Specific impairments in the recognition of emotional facial expressions in Parkinson's disease

Studies investigating the ability to recognize emotional facial expressions in non-demented individuals with Parkinson's disease (PD) have yielded equivocal findings. A possible reason for this variability may lie in the confounding of emotion recognition with cognitive task requirements, a confound arising from the lack of a control condition using non-emotional stimuli. The present study examined emotional facial expression recognition abilities in 20 non-demented patients with PD and 23 control participants relative to their performance on a non-emotional landscape categorization test with comparable task requirements. We found that PD participants were normal on the control task but exhibited selective impairments in the recognition of facial emotion, specifically for anger (driven by those with right hemisphere pathology) and surprise (driven by those with left hemisphere pathology), even when controlling for depression level. Male but not female PD participants further displayed specific deficits in the recognition of fearful expressions. We suggest that the neural substrates that may subserve these impairments include the ventral striatum, amygdala, and prefrontal cortices. Finally, we observed that in PD participants, deficiencies in facial emotion recognition correlated with higher levels of interpersonal distress, which calls attention to the significant psychosocial impact that facial emotion recognition impairments may have on individuals with PD.

[1]  N. Ambady,et al.  Effects of Gaze on Amygdala Sensitivity to Anger and Fear Faces , 2003, Science.

[2]  L. Obler,et al.  Right hemisphere emotional perception: evidence across multiple channels. , 1998, Neuropsychology.

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

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

[5]  S. Folstein,et al.  "Mini-mental state". A practical method for grading the cognitive state of patients for the clinician. , 1975, Journal of psychiatric research.

[6]  Francesco Fera,et al.  The Amygdala Response to Emotional Stimuli: A Comparison of Faces and Scenes , 2002, NeuroImage.

[7]  U. Hess,et al.  Impaired emotional facial expression recognition is associated with interpersonal problems in alcoholism. , 2002, Alcohol and alcoholism.

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

[9]  Rüdiger Hilker,et al.  Decision-Making Impairments in Patients with Parkinson’s Disease , 2005, Behavioural neurology.

[10]  Jennifer C. Britton,et al.  Facial expressions and complex IAPS pictures: Common and differential networks , 2006, NeuroImage.

[11]  Stephan Eliez,et al.  Amygdalar activation associated with positive and negative facial expressions , 2002, Neuroreport.

[12]  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.

[13]  E. Silberman,et al.  Hemispheric lateralization of functions related to emotion , 1986, Brain and Cognition.

[14]  J. Grace,et al.  Body side of motor symptom onset in Parkinson's disease is associated with memory performance , 2006, Journal of the International Neuropsychological Society.

[15]  Amanda Price Explicit category learning in Parkinson's disease: deficits related to impaired rule generation and selection processes. , 2006, Neuropsychology.

[16]  Francesco Fera,et al.  Dopamine Modulates the Response of the Human Amygdala: A Study in Parkinson's Disease , 2002, The Journal of Neuroscience.

[17]  Hervé Abdi,et al.  Processing Faces and Facial Expressions , 2003, Neuropsychology Review.

[18]  M Laruelle,et al.  Single photon emission computed tomographic imaging demonstrates loss of striatal dopamine transporters in Parkinson disease. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[19]  J. Missimer,et al.  Complementary positron emission tomographic studies of the striatal dopaminergic system in Parkinson's disease. , 1995, Archives of neurology.

[20]  R. Schiffer,et al.  Anxiety and Parkinson's disease. , 1996, The Journal of neuropsychiatry and clinical neurosciences.

[21]  Richard B. Ivry,et al.  Rule-Based Category Learning is Impaired in Patients with Parkinson's Disease but not in Patients with Cerebellar Disorders , 2005, Journal of Cognitive Neuroscience.

[22]  H Helenius,et al.  The quality of life in Parkinson's disease , 2000, Movement disorders : official journal of the Movement Disorder Society.

[23]  Jennifer A. Mangels,et al.  A Neostriatal Habit Learning System in Humans , 1996, Science.

[24]  A. Parent Extrinsic connections of the basal ganglia , 1990, Trends in Neurosciences.

[25]  D. Calne,et al.  Patterns of Asymmetry Do Not Change Over the Course of Idiopathic Parkinsonism , 1995, Neurology.

[26]  L. Horowitz,et al.  Inventory of interpersonal problems: psychometric properties and clinical applications. , 1988, Journal of consulting and clinical psychology.

