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Working Memory and Facial Expression Recognition in Patients with Parkinson’s Disease

Published online by Cambridge University Press:  08 April 2014

Laura Alonso-Recio ,
Pilar Martín-Plasencia ,
Ángela Loeches-Alonso  and
Juan M. Serrano-Rodríguez
Laura Alonso-Recio*
Affiliation:
Facultad de Psicología, Universidad a Distancia de Madrid, Collado Villalba, Madrid, Spain
Pilar Martín-Plasencia
Affiliation:
Departamento de Psicología Biológica y de la Salud, Facultad de Psicología, Universidad Autónoma de Madrid, Madrid, Spain
Ángela Loeches-Alonso
Affiliation:
Departamento de Psicología Biológica y de la Salud, Facultad de Psicología, Universidad Autónoma de Madrid, Madrid, Spain
Juan M. Serrano-Rodríguez
Affiliation:
Departamento de Psicología Biológica y de la Salud, Facultad de Psicología, Universidad Autónoma de Madrid, Madrid, Spain
*
Correspondence and reprint requests to: Laura Alonso Recio, Departamento de Psicologia, Universidad a Distancia de Madrid, Camino de la Fonda, 20. 28400 Collado Villalba, Madrid, Spain. E-mail:laura.alonso@udima.es
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Abstract

Facial expression recognition impairment has been reported in Parkinson’s disease. While some authors have referred to specific emotional disabilities, others view them as secondary to executive deficits frequently described in the disease, such as working memory. The present study aims to analyze the relationship between working memory and facial expression recognition abilities in Parkinson’s disease. We observed 50 patients with Parkinson’s disease and 49 healthy controls by means of an n-back procedure with four types of stimuli: emotional facial expressions, gender, spatial locations, and non-sense syllables. Other executive and visuospatial neuropsychological tests were also administered. Results showed that Parkinson’s disease patients with high levels of disability performed worse than healthy individuals on the emotional facial expression and spatial location tasks. Moreover, spatial location task performance was correlated with executive neuropsychological scores, but emotional facial expression was not. Thus, working memory seems to be altered in Parkinson’s disease, particularly in tasks that involve the appreciation of spatial relationships in stimuli. Additionally, non-executive, facial emotional recognition difficulty seems to be present and related to disease progression. (JINS, 2014, 20, 1–10)

Keywords

EmotionExecutive functionVisuospatial abilitiesEmotional impairmentFace recognitionNeurodegenerative disorders
Type
Research Articles
Information
Journal of the International Neuropsychological Society , Volume 20 , Issue 5 , May 2014 , pp. 496 - 505
Copyright
Copyright © The International Neuropsychological Society 2014 

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References

Aarsland, D., Bronnick, K., & Fladby, T. (2011). Mild cognitive impairment in Parkinson’s disease. Current Neurology and Neuroscience Reports, 11(4), 371–378. doi:10.1007/s11910-011-0203-1CrossRefGoogle ScholarPubMed
Adolphs, R. (2002). Neural systems for recognizing emotion. Current Opinion in Neurobiology, 12(2), 169–177. doi:10.1016/S0959-4388(02)00301-XGoogle Scholar
Adolphs, R., Schul, R., & Tranel, D. (1998). Intact recognition of facial emotion in Parkinson’s disease. Neuropsychology, 12(2), 253–258. doi:10.1037/0894.4105.12.2.253Google Scholar
