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Facial emotion recognition and its relationship to cognition and depressive symptoms in patients with Parkinson's disease

Published online by Cambridge University Press:  18 March 2016

J. Pietschnig ,
L. Schröder ,
I. Ratheiser ,
I. Kryspin-Exner ,
M. Pflüger ,
D. Moser ,
E. Auff ,
W. Pirker ,
G. Pusswald  and
J. Lehrner
J. Pietschnig
Affiliation:
Department of Applied Psychology: Health, Development, Enhancement and Intervention, Faculty of Psychology, University of Vienna, Vienna, Austria
L. Schröder
Affiliation:
Department of Applied Psychology: Health, Development, Enhancement and Intervention, Faculty of Psychology, University of Vienna, Vienna, Austria
I. Ratheiser
Affiliation:
Department of Applied Psychology: Health, Development, Enhancement and Intervention, Faculty of Psychology, University of Vienna, Vienna, Austria
I. Kryspin-Exner
Affiliation:
Department of Applied Psychology: Health, Development, Enhancement and Intervention, Faculty of Psychology, University of Vienna, Vienna, Austria
M. Pflüger
Affiliation:
Department of Neurology, Medical University of Vienna, Vienna, Austria
D. Moser
Affiliation:
Department of Neurology, Medical University of Vienna, Vienna, Austria
E. Auff
Affiliation:
Department of Neurology, Medical University of Vienna, Vienna, Austria
W. Pirker
Affiliation:
Department of Neurology, Medical University of Vienna, Vienna, Austria Department of Neurology, Wilhelminenspital Wien, Vienna, Austria
G. Pusswald
Affiliation:
Department of Neurology, Medical University of Vienna, Vienna, Austria
J. Lehrner*
Affiliation:
Department of Neurology, Medical University of Vienna, Vienna, Austria
*
Correspondence should be addressed to: Ass. Prof. Priv. Doz. Mag. Dr J. Lehrner, Department of Neurology, Medical University of Vienna, Währinger Gürtel 18–20, A-1097 Wien, Austria. Phone: +0043-1-40400-31090; Fax: +0043-1-40400-31410. Email: [email protected].
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Abstract

Background:

Impairments in facial emotion recognition (FER) have been detected in patients with Parkinson disease (PD). Presently, we aim at assessing differences in emotion recognition performance in PD patient groups with and without mild forms of cognitive impairment (MCI) compared to healthy controls.

Methods:

Performance on a concise emotion recognition test battery (VERT-K) of three groups of 97 PD patients was compared with an age-equivalent sample of 168 healthy controls. Patients were categorized into groups according to two well-established classifications of MCI according to Petersen's (cognitively intact vs. amnestic MCI, aMCI, vs. non-amnestic MCI, non-aMCI) and Litvan's (cognitively intact vs. single-domain MCI, sMCI, vs. multi-domain MCI, mMCI) criteria. Patients and controls underwent individual assessments using a comprehensive neuropsychological test battery examining attention, executive functioning, language, and memory (Neuropsychological Test Battery Vienna, NTBV), the Beck Depression Inventory, and a measure of premorbid IQ (WST).

Results:

Cognitively intact PD patients and patients with MCI in PD (PD-MCI) showed significantly worse emotion recognition performance when compared to healthy controls. Between-groups effect sizes were substantial, showing non-trivial effects in all comparisons (Cohen's ds from 0.31 to 1.22). Moreover, emotion recognition performance was higher in women, positively associated with premorbid IQ and negatively associated with age. Depressive symptoms were not related to FER.

Conclusions:

The present investigation yields further evidence for impaired FER in PD. Interestingly, our data suggest FER deficits even in cognitively intact PD patients indicating FER dysfunction prior to the development of overt cognitive dysfunction. Age showed a negative association whereas IQ showed a positive association with FER.