[27]  L. Heimer,et al.  "Perestroika" in the basal forebrain: opening the border between neurology and psychiatry. , 1991, Progress in brain research.

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

[29]  W. Sato,et al.  Seeing Happy Emotion in Fearful and Angry Faces: Qualitative Analysis of Facial Expression Recognition in a Bilateral Amygdala-Damaged Patient , 2002, Cortex.

[30]  A. Benton Contributions to Neuropsychological Assessment: A Clinical Manual , 1983 .

[31]  A. Beck,et al.  An inventory for measuring clinical anxiety: psychometric properties. , 1988, Journal of consulting and clinical psychology.

[32]  Richard J. Davidson,et al.  Differential contributions of the two cerebral hemispheres to the perception of happy and sad faces , 1981, Neuropsychologia.

[33]  D. Rubinow,et al.  Impaired recognition of affect in facial expression in depressed patients , 1992, Biological Psychiatry.

[34]  M. Hoehn,et al.  Parkinsonism , 1967, Neurology.

[35]  Judith A. Hall,et al.  Gender differences in nonverbal communication of emotion , 2000 .

[36]  G. E. Alexander,et al.  Functional architecture of basal ganglia circuits: neural substrates of parallel processing , 1990, Trends in Neurosciences.

[37]  R. Adolphs,et al.  Hemispheric perception of emotional valence from facial expressions. , 2001, Neuropsychology.

[38]  R. Adolphs,et al.  Intact recognition of facial emotion in Parkinson's disease. , 1998, Neuropsychology.

[39]  Jill Keane,et al.  Impaired recognition of anger following damage to the ventral striatum. , 2004, Brain : a journal of neurology.

[40]  David I. Perrett,et al.  Amygdala response to facial expressions in children and adults , 2000, NeuroImage.

[41]  R. Adolphs Neural systems for recognizing emotion , 2002, Current Opinion in Neurobiology.

[42]  M. Pell,et al.  Facial expression decoding in early Parkinson's disease. , 2005, Brain research. Cognitive brain research.

[43]  J. Cummings,et al.  Depression in patients with Parkinson's disease , 1999, International journal of geriatric psychiatry.

[44]  S Z Rapcsak,et al.  Fear recognition deficits after focal brain damage: a cautionary note. , 2000, Neurology.

[45]  M. Mcdermott,et al.  The Ups and Downs of Parkinson Disease: A Prospective Study of Mood and Anxiety Fluctuations , 2004, Cognitive and behavioral neurology : official journal of the Society for Behavioral and Cognitive Neurology.

[46]  A J Lees,et al.  Asymmetry of substantia nigra neuronal loss in Parkinson's disease and its relevance to the mechanism of levodopa related motor fluctuations. , 1989, Journal of neurology, neurosurgery, and psychiatry.

[47]  Naomi Yatomi,et al.  Influence of Deteriorating Ability of Emotional Comprehension on Interpersonal Behavior in Alzheimer-Type Dementia , 2001, Brain and Cognition.

[48]  G. E. Alexander,et al.  Parallel organization of functionally segregated circuits linking basal ganglia and cortex. , 1986, Annual review of neuroscience.

[49]  Bastiaan R Bloem,et al.  Gender differences in Parkinson’s disease , 2006, Journal of Neurology, Neurosurgery & Psychiatry.

[50]  R. Pandey,et al.  Quality of life in patients with Parkinson's disease. , 2005, Parkinsonism & related disorders.

[51]  Satoshi Mochizuki,et al.  Recognition Of Emotion From Facial, Prosodic And Written Verbal Stimuli In Parkinson'S Disease , 2002, Cortex.

[52]  Edward T. Bullmore,et al.  A differential neural response to threatening and non-threatening negative facial expressions in paranoid and non-paranoid schizophrenics , 1999, Psychiatry Research: Neuroimaging.

[53]  Bernard Dan,et al.  Recognition of emotional facial expressions in attention-deficit hyperactivity disorder. , 2006, Pediatric neurology.

[54]  Kurt Jellinger,et al.  Amygdala pathology in Parkinson's disease , 2004, Acta Neuropathologica.

[55]  Shawn W. Ell,et al.  Category learning deficits in Parkinson's disease. , 2003, Neuropsychology.

[56]  W. T. Maddox,et al.  Characterizing rule-based category learning deficits in patients with Parkinson's disease , 2007, Neuropsychologia.

[57]  R. Gur,et al.  Hemispheric asymmetries in processing emotional expressions , 1983, Neuropsychologia.