Alonso-Recio, L., Martín, P., Carvajal, F., Ruiz, M., & Serrano, J.M. (2013). A holistic analysis of relationship between executive function and memory in Parkinson’s disease. Journal of Clinical and Experimental Neuropsychology, 35(2), 147–159. doi:10.1080/13803395.2012.758240Google Scholar
Alonso-Recio, L., Serrano-Rodriguez, J.M., Carvajal-Molina, F., Loeches-Alonso, A., & Martin-Plasencia, P. (2012). Reconocimiento de expresiones faciales de emociones en la enfermedad de Parkinson: una revisión teórica. [Recognition of facial expression of emotions in Parkinson’s disease: A theoretical review]. Revista de Neurología, 54(8), 479–489.Google Scholar
Ariatti, A., Benuzzi, F., & Nichelli, P. (2008). Recognition of emotions from visual and prosodic cues in Parkinson’s disease. Neurological Science, 29(4), 219–227.Google Scholar
Assogna, F., Pontieri, F.E., Caltagirone, C., & Spalletta, G. (2008). The recognition of facial emotion expressions in Parkinson’s disease. European Journal of Neuropsychopharmacology, 18(11), 835–848. doi:10.1016/S0010-9452(08)70026-1Google Scholar
Assogna, F., Pontieri, F.E., Cravello, L., Peppe, A., Pierantozzi, M., Stefani, A., … Spalleta, G. (2010). Intensity-dependent facial emotion recognition and cognitive functions in Parkinson’s disease. Journal of the International Neuropsychological Society, 16(5), 867–876. doi:10.1016/j.euroneuro.2008.07.004Google Scholar
Baddeley, A.D. (2003). Working memory: Looking back and looking forward. Nature Reviews Neuroscience, 4, 829–839. doi:10.1038/nin.1201Google Scholar
Baddeley, A.D., & Hitch, G.J. (1974). Working memory. In G.A. Bower (Ed.), Recent advances in learning and motivation (Vol. 8, pp. 47–90). New York: Academic Press.Google Scholar
Beatty, W.W., Goodkin, D.E., Weir, W.S., Staton, R.S., Monson, N., & Beatty, P.A. (1989). Affective judgements by patients with Parkinson’s disease or chronic progressive multiple sclerosis. Bulletin of the Psychonimic Society, 27(4), 361–364.Google Scholar
Benton, A.L., & Hamsher, K. (1978). Multilingual aphasia examination. Iowa City: University of Iowa.Google Scholar
Benton, A.L., Varney, N.R., & Hamsher, K.D. (1978). Visuospatial judgment. A clinical test. Archives of Neurology, 35(6), 364–367.Google Scholar
Borod, J.C., Welkowitz, J., Alpert, M., Brozgold, A.Z., Martin, C., Peselow, E., & Diller, L. (1990). Parameters of emotional processing in neuropsychiatric disorders: Conceptual issues and a battery of tests. Journal of Communication Disorders, 23(4–50), 247–271. doi:10.1016/0021-9924(90)90003-HCrossRefGoogle Scholar
Braak, H., Del Tredici, K., Rüb, U., de Vos, R.A., Steur, J., & Braak, E. (2003). Staging of brain pathology related to sporadic Parkinson’s disease. Neurobiological Aging, 24(2), 197–211. doi:10.1016/S0197-4580(02)00065-9Google Scholar
Braver, T.S., Cohen, J.D., Nystrom, L.E., Jonides, J., Smith, E.E., & Noll, D.C. (1997). A parametric study of prefrontal cortex involvement in human working memory. Neuroimage, 5(1), 49–62. doi:10.1006/nimg.1996.0247Google Scholar
Breitenstein, C., Daum, I., & Ackermann, H. (1998). Emotional processing following cortical and subcortical brain damage: Contribution of the fronto-striatal circuitry. Behavioral Neurology, 11(1), 29–42.CrossRefGoogle ScholarPubMed
Bruce, V., & Young, A. (1986). Understanding face recognition. British Journal of Psychology, 77(Pt 3), 305–327. doi:10.1111/j.2044-8295.1986.tb02199.xCrossRefGoogle ScholarPubMed
Calder, A.J., & Young, A.W. (2005). Understanding the recognition of facial identity and facial expression. Nature Reviews. Neuroscience, 6(8), 641–651. doi:10.1038/nrn1724Google Scholar
