Emotional processing in Parkinson's disease: A systematic review

Parkinson's disease provides a useful model for studying the neural substrates of emotional processing. The striato‐thalamo‐cortical circuits, like the mesolimbic dopamine system that modulates their function, are thought to be involved in emotional processing. As Parkinson's disease is histopathologically characterized by the selective, progressive, and chronic degeneration of the nigrostriatal and mesocorticolimbic dopamine systems, it can therefore serve as a model for assessing the functional role of these circuits in humans. In the present review, we begin by providing a synopsis of the emotional disturbances observed in Parkinson's disease. We then discuss the functional roles of the striato‐thalamo‐cortical and mesolimbic circuits, ending with the conclusion that both these pathways are indeed involved in emotional processing. © 2012 Movement Disorder Society

[1]  H. Ellgring,et al.  Emotional reactions to odours in Parkinson's disease A clinical application of ethological methods , 1992, Journal of Ethology.

[2]  G. Halliday,et al.  Clinical correlates of selective pathology in the amygdala of patients with Parkinson's disease. , 2002, Brain : a journal of neurology.

[3]  E. Bullmore,et al.  Differential activation of the amygdala and the ‘social brain’ during fearful face-processing in Asperger Syndrome , 2007, Neuropsychologia.

[4]  A. Nieoullon Dopamine and the regulation of cognition and attention , 2002, Progress in Neurobiology.

[5]  A. Ellis,et al.  Facial expressions and Parkinson's disease. , 1995, Behavioural neurology.

[6]  T. Pitcairn,et al.  The effects of reduced expression in Parkinson's disease on impression formation by health professionals , 1987 .

[7]  R. Barker,et al.  Movement Disorders , 1994, Stereotactic and Functional Neurosurgery.

[8]  S. Folstein,et al.  Comprehension of prosody in Huntington's disease. , 1990, Journal of neurology, neurosurgery, and psychiatry.

[9]  Simon Baron-Cohen,et al.  Finding a face in the crowd: Testing the anger superiority effect in Asperger Syndrome , 2006, Brain and Cognition.

[10]  Lisa J Rapport,et al.  Experienced emotion and affect recognition in adult attention-deficit hyperactivity disorder. , 2002, Neuropsychology.

[11]  Gilles Pourtois,et al.  Emotion and attention interactions in social cognition: Brain regions involved in processing anger prosody , 2005, NeuroImage.

[12]  D. Bowers,et al.  Startle reflex hyporeactivity in Parkinson's disease: An emotion-specific or arousal-modulated deficit? , 2009, Neuropsychologia.

[13]  J. Hanley,et al.  Perception and memory for faces in Parkinson's disease , 1991, Neuropsychologia.

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

[15]  S. Kotz,et al.  Functional contributions of the basal ganglia to emotional prosody: Evidence from ERPs , 2008, Brain Research.

[16]  C. Caltagirone,et al.  Neuropsychological correlates of alexithymia in Parkinson's disease , 2007, Journal of the International Neuropsychological Society.

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

[18]  Marianne Patt,et al.  Reduced Ventrolateral fMRI Response during Observation of Emotional Gestures Related to the Degree of Dopaminergic Impairment in Parkinson Disease , 2009, Journal of Cognitive Neuroscience.

[19]  C. Ludlow,et al.  Manual of Nerve Conduction Velocity and Clinical Neurophysiology, 3rd Ed. , 1994, Neurology.

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

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

[22]  M. Katsikitis,et al.  A study of facial expression in Parkinson's disease using a novel microcomputer-based method. , 1988, Journal of neurology, neurosurgery, and psychiatry.

[23]  J. Borod,et al.  Parameters of emotional processing in neuropsychiatric disorders: conceptual issues and a battery of tests. , 1990, Journal of communication disorders.

[24]  M. Van der Linden,et al.  The interpretation of dysprosody in patients with Parkinson's disease. , 1991, Journal of neurology, neurosurgery, and psychiatry.

[25]  J. Borod,et al.  Social functioning and facial emotional expression in neurological and psychiatric disorders. , 1998, Applied neuropsychology.

[26]  A. Friederici,et al.  On the lateralization of emotional prosody: An event-related functional MR investigation , 2003, Brain and Language.

[27]  S. Scott,et al.  Saying it with feeling: neural responses to emotional vocalizations , 1999, Neuropsychologia.

[28]  K. Heilman,et al.  Abnormal Emotional Word Ratings in Parkinson's Disease , 2007, Neurocase.

[29]  K. Scherer,et al.  The voices of wrath: brain responses to angry prosody in meaningless speech , 2005, Nature Neuroscience.

[30]  A. Cronin-Golomb,et al.  Specific impairments in the recognition of emotional facial expressions in Parkinson's disease , 2008, Neuropsychologia.

[31]  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.

[32]  H. Haeske-Dewick Are perception and memory for faces influenced by a specific age at onset factor in Parkinson's disease? , 1996, Neuropsychologia.