Keywords

facial emotion recognitionmild cognitive impairmentParkinson's disease
Type
Research Article
Information
International Psychogeriatrics , Volume 28 , Issue 7 , July 2016 , pp. 1165 - 1179
Copyright
Copyright © International Psychogeriatric Association 2016 

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References

Adolphs, R. (2010). What does the amygdala contribute to social cognition? Annals of the New York Academy of Sciences, 1191, 42–61.Google Scholar
Adolphs, R., Schul, R. and Tranel, D. (1998). Intact recognition of facial emotion in Parkinson's disease. Neuropsychology, 12, 253–258.CrossRefGoogle ScholarPubMed
Anderson, I. M. et al. (2011). State-dependent alteration in face emotion recognition in depression. British Journal of Psychiatry, 198, 302–308.Google Scholar
Assogna, F., Pontieri, F. E., Caltagirone, C. and Spalletta, G. (2008). The recognition of facial emotion expressions in Parkinson's disease. European Neuropsychopharmacology, 18, 835–848.Google Scholar
Assogna, F. et al. (2010). Intensity-dependent facial emotion recognition and cognitive functions in Parkinson's disease. Journal of the International Neuropsychological Society, 16, 867–876.Google Scholar
Baggio, H. C. et al. (2012). Structural correlates of facial emotion recognition deficits in Parkinson's disease patients. Neuropsychologia, 50, 2121–2128.CrossRefGoogle ScholarPubMed
Barulli, D. and Stern, Y. (2013). Efficiency, capacity, compensation, maintenance, plasticity: emerging concepts in cognitive reserve. Trends in Cognitive Sciences, 17, 502–509.CrossRefGoogle ScholarPubMed
Braak, H. and Del Tredici, K. (2009). Neuroanatomy and pathology of sporadic Parkinson's disease. Advances in Anatomy, Embryology, and Cell Biology, 201, 1–119.Google Scholar
Clark, U. S, Neargarder, S. and Cronin-Golomb, A. (2010). Visual exploration of emotional facial expressions in Parkinson's disease. Neuropsychologia, 48, 1901–1913.CrossRefGoogle ScholarPubMed
Cohen, J. (1988). Statistical Power Analysis for the Behavioral Sciences, 2nd edn. Hillsdale, NJ: Lawrence Earlbaum Associates.Google Scholar
Derntl, B., Kryspin-Exner, I., Fernbach, E., Moser, E. and Habel, U. (2008). Emotion recognition accuracy in 530 healthy young females is associated with cycle phase. Hormones and Behavior, 53, 90–95.Google Scholar
Dilling, H., Mombour, W. and Schmidt, M. H. (eds.) (2000). Internationale Klassifikation psychischer Störungen: ICD-10 Kapitel V (F). Klinisch-diagnostische Leitlinien [International Classification of psychological disorders: ICD-10 chapter V (F). Clinical and diagnostic guidelines]. Bern: Huber.Google Scholar
Dissanayaka, N. N. N. W., White, E., O'Sullivan, J. D., Marsh, R., Pachana, N. A. and Byrne, G. J. (2014). The clinical spectrum of anxiety in Parkinson's disease. Movement Disorders, 29, 967–975.Google Scholar
Dujardin, K. et al. (2004). Deficits in decoding emotional facial expressions in Parkinson's disease. Neuropsychologia, 42, 239–250.CrossRefGoogle ScholarPubMed
Elfenbein, H. A. and Ambady, N. (2002). On the universality and cultural specificity of emotion recognition: a meta-analysis. Psychological Bulletin, 128, 203–235.Google Scholar
Fahn, S., Elton, R. L. and Committee MotUd. (1987). Unified Parkinsons's disease rating scale. In Fahn, S., Marsden, C. D., Calne, D. B. and Goldstein, M. (eds.), Recent Developments in Parkinson's Disease (pp. 195–202). New York: McMillan.Google Scholar
Folstein, M., Folstein, S. and McHugh, P. R. (1975). Mini-mental state: a practical method for grading the cognitive state of patients for the clinician. Journal of Psychiatry Research, 12, 189–198.Google Scholar
Forni-Santos, L. and Osorio, F. L. (2015). Influence of gender in the recognition of basic facial expressions: a critical literature review. World Journal of Psychiatry, 5, 342–351.Google Scholar