Cohen, H., Gagne, M.H., Hess, U., & Pourcher, E. (2010). Emotion and object processing in Parkinson’s disease. Brain and Cognition, 72(3), 457–463. doi:10.1016/j.bandc.2010.01.001Google Scholar
Cools, R., Miyakawa, A., Sheridan, M., & D’Esposito, M. (2010). Enhanced frontal function in Parkinson’s disease. Brain: A Journal of Neurology, 133(Pt 1), 225–233. doi:10.1093/brain/awp301Google Scholar
Costa, A., Peppe, A., Dell’Agnello, G., Carlesimo, G.A., Murri, L., Bonuccelli, U., & Catagirone, C. (2003). Dopaminergic modulation of visual-spatial working memory in Parkinson’s disease. Dementia and Geriatric Cognitive Disorders, 15(2), 55–66. doi:10.1159/000067968Google Scholar
Courtney, S.M. (2004). Attention and cognitive control as emergent properties of information representation in working memory. Cognitive, Affective & Behavioral Neuroscience, 4(4), 501–516. doi:10.3758/CABN.4.4.501Google Scholar
Crucian, G.P., Barrett, A.M., Burks, D.W., Riestra, A.R., Roth, H.L., Schwartz, R.L., … Heilman, K.M. (2003). Mental object rotation in Parkinson’s disease. Journal of the International Neuropsychological Society, 9(7), 1078–1087. doi:10.107/S1355617703970111Google Scholar
Crucian, G.P., & Okun, M.S. (2003). Visual-spatial ability in Parkinson’s disease. Frontiers in Bioscience, 8, 992–997.Google Scholar
Dakin, S.C., & Watt, R.J. (2009). Biological “bar codes” in human faces. Journal of Vision, 9(4.2), 1–10. doi:10.1167/9.4.2Google Scholar
Dara, C., Monetta, L., & Pell, M.D. (2008). Vocal emotion processing in Parkinson’s disease: Reduced sensitivity to negative emotions. Brain Research, 1188, 100–111. doi:10.1016/j.brainres.2007.10.034Google Scholar
Del Ser, T., Gonzalez-Montalvo, J.I., Martinez-Espinosa, S., Delgado-Villapalos, C., & Bermejo, F. (1997). Estimation of premorbid intelligence in Spanish people with the word accentuation test and its application to the diagnosis of dementia. Brain and Cognition, 33(3), 343–356. doi:10.1006/brcg.1997.0877Google Scholar
Dujardin, K., Blairy, S., Defebvre, L., Duhem, S., Noel, Y., Hess, U., & Destée, A. (2004). Deficits in decoding emotional facial expressions in Parkinson’s disease. Neuropsychologia, 42(2), 239–250. doi:10.1016/S0028-3932(03)00154-4CrossRefGoogle ScholarPubMed
Ebner, N.C., Riediger, M., & Linderberger, U. (2010). FACES--A database of facial expressions in young, middle, and older women and men: Development and validation. Behavior Research Methods, 42(1), 351–362. doi:10.3758/BRM.42.1.351Google 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. J Psychiatric Research, 12(3), 189–198.Google Scholar
García-Rodríguez, B., Casares-Guillén, C., Molina, J., Rubio, G., Jurado-Barba, R., Morales, I., & Ellgring, H. (2011). Efectos diferenciales de la doble tarea en el procesamiento emocional en pacientes con enfermedad de parkinson no medicados. [Differential effects of dual task in emotional processing in unmedicated Parkinson’s disease patients]. Revista de Neurología, 53, 329–336.Google Scholar
Garcia-Rodriguez, B., Fusari, A., & Ellgring, H. (2008). Procesamiento emocional de las expresiones faciales en el envejecimiento normal y patologico. [Emotional processing of facial expressions in normal and pathological ageing]. Revista De Neurologia, 46(10), 609–617.Google Scholar
Goffaux, V., & Dakin, S. (2010). Horizontal information drives the behavioural signatures of face processing. Frontiers in Psychology, 1, 143. doi:10.3389/fpsyg.2010.00143Google Scholar