[33]  I. Daum,et al.  Impaired Perception of Vocal Emotions in Parkinson's Disease: Influence of Speech Time Processing and Executive Functioning , 2001, Brain and Cognition.

[34]  D. Skuse,et al.  Impaired sadness recognition is linked to social interaction deficit in autism , 2007, Neuropsychologia.

[35]  A. Lawrence,et al.  Selective disruption of the recognition of facial expressions of anger , 2002, Neuroreport.

[36]  R G Robinson,et al.  Neuropsychological and neuroradiologic correlates of emotional prosody comprehension , 1994, Neurology.

[37]  A. W. Young,et al.  Disgust in pre-clinical Huntington's disease: A longitudinal study , 2006, Neuropsychologia.

[38]  Marc D. Pell,et al.  The impact of Parkinson’s disease on vocal-prosodic communication from the perspective of listeners , 2006, Brain and Language.

[39]  F. Strack,et al.  Inhibiting and facilitating conditions of the human smile: a nonobtrusive test of the facial feedback hypothesis. , 1988, Journal of personality and social psychology.

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

[41]  D. Bowers,et al.  Faces of emotion in Parkinsons disease: Micro-expressivity and bradykinesia during voluntary facial expressions , 2006, Journal of the International Neuropsychological Society.

[42]  R. A. Weddell Effects of Subcortical Lesion Site on Human Emotional Behavior , 1994, Brain and Cognition.

[43]  W. Rinn,et al.  The neuropsychology of facial expression: a review of the neurological and psychological mechanisms for producing facial expressions. , 1984, Psychological bulletin.

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

[45]  J. Cummings,et al.  Frontal-subcortical circuits and human behavior. , 1993, Journal of psychosomatic research.

[46]  Marc D. Pell,et al.  Vocal emotion processing in Parkinson's disease: Reduced sensitivity to negative emotions , 2008, Brain Research.

[47]  Andrew Kertesz,et al.  Lesion localization in acquired deficits of emotional expression and comprehension , 1990, Brain and Cognition.

[48]  R. Bagby,et al.  The alexithymia construct. A potential paradigm for psychosomatic medicine. , 1991, Psychosomatics.

[49]  M. Katsikitis,et al.  A Controlled Quantitative Study of Facial Expression in Parkinson's Disease and Depression , 1991, The Journal of nervous and mental disease.

[50]  David Sander,et al.  A systems approach to appraisal mechanisms in emotion , 2005, Neural Networks.

[51]  M. Chaves,et al.  Did depressive symptoms affect recognition of emotional prosody in Parkinson’s disease? , 2008, Neuropsychiatric disease and treatment.

[52]  H. Ellgring,et al.  Disturbance of spontaneous and posed facial expressions in Parkinson's disease , 2003 .

[53]  Michael Okun,et al.  Startling facts about emotion in Parkinson's disease: blunted reactivity to aversive stimuli. , 2006, Brain : a journal of neurology.

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

[55]  E. Kosno-Kruszewska,et al.  Degenerative axonal changes in the hippocampus and amygdala in Parkinson's disease. , 2003, Folia neuropathologica.

[56]  Patrik Vuilleumier,et al.  Effects of emotional prosody on auditory extinction for voices in patients with spatial neglect , 2008, Neuropsychologia.

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

[58]  M. Guha The Oxford Companion to Emotion and the Affective Sciences , 2010 .

[59]  K. Scherer,et al.  Conscious emotional experience emerges as a function of multilevel, appraisal-driven response synchronization , 2008, Consciousness and Cognition.

[60]  K. Scherer,et al.  Appraisal processes in emotion: Theory, methods, research. , 2001 .

[61]  Didier Grandjean,et al.  Unpacking the cognitive architecture of emotion processes. , 2008, Emotion.

[62]  Hermann Ackermann,et al.  Emotional processing following cortical and subcortical brain damage: contribution of the fronto-striatal circuitry. , 1998, Behavioural neurology.

[63]  O. Blin,et al.  Dopaminergic Contribution to the Regulation of Emotional Perception , 2005, Clinical neuropharmacology.

[64]  Nirbhay N. Singh,et al.  Recognition of Facial Expressions of Emotion by Children with Attention-Deficit Hyperactivity Disorder , 1998, Behavior modification.

[65]  Yoshiro Okubo,et al.  Effects of dopaminergic and serotonergic manipulation on emotional processing: A pharmacological fMRI study , 2005, NeuroImage.

[66]  O. Blin,et al.  Amygdala Activation Modulated by Levodopa During Emotional Recognition Processing in Healthy Volunteers: A Double-Blind, Placebo-Controlled Study , 2007, Journal of clinical psychopharmacology.

[67]  G. Alpers,et al.  Emotion processing in Parkinson's disease: Dissociation between early neuronal processing and explicit ratings , 2006, Clinical Neurophysiology.

[68]  Joep Sonnemans,et al.  The duration of affective phenomena or emotions, sentiments and passions , 1991 .

