memory: New evidence from three PET studies , 2003, Cognitive, affective & behavioral neuroscience.

[37]  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.

[38]  Glyn W. Humphreys,et al.  Frontal and Temporo-Parietal Lobe Contributions to Theory of Mind: Neuropsychological Evidence from a False-Belief Task with Reduced Language and Executive Demands , 2004, Journal of Cognitive Neuroscience.

[39]  E. Maguire,et al.  The functional neuroanatomy of comprehension and memory: the importance of prior knowledge. , 1999, Brain : a journal of neurology.

[40]  H. Brownell,et al.  Acquired `theory of mind' impairments following stroke , 1999, Cognition.

[41]  J. Decety,et al.  Effect of subjective perspective taking during simulation of action: a PET investigation of agency , 2001, Nature Neuroscience.

[42]  Tim Shallice,et al.  Bizarre Responses, Rule Detection and Frontal Lobe Lesions , 1996, Cortex.

[43]  Mark H. Davis,et al.  Effect of perspective taking on the cognitive representation of persons: a merging of self and other. , 1996, Journal of personality and social psychology.

[44]  D. Perani,et al.  Anosognosia in Very Mild Alzheimer’s Disease but Not in Mild Cognitive Impairment , 2005, Dementia and Geriatric Cognitive Disorders.

[45]  Florence Pasquier,et al.  The Clinical Picture of Frontotemporal Dementia: Diagnosis and Follow-Up , 1999, Dementia and Geriatric Cognitive Disorders.

[46]  Martial Van der Linden,et al.  Self-referential reflective activity and its relationship with rest: a PET study , 2005, NeuroImage.

[47]  J. Stroop.  Studies of interference in serial verbal reactions. , 1992 .

[48]  Robert C. Gardner,et al.  Ethnic stereotypes: Norms on 208 words typically used in their assessment. , 1972 .

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

[50]  Karl J. Friston,et al.  Decreases in Regional Cerebral Blood Flow with Normal Aging , 1991, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

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

[52]  J. Decety,et al.  Functional anatomy of execution, mental simulation, observation, and verb generation of actions: A meta‐analysis , 2001, Human brain mapping.

[53]  Virginia S. Y. Kwan,et al.  Assessing the neural correlates of self-enhancement bias: a transcranial magnetic stimulation study , 2007, Experimental Brain Research.

[54]  John R. Hodges,et al.  Social reasoning, emotion and empathy in frontotemporal dementia , 2006, Neuropsychologia.

[55]  E. Tulving.  Self-knowledge of an amnesic individual is represented abstractly. , 1993 .

[56]  H. Sackeim,et al.  Parietal cortex and representation of the mental Self. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[57]  R. Dolan,et al.  Dissociable Temporal Lobe Activations during Emotional Episodic Memory Retrieval , 2000, NeuroImage.

[58]  Joel H Kramer,et al.  Double dissociation of social functioning in frontotemporal dementia , 2003, Neurology.

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

[60]  Andrew Kertesz,et al.  International approaches to frontotemporal dementia diagnosis: From social cognition to neuropsychology , 2003, Annals of neurology.

[61]  B. Mensour,et al.  Separate neural circuits for primary emotions? Brain activity during self-induced sadness and happiness in professional actors , 2003, Neuroreport.

[62]  Dominic Abrams,et al.  Self-attention and the egocentric assumption of shared perspectives , 1993 .

[63]  R. Tissot,et al.  Pick's disease. Histological and clinical correlations. , 1974, European neurology.

[64]  O. Gambini,et al.  Theory of Mind in schizophrenia: First person vs third person perspective , 2004, Consciousness and Cognition.

[65]  Steven Laureys,et al.  Two aspects of impaired consciousness in Alzheimer's disease. , 2005, Progress in brain research.

[66]  G. Rizzolatti,et al.  A unifying view of the basis of social cognition , 2004, Trends in Cognitive Sciences.

[67]  Leda Cosmides,et al.  A SOCIAL-COGNITIVE NEUROSCIENCE ANALYSIS OF THE SELF , 2002 .

[68]  S. Laureys,et al.  Comparison of Impaired Subcortico-Frontal Metabolic Networks in Normal Aging, Subcortico-Frontal Dementia, and Cortical Frontal Dementia , 1999, NeuroImage.

[69]  C. Frith,et al.  Interacting minds--a biological basis. , 1999, Science.