Gray, H.M., & Tickle-Degnen, L. (2010). A meta-analysis of performance on emotion recognition tasks in Parkinson’s disease. Neuropsychology, 24(2), 176–191. doi:10.1037/a0018104Google Scholar
Harding, A.J., Stimson, E., Henderson, J.M., & Halliday, G.M. (2002). Clinical correlates of selective pathology in the amygdala of patients with Parkinson’s disease. Brain, 125(11), 2431–2445. doi:10.1093/brain/awf251Google Scholar
Haxby, J.V., & Gobbini, M.I. (2011). Distributed neural systems for face perception. In G. Rhodes, A. Calder, M. Johnson & J.V. Haxby (Eds.), Oxford handbook of face perception (pp. 93–110). Oxford: Oxford University Press.Google Scholar
Haxby, J.V., Hoffman, E.A., & Gobbini, M.I. (2000). The distributed human neural system for face perception. Trends in Cognitive Science, 4(6), 223–233.Google Scholar
Herrera, E., Cuetos, F., & Rodriguez-Ferreiro, J. (2011). Emotion recognition impairment in Parkinson’s disease patients without dementia. Journal of Neurological Science, 310(1–2), 237–240. doi:10.1016/j.jns.2011.06.034Google Scholar
Hoehn, M.M., & Yahr, M.D. (1967). Parkinsonism: Onset, progression and mortality. Neurology, 17(5), 427–442.Google Scholar
Hughes, A.J., Ben-Shlomo, Y., Daniel, S.E., & Lees, A.J. (2001). What features improve the accuracy of clinical diagnosis in Parkinson’s disease: A clinicopathologic study. 1992. Neurology, 57(10 Suppl 3), S34–S38. doi:10.1212/WNL.42.6.1142Google Scholar
Ibarretxe-Bilbao, N., Junque, C., Tolosa, E., Martí, M.J., Valldeoriola, F., … Zarei, M. (2009). Neuroanatomical correlates of impaired decision-making and facial emotion recognition in early Parkinson’s disease. European Journal of Neuroscience, 6, 1162–1171. doi:10.1111/j.1460-9568.2009.06892.xGoogle Scholar
Izal, M., Montorio, I., Nuevo, R., Perez-Rojo, G., & Cabrera, I. (2010). Optimising the diagnostic performance of the geriatric depression scale. Psychiatry Research, 178(1), 142–146. doi:10.1016/j.psychres.2009.02.018Google Scholar
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(4), 623–630. doi:10.1016/S0010-9452(08)70026-1Google Scholar
Kaplan, E., Goodglass, H., & Weintraub, S. (1983). Boston Naming Test. Philadelphia: Lee & Febiger.Google Scholar
Kehagia, A.A., Barker, R.A., & Robbins, T.W. (2010). Neuropsychological and clinical heterogeneity of cognitive impairment and dementia in patients with Parkinson’s disease. The Lancet Neurology, 9(12), 1200–1213. doi:10.1016/S1474-4422(10)70212-XGoogle Scholar
Lachenal-Chevallet, K., Bediou, B., Bouvard, M., Thobois, S., Broussolle, E., Vighetto, A., & Krolak-Salmon, P. (2006). Emotional facial expression recognition impairment in Parkinson disease. Psychologie and Neuropsychiatrie Vieillissement, 4(1), 61–67.Google Scholar
Lee, E.Y., Cowan, N., Vogel, E.K., Rolan, T., Valle-Inclan, F., & Hackley, S.A. (2010). Visual working memory deficits in patients with Parkinson’s disease are due to both reduced storage capacity and impaired ability to filter out irrelevant information. Brain: A Journal of Neurology, 133(9), 2677–2689. doi:10.1093/brain/awq197Google Scholar
Low, K.A., Miller, J., & Vierck, E. (2002). Response slowing in Parkinson’s disease: A psychophysiological analysis of premotor and motor processes. Brain: A Journal of Neurology, 125(Pt 9), 1980–1994. doi:10.1093/brain/awf206Google Scholar
Martinez-Martin, P., Forjaz, M.J., Cubo, E., Frades, B., & de Pedro Cuesta, J. (2006). Global versus factor-related impression of severity in Parkinson’s disease: A new clinimetric index (CISI-PD). Movement Disorders, 21(2), 208–214. doi:10.1002/mds.20697Google Scholar
