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Effects of Emotional Facial Expression on Time Perception in Patients with Parkinson’s Disease

Published online by Cambridge University Press:  07 August 2015

Giovanna Mioni*
Affiliation:
Department of General Psychology, University of Padova, Italy
Lucia Meligrana
Affiliation:
U.O. Neurologia, Ospedale San Bortolo, Vicenza, Italy U.O. Psicologia Ospedaliera, Ospedale San Bortolo, Vicenza, Italy
Simon Grondin
Affiliation:
École de Psychologie, Université Laval, Québec, Canada
Francesco Perini
Affiliation:
U.O. Neurologia, Ospedale San Bortolo, Vicenza, Italy
Luigi Bartolomei
Affiliation:
U.O. Neurologia, Ospedale San Bortolo, Vicenza, Italy
Franca Stablum
Affiliation:
Department of General Psychology, University of Padova, Italy
*
Correspondence and reprint requests to: Giovanna Mioni, Department of General Psychology, University of Padova, Via Venezia, 8, 35131, Padova, Italy. E-mail: [email protected]

Abstract

Previous studies have demonstrated that emotional facial expressions alter temporal judgments. Moreover, while some studies conducted with Parkinson's disease (PD) patients suggest dysfunction in the recognition of emotional facial expression, others have shown a dysfunction in time perception. In the present study, we investigate the magnitude of temporal distortions caused by the presentation of emotional facial expressions (anger, shame, and neutral) in PD patients and controls. Twenty-five older adults with PD and 17 healthy older adults took part in the present study. PD patients were divided into two sub-groups, with and without mild cognitive impairment (MCI), based on their neuropsychological performance. Participants were tested with a time bisection task with standard intervals lasting 400 ms and 1600 ms. The effect of facial emotional stimuli on time perception was evident in all participants, yet the effect was greater for PD-MCI patients. Furthermore, PD-MCI patients were more likely to underestimate long and overestimate short temporal intervals than PD-non-MCI patients and controls. Temporal impairment in PD-MCI patients seem to be mainly caused by a memory dysfunction. (JINS, 2016, 22, 890–899)

Type
Research Articles
Copyright
Copyright © The International Neuropsychological Society 2015 

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References

Adolphs, R. (2002a). Recognizing emotion from facial expressions: Psychological and neurological mechanisms. Behavioral and Cognitive Neurosciences Review, 1(1), 2162. doi:10.1177/1534582302001001003 Google Scholar
Adolphs, R. (2002b). Neural systems for recognizing emotion. Current Opinion in Neurobiology, 12(2), 169177. doi:10.1016/S0959-4388(02)00301-X Google Scholar
Angrilli, A., Cherubini, P., Pavese, A., & Manfredini, S. (1997). The influence of affective factors on time perception. Perception & Psychophysics, 59(6), 972982. doi:10.3758/BF03205512 Google Scholar
Appollonio, I., Leone, M., Isella, V., Piamarta, F., Consoli, T., Villa, M.L., & Nichelli, P. (2005). The Frontal Assessment Battery (FAB): Normative values in an Italian population sample. Neurological Sciences, 26(2), 108116. doi:10.1007/s10072-005-0443-4 Google Scholar
Artieda, J., Pastor, M.A., Lacruz, A., & Obeso, J.A. (1992). Temporal discrimination is abnormal in Parkinson’s disease. Brain, 115(1), 199210. doi:10.1093/brain/115.1.199 Google Scholar