[69]  Reinhard Dengler,et al.  Perception of emotional speech in Parkinson's Disease , 2006, Movement disorders : official journal of the Movement Disorder Society.

[70]  Livia Colle,et al.  Impaired recognition of negative basic emotions in autism: A test of the amygdala theory , 2006, Social neuroscience.

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

[72]  M. Terwogt,et al.  Attention to facial emotion expressions in children with autism , 2006, Autism : the international journal of research and practice.

[73]  Takahiro Hoshino,et al.  Disgust-specific impairment of facial expression recognition in Parkinson's disease. , 2006, Brain : a journal of neurology.

[74]  I. Homma,et al.  The amygdala of patients with Parkinson’s disease is silent in response to fearful facial expressions , 2005, Neuroscience.

[75]  P. Ekman An argument for basic emotions , 1992 .

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

[77]  S. Baron-Cohen,et al.  Attention bias to faces in Asperger Syndrome: a pictorial emotion Stroop study , 2006, Psychological Medicine.

[78]  J. Cummings Frontal-subcortical circuits and human behavior. , 1998, Archives of neurology.

[79]  P. A. Beatty,et al.  Affective judgments by patients with Parkinson’s disease or chronic progressive multiple sclerosis , 1989 .

[80]  M. Pell On the Receptive Prosodic Loss in Parkinson's Disease , 1996, Cortex.

[81]  C. Rieffe,et al.  Awareness of Single and Multiple Emotions in High-functioning Children with Autism , 2007, Journal of autism and developmental disorders.

[82]  P. Ekman,et al.  Approaches To Emotion , 1985 .

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

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

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

[86]  K. Strongman International review of studies on emotion , 1991 .

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

[88]  Werner Strik,et al.  The effect of appraisal level on processing of emotional prosody in meaningless speech , 2008, NeuroImage.

[89]  E. Bullmore,et al.  The amygdala theory of autism , 2000, Neuroscience & Biobehavioral Reviews.

[90]  H. Ellgring,et al.  Spontaneous and posed facial expression in Parkinson's Disease , 1996, Journal of the International Neuropsychological Society.

[91]  G. Simons,et al.  Emotional and nonemotional facial expressions in people with Parkinson's disease , 2004, Journal of the International Neuropsychological Society.

[92]  Reinhard Dengler,et al.  Emotional speech in Parkinson's disease , 2008, Movement disorders : official journal of the Movement Disorder Society.

[93]  Francesca Benuzzi,et al.  Recognition of emotions from visual and prosodic cues in Parkinson’s disease , 2008, Neurological Sciences.

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

[95]  R. Mitchell,et al.  Decoding emotional prosody in Parkinson's disease and its potential neuropsychological basis , 2009, Journal of clinical and experimental neuropsychology.

[96]  Tatia M.C. Lee,et al.  The differential effects of thalamus and basal ganglia on facial emotion recognition , 2006, Brain and Cognition.

[97]  F. Caird,et al.  Evidence for an apparent sensory speech disorder in Parkinson's disease. , 1984, Journal of neurology, neurosurgery, and psychiatry.

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

[99]  Jane S. Paulsen,et al.  Beyond disgust: impaired recognition of negative emotions prior to diagnosis in Huntington's disease. , 2007, Brain : a journal of neurology.

[100]  P. Pattison,et al.  Emotion recognition via facial expression and affective prosody in schizophrenia: a methodological review. , 2002, Clinical psychology review.

[101]  A. Bruce Emotional Expression , 1883, The American Naturalist.

[102]  D. Grandjean,et al.  Major depressive disorder skews the recognition of emotional prosody , 2011, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

[103]  A. Lloyd,et al.  Comprehension of Prosody in Parkinson's Disease , 1999, Cortex.

[104]  K. Scherer Neuroscience projections to current debates in emotion psychology , 1993 .

[105]  M. Mimura,et al.  Recognition of emotion from moving facial and prosodic stimuli in depressed patients , 2004, Journal of Neurology, Neurosurgery & Psychiatry.

[106]  Tatia M. C. Lee,et al.  Emotion recognition in patients with idiopathic Parkinson's disease , 2003, Movement disorders : official journal of the Movement Disorder Society.

[107]  Didier Grandjean,et al.  Specific brain networks during explicit and implicit decoding of emotional prosody. , 2012, Cerebral cortex.

[108]  Klaus R. Scherer,et al.  Oxford Companion to Emotion and the Affective Sciences , 2009 .

[109]  B Pentland,et al.  Non-verbal cues in the self-presentation of parkinsonian patients. , 1990, The British journal of clinical psychology.

[110]  O. Blin,et al.  Effect of Levodopa on Healthy Volunteers' Facial Emotion Perception: An fMRI Study , 2005, Clinical neuropharmacology.

[111]  R. Buck,et al.  Nonverbal Communication of Affect in Brain-Damaged Patients , 1980, Cortex.

[112]  Francesco Fera,et al.  Dextroamphetamine Modulates the Response of the Human Amygdala , 2002, Neuropsychopharmacology.

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

[114]  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.