Gatterer, G. (2008). Alters-Konzentrations-Test (AKT), 2nd restandardized edn. Göttingen, Germany: Hogrefe.Google Scholar
Gibb, W. R. G. and Lees, A. J. (1988). The relevance of the lewy body to the pathogenesis of idiopathic Parkinson's disease. Journal of Neurology Neurosurgery and Psychiatry, 51, 745–752.Google Scholar
Goodglass, H. and Kaplan, E. (1983). The Assessment of Aphasia and Related Disorders, 2nd edn. Philadelphia: Lea & Fabinger.Google Scholar
Gray, H. A. and Tickle-Degnen, L. (2010). A meta-analysis of performance on emotion recognition tasks in Parkinson's disease. Neuropsychology, 24, 176–191.Google Scholar
Hautzinger, M., Keller, F. and Kühner, C. (2006). Beck Depressions-Inventar (BDI-II), revised edn. Frankfurt, Germany: Harcourt.Google Scholar
Herrera, E., Cuetos, F. and Rodriguez-Ferreiro, J. (2011). Emotion recognition impairment in Parkinson's disease patients without dementia. Journal of the Neurological Sciences, 15, 237–240.Google Scholar
Hipp, G., Diederich, N. J., Pieria, V. and Vaillant, M. (2014). Primary vision and facial emotion recognition in early Parkinson's disease. Journal of the Neurological Sciences, 15, 178–182.CrossRefGoogle Scholar
Hoffmann, H., Kessler, H., Eppel, T., Rukavina, S. and Traue, H. C. (2010). Expression intensity, gender and facial emotion recognition: women recognize only subtle facial emotions better than men. Acta Psychologica, 135, 278–283.Google Scholar
Ibarretxe-Bilbao, N. et al. (2009). Neuroanatomical correlates of impaired decision-making and facial emotion recognition in early Parkinson's disease. European Journal of Neuroscience, 30, 1162–1171.CrossRefGoogle ScholarPubMed
Kehagia, A. A., Barker, R. A. and Robbins, T. W. (2010). Neuropsychological and clinical heterogeneity of cognitive impairment and dementia in patients with Parkinson's disease. Lancet Neurology, 9, 1200–1213.Google Scholar
Lawrence, A. D., Goerendt, I. K. and 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.Google Scholar
Lehrl, S. and Fischer, B. (1997). Kurztest für cerebale Insuffizienz (c.I.-Test) [A short test for cerebral insufficiency (c.I. Test)]. Ebersberg, Germany: Vless.Google Scholar
Lehrner, J., Gleiß, A., Maly, J., Auff, E. and Dal-Bianco, P. (2006). Der verbale selektive reminding test (VSRT): ein verfahren zur Überprüfung verbaler Gedächtnisfunktionen [The verbal selective reminding test (VSRT): a measure for the assessment of verbal memory functions]. Neuropsychiatrie, 20, 204–214.Google Scholar
Lehrner, J. et al. (2014a). Subjective memory complaints, depressive symptoms and cognition in Parkinson's disease patients. European Journal of Neurology, 21, 1276–1284.Google Scholar
Lehrner, J. et al. (2014b). Prevalence of mild cognitive impairment subtypes in patients with Parkinson's disease: comparison of two modes of classification. Zeitschrift für Neuropsychologie, 25, 49–63.CrossRefGoogle Scholar
Litvan, I. et al. (2011). MDS task force on mild cognitive impairment in Parkinson's disease: critical review of PD-MCI. Movement Disorders, 26, 1814–1824.CrossRefGoogle ScholarPubMed
Litvan, I. et al. (2012). Diagnostic criteria for mild cognitive impairment in Parkison's disease: movement disorder society task force guidelines. Movement Disorders, 27, 349–356.CrossRefGoogle Scholar
Morris, J. C. et al. (1989). The consortium to establish a registry for Alzheimer‘s disease (CERAD). Part I. Clinical and neuropsychological assessment of Alzheimer‘s disease. Neurology, 39, 1159–1165.Google Scholar
Ngo, N. and Isaacowitz, D. M. (2015). Use of context in emotion perception: the role of top-down control, cue type, and perceiver's age. Emotion, 15, 292–302.Google Scholar
Oswald, W. D. and Fleischmann, U. M. (1997). Das Nünberger-Alters-Inventar [Nürnberger Geriatric Inventory]. Göttingen, Germany: Hogrefe.Google Scholar
