Social cognitive deficits and their neural correlates in progressive supranuclear palsy

Although progressive supranuclear palsy is defined by its akinetic rigidity, vertical supranuclear gaze palsy and falls, cognitive impairments are an important determinant of patients’ and carers’ quality of life. Here, we investigate whether there is a broad deficit of modality-independent social cognition in progressive supranuclear palsy and explore the neural correlates for these. We recruited 23 patients with progressive supranuclear palsy (using clinical diagnostic criteria, nine with subsequent pathological confirmation) and 22 age- and education-matched controls. Participants performed an auditory (voice) emotion recognition test, and a visual and auditory theory of mind test. Twenty-two patients and 20 controls underwent structural magnetic resonance imaging to analyse neural correlates of social cognition deficits using voxel-based morphometry. Patients were impaired on the voice emotion recognition and theory of mind tests but not auditory and visual control conditions. Grey matter atrophy in patients correlated with both voice emotion recognition and theory of mind deficits in the right inferior frontal gyrus, a region associated with prosodic auditory emotion recognition. Theory of mind deficits also correlated with atrophy of the anterior rostral medial frontal cortex, a region associated with theory of mind in health. We conclude that patients with progressive supranuclear palsy have a multimodal deficit in social cognition. This deficit is due, in part, to progressive atrophy in a network of frontal cortical regions linked to the integration of socially relevant stimuli and interpretation of their social meaning. This impairment of social cognition is important to consider for those managing and caring for patients with progressive supranuclear palsy.

[1]  Bruce L. Miller,et al.  Comprehension of insincere communication in neurodegenerative disease: Lies, sarcasm, and theory of mind , 2012, Cortex.

[2]  Susanne Weis,et al.  The Neural Correlates of Emotional Prosody Comprehension: Disentangling Simple from Complex Emotion , 2011, PloS one.

[3]  C. Heyes,et al.  Science Perspectives on Psychological Mirror Neuron Forum on Behalf Of: Association for Psychological Science , 2022 .

[4]  M. Martory,et al.  Theory of mind tasks and executive functions: a systematic review of group studies in neurology. , 2011, Journal of neuropsychology.

[5]  John R Hodges,et al.  Cortical atrophy differentiates Richardson's syndrome from the parkinsonian form of progressive supranuclear palsy , 2011, Movement disorders : official journal of the Movement Disorder Society.

[6]  Philip J. Barnard,et al.  Emotional Complexity and the Neural Representation of Emotion in Motion , 2010, Social cognitive and affective neuroscience.

[7]  Sébastien Ourselin,et al.  Distinct profiles of brain atrophy in frontotemporal lobar degeneration caused by progranulin and tau mutations☆ , 2010, NeuroImage.

[8]  J. Hodges,et al.  Behavioural symptoms in progressive supranuclear palsy and frontotemporal dementia , 2010, Journal of Neurology, Neurosurgery & Psychiatry.

[9]  Y. Agid,et al.  Cognitive impairment in patients with multiple system atrophy and progressive supranuclear palsy. , 2010, Brain : a journal of neurology.

[10]  M. Peelen,et al.  Supramodal Representations of Perceived Emotions in the Human Brain , 2010, The Journal of Neuroscience.

[11]  A. Young,et al.  The relation between anger and different forms of disgust: Implications for emotion recognition impairments in Huntington's disease , 2010, Neuropsychologia.

[12]  M. Gorno-Tempini,et al.  Sound naming in neurodegenerative disease , 2010, Brain and Cognition.

[13]  Linda Tickle-Degnen,et al.  A meta-analysis of performance on emotion recognition tasks in Parkinson's disease. , 2010, Neuropsychology.

[14]  Sebastian Seifert,et al.  Orbito-frontal lesions cause impairment during late but not early emotional prosodic processing , 2010, Social neuroscience.

[15]  Ivan Enrici,et al.  Theory of mind ability in the behavioural variant of frontotemporal dementia: An analysis of the neural, cognitive, and social levels , 2010, Neuropsychologia.

[16]  C. Frith,et al.  Rapid Response Subject Collections , 2022 .

[17]  Daniel C. Javitt,et al.  “It's Not What You Say, But How You Say it”: A Reciprocal Temporo-frontal Network for Affective Prosody , 2009, Front. Hum. Neurosci..

[18]  John Duncan,et al.  Executive function and fluid intelligence after frontal lobe lesions , 2009, Brain : a journal of neurology.

