Intensity-dependent facial emotion recognition and cognitive functions in Parkinson’s disease | Journal of the International Neuropsychological Society | Cambridge Core (original) (raw)

Abstract

Patients with Parkinson’s disease (PD) frequently display non-motor symptoms. In this study, we investigated intensity-dependent facial emotion recognition in patients with PD and healthy controls (HC), matched for age, gender, and education, and its relationship to individual cognitive domains. Seventy patients with PD and 70 HC were submitted to a clinical, neuropsychological, and psychopathological evaluation. Facial emotion recognition performance was assessed using the Penn Emotion Recognition Test (PERT). The patients with PD recognized fewer low- and high-intensity facial expressions of disgust than HC. This effect was selective, because their global ability to recognize emotions was intact. Both patients with PD and HC recognized high-intensity better than low-intensity emotions, except for disgust, which was recognized better at low intensity. In the patients with PD, overall facial emotion recognition and selective disgust recognition performances were related to deficits in many neuropsychological domains (verbal and visuo-spatial memory, attention, praxis, and verbal fluency). The ability to recognize emotions is a complex cognitive process requiring the integrity of several functions. Therefore, it is likely that structural or functional derangement of the discrete neural pathways involved in these cognitive functions in patients with PD makes it difficult for them to recognize emotions expressed by others. (JINS, 2010, 16, 867–876.)

References

Ackermann, H., & Ziegler, W. (1996). Articulatory deficits in Parkinsonian dysarthria: An acoustic analysis. Journal of Neurology, Neurosurgery, and Psychiatry, 54, 1093–1098.CrossRefGoogle Scholar

Adolphs, R. (2006). How do we know the minds of others? Domain-specificity, simulation, and enactive social cognition. Brain Research, 1079, 25–35.CrossRefGoogle ScholarPubMed

Adolphs, R., Schul, R., & Tranel, D. (1998). Intact recognition of facial emotion in Parkinson’s disease. Neuropsychology, 12, 253–258.CrossRefGoogle ScholarPubMed

Albert, M.S., Cohen, C., & Koff, E. (1991). Perception of affect in patients with dementia of Alzheimer type. Archives of Neurology, 48, 791–795.CrossRefGoogle Scholar

Alexander, G., Delong, M., & Strick, P. (1986). Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annual Review of Neuroscience, 9, 357–381.CrossRefGoogle ScholarPubMed

American Psychiatric Association. (2000). Diagnostic and statistical manual of mental disorders (4th ed.). Washington, DC: American Psychiatric Press.Google Scholar

Andersen, A., & Phelps, E. (2000). Expression without recognition: Contributions of the human amygdala to emotional communication. Psychological Science, 11, 106–111.CrossRefGoogle Scholar

Ariatti, A., Benuzzi, F., & Nichelli, P. (2008). Recognition of emotions from visual and prosodic cues in Parkinson’s disease. Neurological Sciences, 29, 219–227.CrossRefGoogle ScholarPubMed

Assogna, F., Pontieri, F.E., Caltagirone, C., & Spalletta, G. (2008). The recognition of facial emotion expressions in Parkinson’s disease. European Neuropsychopharmacology, 18, 835–848.CrossRefGoogle ScholarPubMed

Beck, A.T., & Steer, R.A. (1987). Beck depression inventory manual. San Antonio, TX: The Psychological Corporation.Google Scholar

Blonder, L.X., Gur, R.E., & Gur, R.C. (1989). The effects of right and left hemiparkinsonism on prosody. Brain and Language, 36, 193–207.CrossRefGoogle ScholarPubMed

Borod, J.C., Welkowitz, J., Alpert, M., Brozgold, A.Z., Martin, C., Peselow, E., et al. . (1990). Parameters of emotional processing in neuropsychiatric disorders: Conceptual issues and a battery of tests. Journal of Communication Disorders, 23, 247–271.CrossRefGoogle Scholar

Braak, H., Del Tredici, K., Rub, U., de Vos, R.A., Jansen Steur, E.N., & Braak, E. (2003). Staging of brain pathology related to sporadic Parkinson’s disease. Neurobiology of Aging, 24, 197–211.CrossRefGoogle ScholarPubMed

Braak, H., Ghebremedhin, E., Rub, U., Bratzke, H., & Del Tredici, K. (2004). Stages in the development of Parkinson’s disease-related pathology. Cell and Tissue Research, 318, 121–134.CrossRefGoogle ScholarPubMed

Brown, R.G., & Marsden, C.D. (1990). Cognitive function in Parkinson’s disease: From description to theory. Trends in Neurosciences, 13, 21–29.CrossRefGoogle ScholarPubMed

Carlesimo, G.A., Caltagirone, C., & Gainotti, G. (1996). The Mental Deterioration Battery: Normative data, diagnostic reliability and qualitative analyses of cognitive impairment. The Group for the Standardization of the Mental Deterioration Battery. European Neurology, 36, 378–384.CrossRefGoogle Scholar