Assogna, F., Pontieri, F.E., Caltagirone, C., & Spalletta, G. (2008). The recognition of facial emotion expressions in Parkinson’s disease. European Neuropsychopharmacology, 18(11), 835848. doi:10.1016/j.euroneuro.2008.07.004 CrossRefGoogle ScholarPubMed
Beck, A.T., Ward, C.H., Mendelson, M., Mock, J., & Erbaugh, J. (1961). An inventory for measuring depression. Archives of General Psychiatry, 4(6), 561571. doi:10.1001/archpsyc.1961.01710120031004 CrossRefGoogle ScholarPubMed
Blonder, L.X., & Slevin, J.T. (2011). Emotional dysfunction in Parkinson’s disease. Behavioral Neurology, 24(3), 201217. doi:10.3233/BEN-2011-0329 Google Scholar
Buhusi, C.V., & Meck, W.H. (2005). What makes us tick? Functional and neural mechanisms of interval timing. Nature Reviews Neuroscience, 6(10), 755765. doi:10.1038/nrn1764 Google Scholar
Caffarra, P., Vezzadini, G., Dieci, F., Zonato, F., & Venneri, A. (2002). Rey-Osterrieth complex figure: Normative values in an Italian population sample. Neurological Sciences, 22(6), 443447. doi:10.1007/s100720200003 CrossRefGoogle Scholar
Caffarra, P., Vezzadini, G., Dieci, F., Zonato, F., & Venneri, A. (2004). Modified Card Sorting Test: Normative data. Journal of Clinical and Experimental Neuropsychology, 26(2), 246250. doi:10.1076/jcen.26.2.246.28087 Google Scholar
Calder, A.J., Keane, J., Lawrence, A.D., & Manes, F. (2004). Impaired recognition of anger following damage to the ventral striatum. Brain, 127(9), 19581969. doi:10.1093/brain/awh214 Google Scholar
Carlesimo, G.A., Caltagirone, C., Gainotti, G., Fadda, L., Gallassi, R., Lorusso, S., & Parnetti, L. (1996). The Mental Deterioration Battery: Normative data, diagnostic reliability and qualitative analyses of cognitive impairment. European Neurology, 36(6), 378384. doi:10.1159/000117297 CrossRefGoogle ScholarPubMed
Clark, U.S., Neargarder, S., & Cronin-Golomb, A. (2008). Specific impairments in the recognition of emotional facial expressions in Parkinson’s disease. Neuropsychologia, 46(9), 23002309. doi:10.1016/j.neuropsychologia.2008.03.014 CrossRefGoogle ScholarPubMed
Droit-Volet, S., & Meck, W.H. (2007). How emotions colour our perception of time. Trends in Cognitive Sciences, 11(12), 504513. doi:10.1016/j.tics.2007.09.008 Google Scholar
Droit-Volet, S., & Gil, S. (2009). The time-emotion paradox. Philosophical Transactions of the Royal Society B: Biological Sciences, 364(1525), 19431953. doi:10.1098/rstb.2009.0013 Google Scholar
Droit-Volet, S., Brunot, S., & Niedenthal, P.M. (2004). Perception of the duration of emotional events. Cognition & Emotion, 18(6), 849858. doi:10.1080/02699930341000194 CrossRefGoogle Scholar
Dujardin, K., Blairy, S., Defebvre, L., Duhem, S., Noël, Y., Hess, U., & Desté, A. (2004). Deficits in decoding emotional facial expressions in Parkinson’s disease. Neuropsychologia, 42(2), 239250. doi:10.1016/S0028-3932(03)00154-4 Google Scholar
Effron, D.A., Niedenthal, P.M., Gil, S., & Droit-Volet, S. (2006). Embodied temporal perception of emotion. Emotion, 6(1), 19. doi:10.1037/1528-3542.6.1.1 Google Scholar
Fahn, S., Elton, R.L., & the members of the UPDRS Development Committee (1987). The Unified Parkinson’s disease rating scale. In S. Fahn, C.D. Marsden, D.B. Calne, & M. Goldstein (Eds.), Recent developments in Parkinson’s disease (Vol. 2, pp. 153163). Florham Park, NJ: Macmillan Healthcare.Google Scholar
Folstein, M.F., Folstein, S., & McHugh, P. (1975). “Mini-Mental State”: A practical method for grading the cognitive state of patients for the clinician. Journal of Psychiatric Research, 12(3), 189198. doi:10.1016/0022-3956(75)90026-6 Google Scholar
