Impaired recognition of body expressions in the behavioral variant of frontotemporal dementia

Progressive deterioration of social cognition and emotion processing are core symptoms of the behavioral variant of frontotemporal dementia (bvFTD). Here we investigate whether bvFTD is also associated with impaired recognition of static (Experiment 1) and dynamic (Experiment 2) bodily expressions. In addition, we compared body expression processing with processing of static (Experiment 3) and dynamic (Experiment 4) facial expressions, as well as with face identity processing (Experiment 5). The results reveal that bvFTD is associated with impaired recognition of static and dynamic bodily and facial expressions, while identity processing was intact. No differential impairments were observed regarding motion (static vs. dynamic) or category (body vs. face). Within the bvFTD group, we observed a significant partial correlation between body and face expression recognition, when controlling for performance on the identity task. Voxel-Based Morphometry (VBM) analysis revealed that body emotion recognition was positively associated with gray matter volume in a region of the inferior frontal gyrus (pars orbitalis/triangularis). The results are in line with a supramodal emotion recognition deficit in bvFTD.

[1]  B. Gelder,et al.  Emotional information in body and background hampers recognition memory for faces , 2012, Neurobiology of Learning and Memory.

[2]  L. Leyman,et al.  The Karolinska Directed Emotional Faces: A validation study , 2008 .

[3]  N. Hadjikhani,et al.  Fear fosters flight: a mechanism for fear contagion when perceiving emotion expressed by a whole body. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[4]  Beatrice de Gelder,et al.  Moving and Being Moved: The Importance of Dynamic Information in Clinical Populations , 2010 .

[5]  B. Gelder,et al.  Why bodies? Twelve reasons for including bodily expressions in affective neuroscience , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[6]  Y. Levy,et al.  Interactive Processes in Matching Identity and Expressions of Unfamiliar Faces: Evidence for Mutual Facilitation Effects , 2008, Perception.

[7]  S. Schweinberger,et al.  Expression Influences the Recognition of Familiar Faces , 2004, Perception.

[8]  B. Miller,et al.  Classification of primary progressive aphasia and its variants , 2011, Neurology.

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

[10]  J. Grèzes,et al.  Emotional modulation of visual and motor areas by dynamic body expressions of anger , 2008, Social neuroscience.

[11]  Beatrice de Gelder,et al.  The Bodily Expressive Action Stimulus Test (BEAST). Construction and validation of a stimulus basis for measuring perception of whole body expression of emotions , 2011 .

[12]  Qingyang Li,et al.  Emotional perception: Meta-analyses of face and natural scene processing , 2011, NeuroImage.

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

[14]  A. Kertesz,et al.  Functional neural correlates of emotional expression processing deficits in behavioural variant frontotemporal dementia. , 2013, Journal of psychiatry & neuroscience : JPN.

[15]  B. de Gelder,et al.  Configuration perception and face memory , and face context effects in developmental prosopagnosia , 2013 .

[16]  Nick C Fox,et al.  Sensitivity of revised diagnostic criteria for the behavioural variant of frontotemporal dementia. , 2011, Brain : a journal of neurology.

[17]  Olivier Piguet,et al.  Tracking the progression of social cognition in neurodegenerative disorders , 2014, Journal of Neurology, Neurosurgery & Psychiatry.

[18]  J R Hodges,et al.  Incidence of early-onset dementias in Cambridgeshire, United Kingdom , 2008, Neurology.

[19]  Beatrice de Gelder,et al.  Neural Correlates of Perceiving Emotional Faces and Bodies in Developmental Prosopagnosia: An Event-Related fMRI-Study , 2008, PloS one.

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

[21]  Julie Grèzes,et al.  Specific and common brain regions involved in the perception of faces and bodies and the representation of their emotional expressions , 2009, Social neuroscience.

[22]  B. Gelder.  Towards the neurobiology of emotional body language , 2006, Nature Reviews Neuroscience.

[23]  D. Tranel,et al.  Positive facial affect facilitates the identification of famous faces , 2005, Brain and Language.

[24]  Sandra E. Black,et al.  Impaired recognition of negative facial emotions in patients with frontotemporal dementia , 2005, Neuropsychologia.

[25]  B. Miller,et al.  Anterior temporal lobe degeneration produces widespread network-driven dysfunction. , 2013, Brain : a journal of neurology.

[26]  Christian Keysers,et al.  Neural activities during affective processing in people with Alzheimer's disease , 2013, Neurobiology of Aging.

[27]  B. Dubois,et al.  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 , 2012, Journal of the International Neuropsychological Society.

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

[29]  J. Hodges,et al.  Discrete Neural Correlates for the Recognition of Negative Emotions: Insights from Frontotemporal Dementia , 2013, PloS one.

[30]  J. Hodges,et al.  Behavioural-variant frontotemporal dementia: diagnosis, clinical staging, and management , 2011, The Lancet Neurology.