Martinez-Martin, P., & Frades Payo, B. (1998). Quality of life in Parkinson’s disease: Validation study of the PDQ-39 Spanish version. The grupo centro for study of movement disorders. Journal of Neurology, 245(Suppl 1), S34–S38.Google Scholar
Miller, K.M., Price, C.C., Okin, M.S., Montijo, H., & Bowers, D. (2009). Is the N-back task a valid neuropsychological measure for assessing working memory? Archives of Clinical Neuropsychology, 24, 711–717. doi:10.1093/arclin/acp063Google Scholar
Narme, P., Bonnet, A.M., Dubois, B., & Chaby, L. (2011). Understanding facial emotion perception in Parkinson’s disease: The role of configural processing. Neuropsychologia, 49(12), 3295–3302. doi:10.1016/j.neuropsychologia.2011.08.002Google Scholar
Nee, D.E., Brown, J.W., Askren, M.K., Berman, M.G., Demiralp, E., Krawitz, A., & Jonides, J. (2013). A meta-analysis of executive components of working memory. Cerebral Cortex, 23, 264–282. doi:10.1093/cercor/bhs007CrossRefGoogle ScholarPubMed
Owen, A.M. (2004). Cognitive dysfunction in Parkinson’s disease: The role of frontostriatal circuitry. The Neuroscientist, 9(7), 1–13. doi:10.1177/1073858404266776Google Scholar
Owen, A.M., McMillan, K.M., Laird, A.R., & Bullmore, E. (2005). N-back working memory paradigm: A meta-analysis of normative functional neuroimaging studies. Human Brain Mapping, 25(1), 46–59. doi:10.1002/hbm.20131Google Scholar
Park, D.C., & Bischof, G.N. (2013). The aging mind neuroplasticity in response to cognitive training. Dialogues in Clinical Neuroscience, 15(1), 109–119.Google Scholar
Pell, M.D., & Leonard, C.L. (2005). Facial expression decoding in early Parkinson’s disease. Cognitive Brain Research, 23, 327–340. doi:10.1016/j.cogbrainres.2004.11.004Google Scholar
Peron, J., Dondaine, T., Le Jeune, F., Grandjean, D., & Verin, M. (2012). Emotional processing in Parkinson’s disease: A systematic review. Movement Disorders, 27(2), 186–199. doi:10.1002/mds.24025Google Scholar
Phillips, L.H., Channon, S., Tunstall, M., Hedenstrom, A., & Lyons, K. (2008). The role of working memory in decoding emotions. Emotion, 8(2), 184–191. doi:10.1037/1528-3542.8.2.184Google Scholar
Possin, K.L., Filoteo, J.V., Song, D.D., & Salmon, D.P. (2008). Spatial and object working memory deficits in Parkinson’s disease are due to impairment in different underlying processes. Neuropsychology, 22(5), 585–595. doi:10.1037/a0012613Google Scholar
Postle, B.R. (2006). Working memory as an emergent property of the mind and brain. Neuroscience, 139(1), 23–38. doi:10.1016/j.neuroscience.2005.06.005Google Scholar
Ranchet, M., Paire-Ficout, L., Marin-Lamellet, C., Bernard, L., & Brousolle, E. (2011). Impaired updating ability in drivers with Parkinson’s disease. Journal of Neurology, Neurosurgery, and Psychiatry, 82, 218–223. doi:10.1136/jnnp.2009.203166Google Scholar
Repovs, G., & Baddeley, A. (2006). The multi-component model of working memory: Explorations in experimental cognitive psychology. Neuroscience, 139(1), 5–21. doi:10.1016/j.neuroscience.2005.12.061Google Scholar
Reynolds, C.R. (2002). Comprehensive trail-making test. Examiner’s manual. Austin, TX: PRO-ED.Google Scholar
Rilling, L.M. (2003). Complex figure performance in patients with Parkinson’s disease: The role of planning and strategy in visuoconstruction and visuospatial memory. Dissertation Abstracts International: Section B: The Sciences and Engineering, 63(10B), 4922.Google Scholar