Gibbon, J. (1977). Scalar expectancy theory and Weber’s law in animal timing. Psychological Review, 84(3), 279325. doi:10.1037/0033-295X.84.3.279 CrossRefGoogle Scholar
Gibbon, J., Church, R.M., & Meck, W. (1984). Scalar timing in memory. In J. Gibbon & L. Allan (Eds.), Annals of the New Academy of Sciences, Vol. 423: Timing and time perception (pp. 5277). New York: New York Academy of Sciences.Google Scholar
Gil, S., & Droit-Volet, S. (2011). How do emotional facial expression influence our perception of time? In S. Masmoundi, D. Yan Dai, & A. Naceur (Eds.), Attention, representation, and human performance: Integration of cognition, emotion and motivation. London: Psychology Press, Taylor & Francis.Google Scholar
Gil, S., & Droit-Volet, S. (2012). Emotional time distortions: The fundamental role of arousal, cognition and emotion. Cognition and Emotion, 26(5), 847862. doi:10.1080/02699931.2011.625401 Google Scholar
Gil, S., Niedenthal, P.M., & Droit-Volet, S. (2007). Anger and temporal perception in children. Emotion, 7(1), 219225. doi:10.1037/1528-3542.7.1.219 Google Scholar
Gil, S., Rousset, S., & Droit-Volet, S. (2009). How liked and disliked food affect time perception. Emotion, 9(4), 457463. doi:10.1037/a0015751 Google Scholar
Giovagnoli, A.R., Del Pesce, M., Simoncelli, M., Laiacona, M., & Capitani, E. (1996). Trail making test: Normative values from 287 normal adult controls. The Italian Journal of Neurological Sciences, 17(4), 305309. doi:10.1007/BF01997792 Google Scholar
Goodglass, H., & Kaplan, E. (1972). The assessment of aphasias and related disorders. Philadelphia: Lea and Febiger.Google Scholar
Gray, H.M., & Tickle-Degnen, L. (2010). A meta-analysis of performance on emotion recognition tasks in Parkinson’s disease. Neuropsychology, 24(2), 176191. doi:10.1037/a0018104 Google Scholar
Grondin, S. (2008). Methods for studying psychological time. In S. Grondin (Ed.), Psychology of time (pp. 5174). Bingley, UK: Emerald Group Publishing.Google Scholar
Grondin, S. (2010). Timing and time perception: A review of recent behavioral and neuroscience findings and theoretical directions. Attention, Perception & Psychophysics, 72(3), 561582. doi:10.3758/APP.72.3.561 CrossRefGoogle ScholarPubMed
Grondin, S., Laflamme, V., & Gontier, E. (2014). Effect on perceived duration and sensitivity to time when observing disgusted faces and disgusting mutilation pictures. Attention, Perception & Psychophysics, 76(6), 15221534. doi:10.3758/s13414-014-0682-7 CrossRefGoogle ScholarPubMed
Ivry, R.B., & Keele, S.W. (1989). Timing functions of the cerebellum. Journal of Cognitive Neuroscience, 1(2), 136152. doi:10.1162/jocn.1989.1.2.136 Google Scholar
Haidt, J. (2003). The moral emotions. In R.J. Davidson, K.R. Scherer & H.H. Goldsmith (Eds.), Handbook of affective sciences (pp. 852870). Oxford: Oxford University Press.Google Scholar
Harrington, D.L., Haaland, K.Y., & Knight, R.T. (1998). Cortical networks underlying mechanisms of time perception. The Journal of Neuroscience, 18(3), 10851095.Google Scholar
Harrington, D.L., Zimbelman, J.L., Hinton, S.C., & Rao, S.M. (2010). Neural modulation of temporal encoding, maintenance, and decision processes. Cerebellar Cortex, 20(6), 12741285. doi:10.1093/cercor/bhp194 Google Scholar
Harrington, D.L., Castillo, G.N., Greenberg, P.A., Song, D.D., Lessig, S., Lee, R.R., & Rao, S.M. (2011). Neurobehavioral mechanisms of temporal processing deficits in Parkinson’s disease. PLoS One, 6(2), e17461. doi:10.1371/journal.pone.0017461 CrossRefGoogle ScholarPubMed