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

[59]  J F Thayer,et al.  Sex differences in judgement of facial affect: a multivariate analysis of recognition errors. , 2000, Scandinavian journal of psychology.

[60]  J. Borod,et al.  A Review of the Cognitive and Behavioral Sequelae of Parkinson's Disease: Relationship to Frontostriatal Circuitry , 2003, Cognitive and behavioral neurology : official journal of the Society for Behavioral and Cognitive Neurology.

[61]  K. Heilman,et al.  Emotional facial imagery, perception, and expression in Parkinson's disease , 1995, Neurology.

[62]  Ursula Hess,et al.  Deficits in decoding emotional facial expressions in Parkinson’s disease , 2004, Neuropsychologia.

[63]  C. Darwin The Expression of the Emotions in Man and Animals , .

[64]  R. Gur,et al.  The effects of right and left hemiparkinsonism on prosody , 1989, Brain and Language.

[65]  S. Rauch,et al.  A functional MRI study of human amygdala responses to facial expressions of fear versus anger. , 2001, Emotion.

[66]  Judith A. Hall,et al.  Gender differences in judgments of multiple emotions from facial expressions. , 2004, Emotion.

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

[68]  R. Hilker,et al.  Activation of basal ganglia loops in idiopathic Parkinson’s disease: a PET study , 2003, Journal of Neural Transmission.

[69]  N. Fox,et al.  Asymmetrical brain activity discriminates between positive and negative affective stimuli in human infants. , 1982, Science.

[70]  J. Rinne,et al.  Neuritic degeneration in the hippocampus and amygdala in Parkinson’s disease in relation to Alzheimer pathology , 1999, Acta Neuropathologica.

[71]  T. Benke,et al.  A Study of Emotional Processing in Parkinson's Disease , 1998, Brain and Cognition.

[72]  G. Ganis,et al.  Frontostriatal circuits are necessary for visuomotor transformation: Mental rotation in Parkinson's disease , 2006, Neuropsychologia.

[73]  M. Pell,et al.  Processing emotional tone from speech in Parkinson’s disease: A role for the basal ganglia , 2003, Cognitive, affective & behavioral neuroscience.

[74]  E. Haan,et al.  Processing of Emotional Facial Expressions in Korsakoff's Syndrome , 2006, Cortex.

[75]  M. Iyo,et al.  Alterations in binding site density of dopamine transporter in the striatum, orbitofrontal cortex, and amygdala in early Parkinson's disease: Compartment analysis for β‐CFT binding with positron emission tomography , 1999, Annals of neurology.

[76]  G. E. Alexander,et al.  Basal ganglia-thalamocortical circuits: parallel substrates for motor, oculomotor, "prefrontal" and "limbic" functions. , 1990, Progress in brain research.

[77]  J. Hietanen,et al.  Depression biases the recognition of emotionally neutral faces , 2004, Psychiatry Research.

[78]  E. Mikhailova,et al.  Abnormal recognition of facial expression of emotions in depressed patients with major depression disorder and schizotypal personality disorder , 1996, Biological Psychiatry.

[79]  H. Przuntek,et al.  Facial expression recognition in people with medicated and unmedicated Parkinson’s disease , 2003, Neuropsychologia.

[80]  Bonnie Wong,et al.  Patterns of visual scanning as predictors of emotion identification in normal aging. , 2005, Neuropsychology.

[81]  N. Adams,et al.  Contributions to Neuropsychological Assessment , 1995, Neurology.

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

[83]  P. Schyns,et al.  A mechanism for impaired fear recognition after amygdala damage , 2005, Nature.

[84]  H. Braak,et al.  Staging of brain pathology related to sporadic Parkinson’s disease , 2003, Neurobiology of Aging.

[85]  Bruce P. Rosenthal,et al.  Functional assessment of low vision , 1996 .

[86]  E. Walker,et al.  Facial discrimination and emotional recognition in schizophrenia and affective disorders. , 1986, Archives of general psychiatry.

[87]  W. T. Maddox,et al.  Striatal contributions to category learning: Quantitative modeling of simple linear and complex nonlinear rule learning in patients with Parkinson's disease , 2001, Journal of the International Neuropsychological Society.

[88]  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.

[89]  H. Kraemer,et al.  Facial emotion discrimination: II. Behavioral findings in depression , 1992, Psychiatry Research.

[90]  G. Schwartz,et al.  Differential lateralization for positive versus negative emotion , 1979, Neuropsychologia.