[19]  David Rudrauf,et al.  Damage to Association Fiber Tracts Impairs Recognition of the Facial Expression of Emotion , 2009, The Journal of Neuroscience.

[20]  Katherine P. Rankin,et al.  Detecting sarcasm from paralinguistic cues: Anatomic and cognitive correlates in neurodegenerative disease , 2009, NeuroImage.

[21]  John Ashburner,et al.  Computational anatomy with the SPM software. , 2009, Magnetic resonance imaging.

[22]  A. Calder,et al.  Emotion recognition in progressive supranuclear palsy , 2009, Journal of Neurology, Neurosurgery & Psychiatry.

[23]  Henry S. Cheang,et al.  Acoustic markers of sarcasm in Cantonese and English. , 2009, The Journal of the Acoustical Society of America.

[24]  C. Keysers,et al.  Evidence for mirror systems in emotions , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[25]  A. Bailey,et al.  Are there theory of mind regions in the brain? A review of the neuroimaging literature , 2009, Human brain mapping.

[26]  J. Hodges,et al.  Emotion, social functioning and activities of daily living in frontotemporal dementia , 2009, Neurocase.

[27]  J R Hodges,et al.  Atrophy patterns in histologic vs clinical groupings of frontotemporal lobar degeneration , 2009, Neurology.

[28]  F. Van Overwalle Social cognition and the brain: A meta‐analysis , 2009, Human brain mapping.

[29]  J. Aharon-Peretz,et al.  Two systems for empathy: a double dissociation between emotional and cognitive empathy in inferior frontal gyrus versus ventromedial prefrontal lesions. , 2009, Brain : a journal of neurology.

[30]  J R Hodges,et al.  Understanding social dysfunction in the behavioural variant of frontotemporal dementia: the role of emotion and sarcasm processing. , 2009, Brain : a journal of neurology.

[31]  Guy B. Williams,et al.  Comparative Reliability of Total Intracranial Volume Estimation Methods and the Influence of Atrophy in a Longitudinal Semantic Dementia Cohort , 2009, Journal of neuroimaging : official journal of the American Society of Neuroimaging.

[32]  Y. Agid,et al.  Riluzole treatment, survival and diagnostic criteria in Parkinson plus disorders: The NNIPPS Study , 2008, Brain : a journal of neurology.

[33]  Raffaele Lodi,et al.  Diffusion-weighted brain imaging study of patients with clinical diagnosis of corticobasal degeneration, progressive supranuclear palsy and Parkinson's disease. , 2009, Brain : a journal of neurology.

[34]  Aldo Quattrone,et al.  Apparent diffusion coefficient of the superior cerebellar peduncle differentiates progressive supranuclear palsy from Parkinson's disease , 2008, Movement disorders : official journal of the Movement Disorder Society.

[35]  H. Fukuyama,et al.  Theory of mind and frontal lobe pathology in schizophrenia: A voxel-based morphometry study , 2008, Schizophrenia Research.

[36]  Paula Tavares,et al.  Paying attention to social meaning: an FMRI study. , 2008, Cerebral cortex.

[37]  Nick C. Fox,et al.  Defective emotion recognition in early HD is neuropsychologically and anatomically generic , 2008, Neuropsychologia.

[38]  B. Borroni,et al.  Cognitive and behavioral assessment in the early stages of neurodegenerative extrapyramidal syndromes. , 2008, Archives of gerontology and geriatrics.

[39]  F. Gosselin,et al.  The Montreal Affective Voices: A validated set of nonverbal affect bursts for research on auditory affective processing , 2008, Behavior research methods.

[40]  K. Scherer,et al.  The New Handbook of Methods in Nonverbal Behavior Research , 2008 .

[41]  Guy B. Williams,et al.  The impact of skull-stripping and radio-frequency bias correction on grey-matter segmentation for voxel-based morphometry , 2008, NeuroImage.

[42]  C. Jack,et al.  Voxel-based morphometry in autopsy proven PSP and CBD , 2008, Neurobiology of Aging.

[43]  Luke Clark,et al.  The relationship between affective decision-making and theory of mind in the frontal variant of fronto-temporal dementia , 2007, Neuropsychologia.

[44]  David J. Brooks,et al.  Impaired recognition of facial expressions of anger in Parkinson's disease patients acutely withdrawn from dopamine replacement therapy , 2007, Neuropsychologia.