Jankovic, J., & Tolosa, E. (eds.) (2007). Parkinson's disease and movement disorders. Philadelphia: Lippincott Williams & Wilkins.Google Scholar
Jones, C.R.G., Malone, T.J.L., Dirnberger, G., Edwards, M., & Jahanshahi, M. (2008). Basal ganglia, dopamine and temporal processing: Performance on three timing tasks on and off medication in Parkinson’s disease. Brain and Cognition, 68(1), 3041. doi:10.1016/j.bandc.2008.02.121 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(4), 623630. doi:10.1016/S0010-9452(08)70026-1 Google Scholar
Koch, G., Brusa, L., Olivieri, M., Stanzione, P., & Caltagirone, C. (2005). Memory for time intervals is impaired in left hemi-Parkinson patients. Neuropsychologia, 43(8), 11631167. doi:10.1016/j.neuropsychologia.2004.11.017 CrossRefGoogle ScholarPubMed
Koch, G., Costa, A., Brusa, L., Peppe, A., Gatto, I., … Caltagirone, C. (2008). Impaired reproduction of second but not millisecond time intervals in Parkinson’s disease. Neuropsychologia, 46(5), 13051313. doi:10.1016/j.neuropsychologia.2007.12.005 Google Scholar
Lagattuta, K.H., & Thompson, R.A. (2007). The development of self-conscious emotions: Cognitive processes and social influences. In J.L. Tracy, R.W. Robins, & J.P. Tangney (Eds.), The self-conscious emotions: Theory and research (pp. 91113). New York: Guilford.Google Scholar
Lange, K.W., Tucha, O., Steup, A., Gsell, W., & Naumann, M. (1995). Subjective time estimation in Parkinson’s disease. Journal of Neural Transmission. Supplementum, 46, 433438.Google 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(1), 6574. doi:10.1016/j.neuropsychologia.2006.04.016 Google Scholar
Lee, K.L., Seelam, K., & O’Brien, T. (2011). The relativity of time perception produced by facial emotion stimuli. Cognition & Emotion, 25(8), 14711480. doi:10.1080/02699931.2010.544455 Google Scholar
Litvan, I., Goldman, J.G., Tröster, A.I., Schmand, B.A., Weintraub, D., Petersen, R.C., & Emre, M. (2012). Diagnostic criteria for mild cognitive impairment in Parkinson's disease: Movement disorder society task force guidelines. Movement Disorders, 27(3), 349356. doi:10.1002/mds.24893 Google Scholar
Luzzatti, C., Willmes, K., & De Bleser, R. (1991). AAT - Aachener Aphasia test (AAT) - Versione Italiana. Firenze: OS–Organizzazioni speciali.Google Scholar
Malapani, C., Deweer, B., & Gibbon, J. (2002). Separating storage from retrieval dysfunction of temporal memory in Parkinson’s disease. Journal of Cognitive Neuroscience, 14(2), 311322. doi:10.1162/089892902317236920 Google Scholar
Malapani, C., Rakitin, B., Levy, R., Meck, W., Deweer, B., Dubois, B., & Gibbon, J. (1998). Coupled temporal memories in Parkinson’s disease: A dopamine-related dysfunction. Journal of Cognitive Neuroscience, 10(3), 316331. doi:10.1162/089892998562762 Google Scholar
Meck, W.H. (1996). Neuropharmacology of timing and time perception. Cognitive Brain Research, 3(3), 227242. doi:10.1016/0926-6410(96)00009-2 CrossRefGoogle ScholarPubMed
Meck, W.H. (2005). Neuropsychology of timing and time perception. Brain and Cognition, 58(1), 18. doi:10.1016/j.bandc.2004.09.004 Google Scholar
Meck, W.H., & Benson, A.M. (2002). Dissecting the brain’s internal clock: How frontal–striatal circuitry keeps time and shifts attention. Brain and Cognition, 48(1), 195211. doi:10.1006/brcg.2001.1313 CrossRefGoogle ScholarPubMed
Mella, N., Conty, L., & Pouthas, V. (2011). The role of physiological arousal in time perception: Psychophysiological evidence from an emotion regulation paradigm. Brain and Cognition, 75(2), 182187. doi:10.1016/j.bandc.2010.11.012 CrossRefGoogle ScholarPubMed