Pagonabarraga, J., Kulisevsky, J., Strafella, A. P. and Krack, P. (2015). Apathy in Parkinson's disease: clinical features, neural substrates, diagnosis, and treatment. Lancet Neurology, 14, 518–531.CrossRefGoogle ScholarPubMed
Pell, M. D. and Leonard, C. L. (2005). Facial expression decoding in early Parkinson's disease. Cognitive Brain Research, 23, 327–340.Google Scholar
Peron, J., Dondaine, T., Le Jeune, F., Grandjean, D. and Verin, M. (2012). Emotional processing in Parkinson's disease: a systematic review. Movement Disorders, 27, 186–199.Google Scholar
Petersen, R. C. (2004). Mild cognitive impairment as a diagnostic entity. Journal of Internal Medicine, 256, 183–194.Google Scholar
Pietschnig, J. et al. (2016). Facial emotion recognition in patients with subjective cognitive decline and mild cognitive impairment. International Psychogeriatrics, 28, 477–485.Google Scholar
Pusswald, G. et al. (2013). Prevalence of mild cognitive impairment subtypes in patients attending a memory outpatient clinic – comparison of two modes of MCI classification: results of the vienna conversion to dementia study (VCD-study). Alzheimer's and Dementia, 9, 366–376.Google Scholar
R Core Team (2015). R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing.Google Scholar
Regard, M., Strauss, E. and Knapp, P. (1982). Children‘s production on verbal and non-verbal fluency tasks. Perceptual and Motor Skills, 55, 839–844.CrossRefGoogle ScholarPubMed
Reitan, R. (1979). Trail Making Test (TMT). Tucson, AZ: Reitan Neuropsychology Laboratory.Google Scholar
Ruffman, T., Henry, J. D., Livingstone, V. and Phillips, L. H. (2008). A meta-analytic review of emotion recognition and aging: implications for neuropsychological models of aging. Neuroscience and Biobehavioral Reviews, 32, 863–881.Google Scholar
Saß, H., Wittchen, H.-U., Zaudig, M. and Houben, I. (2003). Diagnostisches und Statistisches Manual Psychischer Störungen - Textrevision - DSM-IV-TR [Diagnostic and Statistical Manual of Psychological Disorders – Text Revision – DSM-IV-TR]. Göttingen, Germany: Hogrefe.Google Scholar
Schmidt, K.-H. and Metzler, P. (1992). Wortschatztest (WST): Ein Rasch-skalierter Test zur Abschätzung der verbalen Intelligenz [Vocabulary test (WST): A Rasch-Calibrated Test for Assessment of Verbal Intelligence]. Weinheim, Germany: Beltz.Google Scholar
Sprengelmeyer, R. et al. (2003). Facial expression recognition in people with medicated and unmedicated Parkinson's disease. Neuropsychologia, 41, 1047–1057.Google Scholar
Sullivan, S. and Ruffman, T. (2004). Emotion recognition deficits in the elderly. International Journal of Neuroscience, 114, 403–432.Google Scholar
Tewes, U. (1994). Hamburg-Wechsler-Intelligenztest für Erwachsene-Revision 1991 (HAWIE-R) [The Wechsler Adult Intelligence Scale-Revised 1991 (HAWIE-R)]. Bern, Switzerland: Huber.Google Scholar
van Mierlo, T. J., Chung, C., Foncke, E. M., Berendse, H. W. and van den Heuvel, O. A. (2015). Depressive symptoms in Parkinson's disease are related to decreased hippocampus and amygdala volume. Movement Disorders, 30, 245–252.Google Scholar
Vandekerckhove, M. et al. (2014). Impaired facial emotion recognition in patients with ventromedial prefrontal hypoperfusion. Neuropsychology, 28, 605–612.Google Scholar
Vriend, C., Boedhoe, P. S., Rutten, S., Berendse, H. W., van der Werf, Y. D. and van den Heuvel, O. A. (2016). A smaller amygdala is associated with anxiety in Parkinson's disease: a combined FreeSurfer-VBM study. Journal of Neurology, Neurosurgery & Psychiatry, in press.Google Scholar
Vriend, C. et al. (2014). Depression and impulse control disorders in Parkinson's disease: two sides of the same coin? Neuroscience and Biobehavioral Reviews, 38, 60–71.Google Scholar
Yip, J. T. H., Lee, T. M. C., Ho, S. L., Tsang, K. L. and Li, L. S. W. (2003). Emotion recognition in patients with idiopathic Parkinson's disease. Movement Disorders, 18, 1115–1122.Google Scholar