Clark, U.S., Neargarder, S., & Cronin-Golomb, A. (2008). Specific impairment in the recognition of emotional facial expressions in Parkinson’s disease. Neuropsychologia, 46, 2300–2309.CrossRefGoogle ScholarPubMed

Cooper, J.A., Sagar, H.J., Tidswell, P., & Jordan, N. (1994). Slowed central processing in simple and go/no-go reaction time tasks in Parkinson’s disease. Brain, 117, 517–529.CrossRefGoogle ScholarPubMed

Dujardin, K., Blairy, S., Defebvre, L., Duhem, S., Noel, Y., Hess, U., et al. . (2004). Deficits in decoding emotional facial expressions in Parkinson’s disease. Neuropsychologia, 42, 239–250.CrossRefGoogle ScholarPubMed

First, M., Spitzer, R., Gibbon, M., & Williams, J.B.W. (1997). Structured clinical interview for DSM-IV axis I disorders, research version, non-patient edition (SCID-I/NP). New York: Biometrics Research, New York State Psychiatric Institute.Google Scholar

First, M.B., Spitzer, R.L., Gibbon, M., & Williams, J.B.W. (2002). Structured clinical interview for DSM-IV-TR axis I disorders, research version, patient edition (SCID-I/P). New York: Biometrics Research, New York State Psychiatric Institute.Google Scholar

Folstein, M.F., Folstein, S.E., & McHugh, P.R. (1975). “Mini-mental state”. A practical method for grading the cognitive state of patients for the clinician. Journal of Psychiatric Research, 12, 189–198.CrossRefGoogle ScholarPubMed

Greve, K.W. (2001). The WCST-64: A standardized short-form of Wisconsin Card Sorting Test. The Clinical Neuropsychologist, 15, 228–234.CrossRefGoogle ScholarPubMed

Gur, R.C., Sara, R., Hagendoorn, M., Marom, O., Hughett, P., Macy, L., et al. . (2002). A method for obtaining 3-dimensional facial expressions and its standardization for use in neurocognitive studies. Journal of Neuroscience Methods, 115, 137–143.CrossRefGoogle ScholarPubMed

Hughes, A.J., Daniel, S.E., & Lees, A.J. (2001). Improved accuracy of clinical diagnosis of Lewy body Parkinson’s disease. Neurology, 57, 1497–1499.CrossRefGoogle ScholarPubMed

Ivory, S.J., Knight, R.G., Longmore, B.E., & Caradoc-Davies, T. (1999). Verbal memory in non-demented patients with idiopathic Parkinson’s disease. Neuropsychologia, 37, 817–828.CrossRefGoogle ScholarPubMed

Kan, Y., Kawamura, M., Hasegawa, Y., Mochizuki, S., & Nakamura, K. (2002). Recognition of emotion from facial, prosodic and written verbal stimuli in Parkinson’s disease. Cortex, 38, 623–630.CrossRefGoogle ScholarPubMed

Kawamura, M., & Kobayakawa, M. (2009). Emotional impairment in Parkinson’s disease. Parkinsonism & Related Disorders, 15(Suppl.), 47–52.CrossRefGoogle ScholarPubMed

Kohler, C., Turner, T.H., Bilker, W.B., Brensinger, C.M., Siegel, S.J., Kanes, S.J., et al. . (2003). Facial emotion recognition in schizophrenia: Intensity effects and error pattern. The American Journal of Psychiatry, 160, 1768–1774.CrossRefGoogle ScholarPubMed

Langston, J.W., Widner, H., Goetz, C.G., Brooks, D., Fahn, S., Freeman, T., et al. . (1992). Core assessment program for intracerebral transplantations (CAPIT). Movement Disorders, 7, 2–13.CrossRefGoogle ScholarPubMed

Lawrence, A.D., Goerendt, I.K., & Brooks, D.J. (2007). Impaired recognition of facial expressions of anger in Parkinson’s disease patients acutely withdrawn from dopamine replacement therapy. Neuropsychologia, 45, 65–74.CrossRefGoogle ScholarPubMed

Mayeux, R., Stern, Y., Sano, M., Cote, L., & Williams, J.B. (1987). Clinical and biochemical correlates of bradyphrenia in Parkinson’s disease. Neurology, 37, 1130–1134.CrossRefGoogle ScholarPubMed

Murphy, F.C., Nimmo-Smith, I., & Lawrence, A.D. (2003). Functional neuroanatomy of emotions: A meta-analysis. Cognitive, Affective & Behavioral Neuroscience, 3, 207–233.CrossRefGoogle ScholarPubMed

Osterrieth, P.A. (1944). Le test de copie d’une figure complexe: Contribution à l’ètude de la perception et de la mèmoire. Archives de Psychologie, 30, 286–350.Google Scholar