[31]  Swann Pichon,et al.  Similarities and differences in perceiving threat from dynamic faces and bodies. An fMRI study , 2011, NeuroImage.

[32]  J. Gross,et al.  Empathy for positive and negative emotions in social anxiety disorder. , 2016, Behaviour research and therapy.

[33]  Matthew L Senjem,et al.  Distinct anatomical subtypes of the behavioural variant of frontotemporal dementia: a cluster analysis study. , 2009, Brain : a journal of neurology.

[34]  M. Kret,et al.  Emotion processing deficits: A liability spectrum providing insight into comorbidity of mental disorders , 2015, Neuroscience & Biobehavioral Reviews.

[35]  Marco Tamietto,et al.  Standing up for the body. Recent progress in uncovering the networks involved in the perception of bodies and bodily expressions , 2010, Neuroscience & Biobehavioral Reviews.

[36]  Martin A. Giese,et al.  Dynamic Faces: Insights from Experiments and Computation , 2010 .

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

[38]  D. Neary,et al.  Emotion recognition in Huntington's disease and frontotemporal dementia , 2008, Neuropsychologia.

[39]  K. Lander,et al.  Matching Faces with Emotional Expressions , 2011, Front. Psychology.

[40]  Béatrice de Gelder,et al.  Dissimilar processing of emotional facial expressions in human and monkey temporal cortex , 2013, NeuroImage.

[41]  J. Grèzes,et al.  Men Fear Other Men Most: Gender Specific Brain Activations in Perceiving Threat from Dynamic Faces and Bodies – An fMRI Study , 2010, Front. Psychology.

[42]  B. de Gelder,et al.  Body expressions influence recognition of emotions in the face and voice. , 2007, Emotion.

[43]  Béatrice de Gelder,et al.  Lateralization for dynamic facial expressions in human superior temporal sulcus , 2015, NeuroImage.

[44]  J. Hodges,et al.  Recognition of Positive Vocalizations Is Impaired in Behavioral-Variant Frontotemporal Dementia , 2013, Journal of the International Neuropsychological Society.

[45]  A. Drzezga,et al.  Imaging Frontotemporal Lobar Degeneration , 2014, Current Neurology and Neuroscience Reports.

[46]  O. Piguet,et al.  Disturbance of Emotion Processing in Frontotemporal Dementia: A Synthesis of Cognitive and Neuroimaging Findings , 2012, Neuropsychology Review.

[47]  Maria Luisa Gorno-Tempini,et al.  Frontal paralimbic network atrophy in very mild behavioral variant frontotemporal dementia. , 2008, Archives of neurology.

[48]  J. Hodges,et al.  One size does not fi t all : Face emotion processing impairments in semantic dementia , behavioural-variant frontotemporal dementia and Alzheimer ’ s disease are mediated by distinct cognitive de fi cits , 2014 .

[49]  Swann Pichon,et al.  Perceiving fear in dynamic body expressions , 2007, NeuroImage.

[50]  Gudrun Wacker.  Similarities and Differences , 2005 .

[51]  Garrison W. Cottrell,et al.  Transmitting and Decoding Facial Expressions , 2005, Psychological science.

[52]  Christian Keysers,et al.  Empathy for positive and negative emotions in the gustatory cortex , 2007, NeuroImage.

[53]  Claus Lamm,et al.  Meta-analytic evidence for common and distinct neural networks associated with directly experienced pain and empathy for pain , 2011, NeuroImage.

[54]  S. Baez,et al.  Structural neuroimaging of social cognition in progressive non-fluent aphasia and behavioral variant of frontotemporal dementia , 2013, Front. Hum. Neurosci..

[55]  A. Young,et al.  Configural information in facial expression perception. , 2000, Journal of experimental psychology. Human perception and performance.

[56]  Sophie K. Scott,et al.  The structural neuroanatomy of music emotion recognition: Evidence from frontotemporal lobar degeneration , 2011, NeuroImage.

[57]  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.

[58]  Y. Trope,et al.  Body Cues, Not Facial Expressions, Discriminate Between Intense Positive and Negative Emotions , 2012, Science.

[59]  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.

[60]  J. Hodges,et al.  One Size Does Not Fit All: Face Emotion Processing Impairments in Semantic Dementia, Behavioural-Variant Frontotemporal Dementia and Alzheimer’s Disease Are Mediated by Distinct Cognitive Deficits , 2011, Behavioural neurology.

[61]  Howard J. Rosen,et al.  Neuroanatomical correlates of impaired recognition of emotion in dementia , 2006, Neuropsychologia.

[62]  G. Rhodes,et al.  Do I know you? Examining face and object memory in frontotemporal dementia , 2015, Neuropsychologia.

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

[64]  Beatrice ede Gelder,et al.  Face identity matching is influenced by emotions conveyed by face and body , 2014, Front. Hum. Neurosci..

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