Rottschy, C., Caspers, S., Roski, C., Reetz, K., Dogan, I., Schultz, J.B., … Eickhoff, S.B. (2012). Differentiated parietal connectivity of frontal regions for “what” and “where” memory. Brain Structure and Function. Retrieved from http://cogprints.org/5780/1/ECSRAP.F07.pdf. doi:10.1007/s00429-012-0476-4Google Scholar
Rottschy, C., Langner, R., Dogan, I., Reetz, K., Laird, A.R., Schulz, J.B., … Eickhoff, S.B. (2012). Modelling neural correlates of working memory: A coordinate- based meta-analysis. Neuroimage, 60(1), 830–846. doi:10.1016/j.neuroimage.2011.11.050Google Scholar
Salgado-Pineda, P., Delaveau, P., Blin, O., & Nieoullon, A. (2005). Dopaminergic contribution to the regulation of emotional perception. Clinical Neuropharmacology, 28(5), 228–237.Google Scholar
Schröder, C., Mobes, J., Schutze, M., Szymanowski, F., Nager, W., Bangert, M., … Dengler, R. (2006). Perception of emotional speech in Parkinson’s disease. Movement Disorders, 21(10), 1774–1778. doi:10.1002/mds.21038CrossRefGoogle ScholarPubMed
Schwab, R.S., & England, A.C. (1969). Projection technique for evaluating surgery in Parkinson’s disease. In F.J. Gillingham & I.M.L. Donaldson (Eds.), Third symposium on Parkinson’s disease (pp. 152–157). Edinburgh: E&S Livingstone.Google Scholar
Siegert, R.J., Weatherall, M., Taylor, K.D., & Abernethy, D.A. (2008). A meta-analysis of performance on simple span and more complex working memory tasks in Parkinson’s disease. Neuropsychology, 22(4), 450–461. doi:10.1037/0894-4105.22.4.450Google Scholar
Simons, G., Ellgring, H., & Pasqualini, M.C. (2003). Disturbance of spontaneous and posed facial expressions in Parkinson’s disease. Cognition and Emotion, 17, 759–778. doi:10.1080/02699930244000138Google Scholar
Stella, F., Gobbi, L.T.B., Gobbi, S., Oliani, M.M., Tanaka, K., & Pieruccini-Faria, F. (2007). Early impairment of cognitive functions in Parkinson’s disease. Arquivos de Neuro-psiquiatria, 65(2B), 406–410. doi:10.1590/S0004-282X2007000300008Google Scholar
Stoffers, D., Berendse, H.W., Deijen, J.B., & Wolters, E.C. (2003). Deficits on Corsi’s block-tapping task in early stage Parkinson’s disease. Parkinsonism & Related Disorders, 10(2), 107–111. doi:10.1016/S1353-8020(03)00106-8CrossRefGoogle ScholarPubMed
Stuss, D.T., & Knight, R.T. (2002). Principles of Frontal lobe Function. Oxford: Oxford University Press.Google Scholar
Suzuki, A., Hoshino, T., Shigemasu, K., & Kawamura, M. (2006). Disgust-specific impairment of facial expression recognition in Parkinson’s disease. Brain, 129(Pt 3), 707–717. doi:10.1093/brain/awl011Google Scholar
Volle, E., Kinkingnehun, S., Pochon, J.B., Mondon, K., Thiebaut de Schotten, M., Seassau, M., … Levy, R. (2008). The functional architecture of the left posterior and lateral prefrontal cortex in humans. Cerebral Cortex, 18(10), 2460–2469. doi:10.1093/cercor/bhn010Google Scholar
Wager, T.D., & Smith, E.E. (2003). Neuroimaging studies of working memory: A meta-analysis. Cognitive, Affective & Behavioral Neuroscience, 3(4), 255–274. doi:10.3758/CABN.3.4.255Google Scholar
Weschler, D. (2004). Escala de memoria de weschler (WMS-III). Madrid: TEA Ediciones.Google Scholar
Yip, J.T., Lee, T.M., Ho, S.L., Tsang, K.L., & Li, L.S. (2003). Emotion recognition in patients with idiopathic Parkinson’s disease. Movement Disorders, 18(10), 1115–1122. doi:10.1002/mds.10497Google Scholar
Zgaljardic, R.J., Borod, J.C., Foldi, N.S., & Mattis, P. (2003). A review of the cognitive and behavioral sequelae of Parkinson’s disease: Relationship to frontostriatal circuitry. Cognitive and Behavioral Neuroscience, 16(4), 193–210. doi:10.1097/00146965-200312000-00001Google Scholar