Mioni, G., Mattalia, G., & Stablum, F. (2013). Time perception in severe traumatic brain injury patients: A study comparing different methodologies. Brain and Cognition, 81(3), 305312. doi:10.1016/j.bandc.2012.12.005 Google Scholar
Mioni, G., Stablum, F., McClintock, S.M., & Grondin, S. (2014). Different methods for reproducing time, different results. Attention, Perception and Psychophysics, 76(3), 675681. doi:10.3758/s13414-014-0625-3 Google Scholar
Mondini, S., Mapelli, D., Vestri, A., & Bisiacchi, P.S. (2003). Esame neuropsicologico breve. Una batteria di test per lo screening neuropsicologico. Milano: Cortina Raffaello.Google Scholar
Nasreddine, Z.S., Phillips, N.A., Bedirian, V., Charbonneau, S., Whitehead, V., Collin, I., & Chertkow, H. (2005). The Montreal Cognitive Assessment, MoCA: A brief screening tool for mild cognitive impairment. Journal of the American Geriatrics Society, 53(4), 695699. doi:10.1111/j.1532-5415.2005.53221.x CrossRefGoogle Scholar
Nelson, H.E. (1976). A modified card sorting test sensitive to frontal lobe defects. Cortex, 12(4), 313324. doi:10.1016/S0010-9452(76)80035-4 Google Scholar
Noulhiane, M., Mella, N., Samson, S., Ragot, R., & Pouthas, V. (2007). How emotional auditory stimuli modulate time perception. Emotion, 7(4), 697704. doi:10.1037/1528-3542.7.4.697 Google Scholar
Novelli, G., Papagno, C., Capitani, E., Laiacona, M., Cappa, S.F., & Vallar, G. (1986). Tre test clinici di ricerca e produzione lessicale. Taratura su soggetti normali. Archivio di Psicologia Neurologia Psichiatria, 47, 477506.Google Scholar
O’Boyle, D.J., Freeman, J.S., & Cody, F.W. (1996). The accuracy and precision of timing of self-paced, repetitive movements in subjects with Parkinson’s disease. Brain, 119(1), 5170. doi:10.1093/brain/119.1.51 Google Scholar
Osterrieth, P.A. (1944). Les tets de copie d’une figure complexe. Archives de Psicologies, 30, 206356.Google Scholar
Pastor, M.A., Jahanshahi, M., Artieda, J., & Obeso, J.A. (1992). Performance of repetitive wrist movements in Parkinson’s disease. Brain, 115(3), 875891. doi:10.1093/brain/115.3.875 Google Scholar
Pastor, M.A., Artieda, J., Jahanshahi, M., & Obeso, J.A. (1992). Time estimation and reproduction is abnormal in Parkinson’s disease. Brain, 115(1), 211225. doi:10.1093/brain/115.1.211 Google Scholar
Phelps, E.A., & Ledoux, J.E. (2005). Contributions of the amygdala to emotion processing: From animal models to human behavior. Neuron, 48(2), 175187. doi:10.1016/j.neuron.2005.09.025 Google Scholar
Perbal, S., Droit-Volet, S., Isingrini, M., & Pouthas, V. (2002). Relationships between age-related changes in time estimation and age-related changes in processing speed, attention, and memory. Aging, Neuropsychology and Cognition, 9(3), 201216. doi:10.1076/anec.9.3.201.9609 CrossRefGoogle Scholar
Perbal, S., Deweer, B., Pillon, B., Vidailhet, M., Dubois, B., & Pouthas, V. (2005). Effects of internal clock and memory disorders on duration reproductions and duration productions in patients with Parkinson’s disease. Brain and Cognition, 58(1), 3548. doi:10.1016/j.bandc.2005.02.003 Google Scholar
Péron, J., Dondaine, T., LeJeune, F., Grandjean, D., & Vérin, M. (2012). Emotional processing in Parkinson’s disease: A systematic review. Movement Disorders, 27(2), 186199. doi:10.1002/mds.24025 Google Scholar