Papa, D., & Bersani, G. (2007). Volto, identità ed emozione nella schizofrenia: dalla percezione all’espressione. Giornale Italiano di Psicopatologia, 13, 14–25.Google Scholar

Pell, M.D., & Leonard, C.L. (2005). Facial expression decoding in early Parkinson’s disease. Brain Research. Cognitive Brain Research, 23, 327–340.CrossRefGoogle ScholarPubMed

Pellicano, C., Benincasa, D., Pisani, V., Buttarelli, F.R., Giovannelli, M., & Pontieri, F.E. (2007). Prodromal non-motor symptoms of Parkinson’s disease. Neuropsychiatric Disease and Treatment, 3, 145–152.CrossRefGoogle ScholarPubMed

Phan, K.L., Wager, T., Taylor, S.F., & Liberzon, I. (2002). Functional neuroanatomy of emotions: A meta-analysis of emotion activation studies in PET and fMRI. Neuroimage, 16, 331–348.CrossRefGoogle ScholarPubMed

Remy, P., Doder, M., Lees, A., Turjanski, N., & Brooks, D. (2005). Depression in Parkinson’s disease: Loss of dopamine and noradrenaline innervation in the limbic system. Brain, 128, 1314–1322.CrossRefGoogle ScholarPubMed

Rey, A. (1941). L’examen psychologique dan les cas d’encéphalopathie traumatique (Les problèmes). Archives de Psychologie, 28, 286–340.Google Scholar

Rozin, P., Lowery, L., Imada, S., & Haidt, J. (1999). The CAD triad hypothesis: A mapping between three moral emotions (contempt, anger, disgust) and three moral codes (community, autonomy, divinity). Journal of Personality and Social Psychology, 76, 574–586.CrossRefGoogle ScholarPubMed

Spoletini, I., Marra, C., Di Iulio, F., Gianni, W., Sancesario, G., Giubilei, F., et al. . (2008). Facial emotion recognition deficit in amnestic mild cognitive impairment and Alzheimer disease. The American Journal of Geriatric Psychiatry, 16, 389–398.CrossRefGoogle ScholarPubMed

Sprengelmeyer, R., Young, A.W., Mahn, K., Schroeder, U., Woitalla, D., Büttner, T., et al. . (2003). Facial expression recognition in people with medicated and unmedicated Parkinson’s disease. Neuropsychologia, 41, 1047–1057.CrossRefGoogle ScholarPubMed

Stroop, J. (1935). Studies of interference in serial verbal reactions. Journal of Experimental Psychology, 18, 643–662.CrossRefGoogle Scholar

Suzuki, A., Hoshino, T., Shigemasu, K., & Kawamura, M. (2006). Disgust-specific impairment of facial expression recognition in Parkinson’s disease. Brain, 129, 707–717.CrossRefGoogle ScholarPubMed

Takahashi, H., Yahata, N., Koeda, M., Takano, A., Asai, K., Suhara, T., et al. . (2005). Effects of dopaminergic and serotonergic manipulation on emotional processing: A pharmacological fMRI study. Neuroimage, 27, 991–1001.CrossRefGoogle ScholarPubMed

Teng, E., Lu, P.H., & Cummings, J.L. (2007). Deficits in facial emotion processing in mild cognitive impairment. Dementia and Geriatric Cognitive Disorders, 23, 271–279.CrossRefGoogle ScholarPubMed

Tessitore, A., Hariri, A.R., Fera, F., Smith, W.G., Chase, T.N., Hyde, T.M., et al. . (2002). Dopamine modulates the response of the human amygdala: A study in Parkinson’s disease. The Journal of Neuroscience, 22, 9099–9103.CrossRefGoogle ScholarPubMed

Torack, R., & Morris, J. (1988). The association of ventral tegmental area histopathology with adult dementia. Archives of Neurology, 45, 497–501.CrossRefGoogle ScholarPubMed

Weiss, E.M., Kohler, C.G., Vonbank, J., Stadelmann, E., Kemmler, G., Hinterhuber, H., et al. . (2008). Impairment in emotion recognition abilities in patients with mild cognitive impairment, early and moderate Alzheimer disease compared with healthy comparison subjects. The American Journal of Geriatric Psychiatry, 16, 974–980.CrossRefGoogle ScholarPubMed

Yip, J., Lee, T., Ho, S., Tsang, K., & Li, L. (2003). Emotion recognition in patients with idiopathic Parkinson’s disease. Movement Disorders, 18, 1115–1122.CrossRefGoogle ScholarPubMed

Yoshimura, N., Kawamura, M., Masaoka, Y., & Homma, I. (2005). The amygdala of patients with Parkinson’s disease is silent in response to fearful facial expressions. Neuroscience, 131, 523–534.CrossRefGoogle ScholarPubMed