[45]  W. Kamphorst,et al.  Frontal presentation in progressive supranuclear palsy , 2007, Neurology.

[46]  Gereon R. Fink,et al.  Mirror Neuron and Theory of Mind Mechanisms Involved in Face-to-Face Interactions: A Functional Magnetic Resonance Imaging Approach to Empathy , 2007, Journal of Cognitive Neuroscience.

[47]  M. Weiner,et al.  Emotional reactivity and emotion recognition in frontotemporal lobar degeneration , 2007, Neurology.

[48]  C. M. Kipps,et al.  Disgust and Happiness Recognition Correlate with Anteroventral Insula and Amygdala Volume Respectively in Preclinical Huntington's Disease , 2007, Journal of Cognitive Neuroscience.

[49]  L. Golbe,et al.  A clinical rating scale for progressive supranuclear palsy. , 2007, Brain : a journal of neurology.

[50]  Stefan Wagenpfeil,et al.  The Ekman 60 Faces Test as a diagnostic instrument in frontotemporal dementia. , 2007, Archives of clinical neuropsychology : the official journal of the National Academy of Neuropsychologists.

[51]  H. Reichmann,et al.  Prefrontal cortex dysfunction and depression in atypical parkinsonian syndromes , 2007, Movement disorders : official journal of the Movement Disorder Society.

[52]  Jean-Baptiste Poline,et al.  Analysis of a large fMRI cohort: Statistical and methodological issues for group analyses , 2007, NeuroImage.

[53]  P. Rockwell,et al.  Vocal Features of Conversational Sarcasm: A Comparison of Methods , 2007, Journal of psycholinguistic research.

[54]  Uta Noppeney,et al.  Temporal lobe lesions and semantic impairment: a comparison of herpes simplex virus encephalitis and semantic dementia. , 2006, Brain : a journal of neurology.

[55]  Anne Lacheret,et al.  FMRI study of emotional speech comprehension. , 2006, Cerebral cortex.

[56]  M. Heim SLO-rapport 'Hoe communiceer jij?' gaat voorbij aan bestaande kennis , 2007 .

[57]  S. Brockstedt,et al.  Tracking the neurodegeneration of parkinsonian disorders – a pilot study , 2007, Neuroradiology.

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

[59]  J. Decety,et al.  Social brain dysfunctions in schizophrenia: A review of neuroimaging studies , 2006, Psychiatry Research: Neuroimaging.

[60]  T. Johnstone,et al.  The voice of emotion: an FMRI study of neural responses to angry and happy vocal expressions. , 2006, Social cognitive and affective neuroscience.

[61]  C. Keysers,et al.  Empathy and the Somatotopic Auditory Mirror System in Humans , 2006, Current Biology.

[62]  M. Iacoboni,et al.  Getting a grip on other minds: Mirror neurons, intention understanding, and cognitive empathy , 2006, Social Neuroscience.

[63]  Daniel C Javitt,et al.  Theory of Mind (ToM) and counterfactuality deficits in schizophrenia: misperception or misinterpretation? , 2006, Psychological Medicine.

[64]  Nick C Fox,et al.  Regional brain volumes distinguish PSP, MSA‐P, and PD: MRI‐based clinico‐radiological correlations , 2006, Movement disorders : official journal of the Movement Disorder Society.

[65]  Stephen Lawrie,et al.  Functional Specialization within Rostral Prefrontal Cortex (Area 10): A Meta-analysis , 2006, Journal of Cognitive Neuroscience.

[66]  C. Frith,et al.  Meeting of minds: the medial frontal cortex and social cognition , 2006, Nature Reviews Neuroscience.

[67]  Nick C Fox,et al.  Longitudinal MRI in progressive supranuclear palsy and multiple system atrophy: rates and regions of atrophy. , 2006, Brain : a journal of neurology.

[68]  Michael Erb,et al.  Cerebral pathways in processing of affective prosody: A dynamic causal modeling study , 2006, NeuroImage.

[69]  D. Burn,et al.  Characterizing behavioral and cognitive dysexecutive changes in progressive supranuclear palsy , 2006, Movement disorders : official journal of the Movement Disorder Society.

[70]  S. Kotz,et al.  Beyond the right hemisphere: brain mechanisms mediating vocal emotional processing , 2006, Trends in Cognitive Sciences.