Péron, J., Biseul, I., Leray, E., Vicente, S., La Jeune, F., Drapier, S., & Vérin, M. (2010). Subthalamic nucleus stimulation affects fear and sadness recognition in Parkinson’s disease. Neuropsychology, 24(1), 18. doi:10.1037/a0017433 Google Scholar
Rammsayer, T.H. (1997). The effects of body core temperature and brain dopamine activity on timing processes in humans. Biological Psychology, 46(2), 169192. doi:10.1016/S0301-0511(97)05251-4 Google Scholar
Rammsayer, T.H. (1999). Neuropharmacological evidence for different timing mechanism in humans. The Quarterly Journal of Experimental Psychology: Section B, 52(3), 273286. doi:10.1080/713932708 Google Scholar
Reitan, R.M. (1958). Validity of the Trial Making Test as an indicator of organic brain damage. Perceptual and Motor Skills, 8(3), 271276. doi:10.2466/pms.1958.8.3.271 Google Scholar
Rey, A. (1958). Mémorisation d’une série de 15 mots en 5 répétitions. In A. Rey (Ed.), L’examen Clinique en Psychologie. Paris: Presses Universitaires de France.Google Scholar
Riesen, J.M., & Schnider, A. (2001). Time estimation in Parkinson's disease: normal long duration estimation despite impaired short duration discrimination. Journal of Neurology, 248(1), 2735. doi:10.1007/s004150170266 Google Scholar
Smith, J.G., Harper, D.N., Gittings, D., & Abernethy, D. (2007). The effect of Parkinson’s disease on time estimation as a function of stimulus duration range and modality. Brain and Cognition, 64(2), 130143. doi:10.1016/j.bandc.2007.01.005 CrossRefGoogle ScholarPubMed
Sotgiu, I., & Rusconi, M.L. (2013). Investigating emotions in Parkinson’s disease: What we know and what we still don’t know. Frontiers in Psychology, 4, 336. doi:10.3389/fpsyg.2013.00336 Google Scholar
Sprengelmeyer, R., Young, A.W., Mahn, K., Schroeder, U., Woitalla, D., Buttner, T., & Przuntek, H. (2003). Facial expression recognition in people with medicated and un-medicated Parkinson’s disease. Neuropsychologia, 41(8), 10471057. doi:10.1016/S0028-3932(02)00295-6 Google Scholar
Suzuki, A., Hoshino, T., Shigemasu, K., & Kawamura, M. (2006). Disgust-specific impairment of facial expression recognition in Parkinson's disease. Brain, 129(3), 707717. doi:10.1093/brain/awl011 Google Scholar
Tangney, J.P., & Dearing, R.L. (2002). Shame and guilt. New York: Guilford Press.Google Scholar
Tipples, J. (2008). Negative emotionality influences the effects of emotion on time perception. Emotion, 8(1), 127131. doi:10.1037/1528-3542.8.1.127 Google Scholar
Treisman, M. (1963). Temporal discrimination and the indifference interval: Implication for model of the “internal clock”. Psychological Monographs General and Applied, 77(13), 131.Google Scholar
Wearden, J.H., & Penton-Voak, I.S. (1995). Feeling the heat: Body temperature and the rate of subjective time revisited. The Quarterly Journal of Experimental Psychology, 48(2), 129141. doi:10.1080/14640749508401443 Google Scholar
Yip, J.T., Lee, T., Ho, S.L., Tsang, K.L., & Li, L.S. (2003). Emotion recognition in patients with idiopathic Parkinson’s disease. Movement Disorder, 18(10), 11151122. doi:10.1002/mds.10497 Google Scholar
Zakay, D., & Block, R.A. (1996). The role of attention in time estimation processes. In M.A. Pastor & J. Artieda (Eds.), Time, internal clocks and movement (pp. 143164). Amsterdam: Elsevier.Google Scholar
Zélanti, P.S., & Droit-Volet, S. (2011). Cognitive abilities explaining age-related changes in time perception of short and long durations. Journal of Experimental Child Psychology, 109(2), 143157. doi:10.1016/j.jecp.2011.01.003 CrossRefGoogle Scholar