[71]  D Perani,et al.  Diffusion tensor imaging and voxel based morphometry study in early progressive supranuclear palsy , 2005, Journal of Neurology, Neurosurgery & Psychiatry.

[72]  Nick C Fox,et al.  Magnetic resonance imaging signatures of tissue pathology in frontotemporal dementia. , 2005, Archives of neurology.

[73]  Karl J. Friston,et al.  Unified segmentation , 2005, NeuroImage.

[74]  C. Pantelis,et al.  Clinical deficits correlate with regional cerebral atrophy in progressive supranuclear palsy. , 2005, Brain : a journal of neurology.

[75]  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.

[76]  Nick C Fox,et al.  Quantitative MRI measurement of superior cerebellar peduncle in progressive supranuclear palsy , 2005, Neurology.

[77]  Wolfgang Grodd,et al.  Identification of emotional intonation evaluated by fMRI , 2005, NeuroImage.

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

[79]  K. Scherer,et al.  Vocal expression of affect , 2005 .

[80]  Nick C Fox,et al.  Pathological substrate for regional distribution of increased atrophy rates in progressive supranuclear palsy , 2004, Journal of Neurology, Neurosurgery & Psychiatry.

[81]  Nick C. Fox,et al.  Voxel-based morphometry detects patterns of atrophy that help differentiate progressive supranuclear palsy and Parkinson's disease , 2004, NeuroImage.

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

[83]  A Weindl,et al.  Neural correlates associated with impaired disgust processing in pre-symptomatic Huntington's disease. , 2004, Brain : a journal of neurology.

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

[85]  G K Wenning,et al.  Voxel based morphometry reveals a distinct pattern of frontal atrophy in progressive supranuclear palsy , 2004, Journal of Neurology, Neurosurgery & Psychiatry.

[86]  Joseph A Maldjian,et al.  Precentral gyrus discrepancy in electronic versions of the Talairach atlas , 2004, NeuroImage.

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

[88]  Andrew Calder,et al.  Acquired theory of mind impairments in individuals with bilateral amygdala lesions , 2003, Neuropsychologia.

[89]  M. Jahanshahi,et al.  Health‐related quality of life in patients with progressive supranuclear palsy , 2003, Movement disorders : official journal of the Movement Disorder Society.

[90]  G. Rizzolatti,et al.  Both of Us Disgusted in My Insula The Common Neural Basis of Seeing and Feeling Disgust , 2003, Neuron.

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

[92]  R Saxe,et al.  People thinking about thinking people The role of the temporo-parietal junction in “theory of mind” , 2003, NeuroImage.

[93]  Paul J. Laurienti,et al.  An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets , 2003, NeuroImage.

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

[95]  Skye McDonald,et al.  TASIT: A New Clinical Tool for Assessing Social Perception After Traumatic Brain Injury , 2003, The Journal of head trauma rehabilitation.

[96]  I. McKeith,et al.  SIC Task Force appraisal of clinical diagnostic criteria for parkinsonian disorders , 2003, Movement disorders : official journal of the Movement Disorder Society.

[97]  Klaus R. Scherer,et al.  Vocal communication of emotion: A review of research paradigms , 2003, Speech Commun..

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

[99]  Mario Dzemidzic,et al.  A cross‐linguistic fMRI study of perception of intonation and emotion in Chinese , 2003, Human brain mapping.

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

[101]  Stephen M Smith,et al.  Fast robust automated brain extraction , 2002, Human brain mapping.

[102]  N. Schuff,et al.  Emotion comprehension in the temporal variant of frontotemporal dementia. , 2002, Brain : a journal of neurology.

[103]  M. Erb,et al.  Dynamic Brain Activation during Processing of Emotional Intonation: Influence of Acoustic Parameters, Emotional Valence, and Sex , 2002, NeuroImage.

[104]  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.

[105]  J. Currie,et al.  Frontal atrophy correlates with behavioural changes in progressive supranuclear palsy. , 2002, Brain : a journal of neurology.

[106]  N. Tzourio-Mazoyer,et al.  Automated Anatomical Labeling of Activations in SPM Using a Macroscopic Anatomical Parcellation of the MNI MRI Single-Subject Brain , 2002, NeuroImage.

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

[108]  Hanna Damasio,et al.  Neural systems for recognition of emotional prosody: a 3-D lesion study. , 2002, Emotion.

[109]  Anders M. Dale,et al.  A hybrid approach to the Skull Stripping problem in MRI , 2001, NeuroImage.

[110]  Andrew W. Young,et al.  Neuropsychology of fear and loathing , 2001, Nature Reviews Neuroscience.

[111]  I Litvan,et al.  Neuropsychiatric symptoms of patients with progressive supranuclear palsy and Parkinson's disease. , 2001, The Journal of neuropsychiatry and clinical neurosciences.

[112]  S. Baron-Cohen,et al.  The "Reading the Mind in the Eyes" Test revised version: a study with normal adults, and adults with Asperger syndrome or high-functioning autism. , 2001, Journal of child psychology and psychiatry, and allied disciplines.

[113]  A. Young,et al.  Impaired recognition and experience of disgust following brain injury , 2000, Nature Neuroscience.

[114]  J L Lancaster,et al.  Automated Talairach Atlas labels for functional brain mapping , 2000, Human brain mapping.

[115]  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.

[116]  G. Halliday,et al.  Regional brain atrophy in progressive supranuclear palsy and Lewy body disease , 2000, Annals of neurology.

[117]  K. Zilles,et al.  Recognition of emotional prosody and verbal components of spoken language: an fMRI study. , 2000, Brain research. Cognitive brain research.

[118]  R. Adolphs,et al.  A Role for Somatosensory Cortices in the Visual Recognition of Emotion as Revealed by Three-Dimensional Lesion Mapping , 2000, The Journal of Neuroscience.

[119]  K. Nakamura,et al.  Activation of the right inferior frontal cortex during assessment of facial emotion. , 1999, Journal of neurophysiology.

[120]  U. Eysel,et al.  Neural structures associated with recognition of facial expressions of basic emotions , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

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

[122]  J. Hodges,et al.  The neuropsychology of progressive supranuclear palsy , 1998 .

[123]  Alan C. Evans,et al.  A nonparametric method for automatic correction of intensity nonuniformity in MRI data , 1998, IEEE Transactions on Medical Imaging.

[124]  Jack L. Lancaster,et al.  The Talairach Daemon a database server for talairach atlas labels , 1997 .

[125]  D. Perrett,et al.  A specific neural substrate for perceiving facial expressions of disgust , 1997, Nature.

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

[127]  R. Adolphs,et al.  Cortical Systems for the Recognition of Emotion in Facial Expressions , 1996, The Journal of Neuroscience.

[128]  Jeffrey L. Cummings,et al.  Neuropsychiatric aspects of progressive supranuclear palsy , 1996, Neurology.

[129]  D. Perrett,et al.  Loss of disgust. Perception of faces and emotions in Huntington's disease. , 1996, Brain : a journal of neurology.

[130]  A. Calder Facial emotion recognition after bilateral amygdala damage: Differentially severe impairment of fear , 1996 .

[131]  K. Heilman,et al.  Understanding emotional prosody activates right hemisphere regions. , 1996, Archives of neurology.

[132]  I Litvan,et al.  Natural history of progressive supranuclear palsy (Steele-Richardson-Olszewski syndrome) and clinical predictors of survival: a clinicopathological study. , 1996, Journal of neurology, neurosurgery, and psychiatry.

[133]  J. Grafman,et al.  Neuropsychological Features of Progressive Supranuclear Palsy , 1995, Brain and Cognition.

[134]  R. Adolphs,et al.  Impaired recognition of emotion in facial expressions following bilateral damage to the human amygdala , 1994, Nature.

[135]  J. Russell Is there universal recognition of emotion from facial expression? A review of the cross-cultural studies. , 1994, Psychological bulletin.

[136]  D. Perl,et al.  Neuropathology of dementia. , 1986, Neurologic clinics.

[137]  Diane C. Tsai Recent Developments in Parkinson's Disease , 1986, The Yale Journal of Biology and Medicine.

[138]  Bruce Bowe The Face of Emotion , 1985 .

[139]  D. Premack,et al.  Does the chimpanzee have a theory of mind? , 1978, Behavioral and Brain Sciences.

[140]  P. Ekman Pictures of Facial Affect , 1976 .

[141]  J. Olszewski,et al.  SUPRANUCLEAR OPHTHALMOPLEGIA, PSEUDOBULBAR PALSY, NUCHAL DYSTONIA AND DEMENTIA. A CLINICAL REPORT ON EIGHT CASES OF "HETEROGENOUS SYSTEM DEGENERATION". , 1963, Transactions of the American Neurological Association.