Hostname: page-component-7479d7b7d-q6k6v Total loading time: 0 Render date: 2024-07-12T19:55:01.609Z Has data issue: false hasContentIssue false
  • English
  • Français

Reduced Enhancement of Memory for Faces Encoded by Semantic and Socioemotional Processes in Patients with Parkinson’s Disease

Published online by Cambridge University Press:  11 December 2019

Paeksoon Park ,
Hodaka Yamakado ,
Ryosuke Takahashi ,
Shikiho Dote ,
Shiho Ubukata ,
Toshiya Murai  and
Takashi Tsukiura
Paeksoon Park*
Affiliation:
Department of Cognitive and Behavioral Sciences, Graduate School of Human and Environmental Studies, Kyoto University, Kyoto, Kyoto606-8501, Japan Department of Psychiatry, Kyoto University Graduate School of Medicine, Kyoto, Kyoto606-8507, Japan Faculty of Comprehensive Rehabilitation, Kobegakuin University, Kobe, Hyogo651-2180, Japan
Hodaka Yamakado
Affiliation:
Department of Neurology, Kyoto University Graduate School of Medicine, Kyoto, Kyoto606-8507, Japan
Ryosuke Takahashi
Affiliation:
Department of Neurology, Kyoto University Graduate School of Medicine, Kyoto, Kyoto606-8507, Japan
Shikiho Dote
Affiliation:
Department of Cognitive and Behavioral Sciences, Graduate School of Human and Environmental Studies, Kyoto University, Kyoto, Kyoto606-8501, Japan
Shiho Ubukata
Affiliation:
Department of Psychiatry, Kyoto University Graduate School of Medicine, Kyoto, Kyoto606-8507, Japan
Toshiya Murai
Affiliation:
Department of Psychiatry, Kyoto University Graduate School of Medicine, Kyoto, Kyoto606-8507, Japan
Takashi Tsukiura
Affiliation:
Department of Cognitive and Behavioral Sciences, Graduate School of Human and Environmental Studies, Kyoto University, Kyoto, Kyoto606-8501, Japan
*
*Correspondence and reprint requests to: Paeksoon Park, Department of Cognitive and Behavioral Sciences, Graduate School of Human and Environmental Studies, Kyoto University, Yoshida-Nihonmatsu-Cho, Sakyo-ku, Kyoto, Kyoto 606-8501, Japan. E-mail: park.paeksoon.4a@kyoto-u.ac.jp
Get access Rights & Permissions [Opens in a new window]

Abstract

Objectives:

Patients with Parkinson’s disease (PD) exhibit impaired semantic and socioemotional processes, which are thought to be related to dysfunctions in the fronto-striatal circuit. However, little is known about how the memory enhancement by these processes was reduced in PD. The present study investigated this issue.

Methods:

The retrieval performance of face memories encoded by semantic and socioemotional processes was compared between 24 PD patients and 24 age-matched healthy controls (HC). During encoding, participants were presented with unfamiliar faces and made judgment about them in three encoding conditions of semantic judgment (Semantics), attractiveness judgment (Attractiveness), and form judgment (Form). In Semantics, participants rated to what degree each face looked like an office worker, whereas in Attractiveness, participants rated how attractive each face was. The Form condition as a control required participants to judge the shape of each face. During retrieval after encoding, participants made old or new judgment for target and distracter faces.

Results:

In HC, the retrieval of faces encoded by Semantics and Attractiveness was significantly more accurate than that encoded by Form, whereas this memory enhancement was not identified in PD. In addition, individual scores in frontal lobe function and long-term memory correlated with the retrieval performance of memories encoded in Semantics and Attractiveness but not Form.

Conclusions:

These findings suggest that the processing of semantic and socioemotional signals conveyed from faces could be impaired in PD and that the impairment of these processes could decrease the enhancement of face memories by semantic and socioemotional elaborations.

Keywords

Face memoryEncodingSemantic elaborationSocioemotional elaborationMemory enhancementFronto-striatal circuit
Type
Regular Research
Information
Journal of the International Neuropsychological Society , Volume 26 , Issue 4 , April 2020 , pp. 418 - 429
Copyright
Copyright © INS. Published by Cambridge University Press, 2019

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Adcock, R.A., Thangavel, A., Whitfield-Gabrieli, S., Knutson, B., & Gabrieli, J.D. (2006). Reward-motivated learning: mesolimbic activation precedes memory formation. Neuron, 50(3), 507–517. doi: 10.1016/j.neuron.2006.03.036CrossRefGoogle ScholarPubMed
Algarabel, S., Rodriguez, L.A., Escudero, J., Fuentes, M., Peset, V., Pitarque, A., Cómbita, L.M., & Mazon, J.F. (2010). Recognition by familiarity is preserved in Parkinson’s without dementia and Lewy-Body disease. Neuropsychology, 24(5), 599–607. doi: 10.1037/a0019221CrossRefGoogle ScholarPubMed
Argaud, S., Verin, M., Sauleau, P., & Grandjean, D. (2018). Facial emotion recognition in Parkinson’s disease: a review and new hypotheses. Movement Disorders, 33(4), 554–567. doi: 10.1002/mds.27305CrossRefGoogle ScholarPubMed
Beatty, W.W., Monson, N., & Goodkin, D.E. (1989). Access to semantic memory in Parkinson’s disease and multiple sclerosis. Journal of Geriatric Psychiatry and Neurology, 2(3), 153–162. doi: 10.1177/089198878900200306Google ScholarPubMed
Bower, G.H. & Karlin, M.B. (1974). Depth of processing pictures of faces and recognition memory. Journal of Experimental Psychology, 103(4), 751. doi: 10.1037/h0037190CrossRefGoogle Scholar
Cohn, M., Moscovitch, M., & Davidson, P.S. (2010). Double dissociation between familiarity and recollection in Parkinson’s disease as a function of encoding tasks. Neuropsychologia, 48(14), 4142–4147. doi: 10.1016/j.neuropsychologia.2010.10.013CrossRefGoogle ScholarPubMed
Craik, F.I.M. & Lockhart, R.S. (1972). Levels of processing: a framework for memory research. Journal of Verbal Learning and Verbal Behavior, 11(6), 671–684. doi: 10.1016/S0022-5371(72)80001-XCrossRefGoogle Scholar
Daselaar, S.M., Fleck, M.S., Dobbins, I.G., Madden, D.J., & Cabeza, R. (2006). Effects of healthy aging on hippocampal and rhinal memory functions: an event-related fMRI study. Cerebral Cortex, 16(12), 1771–1782. doi: 10.1093/cercor/bhj112CrossRefGoogle Scholar
Davidson, P.S., Anaki, D., Saint-Cyr, J.A., Chow, T.W., & Moscovitch, M. (2006). Exploring the recognition memory deficit in Parkinson’s disease: estimates of recollection versus familiarity. Brain, 129(Pt 7), 1768–1779. doi: 10.1093/brain/awl115CrossRefGoogle ScholarPubMed
Dubois, B., Slachevsky, A., Litvan, I., & Pillon, B. (2000). The FAB: a Frontal Assessment. Neurology, 55(11), 1621–1626. doi: 10.1212/WNL.55.11.1621CrossRefGoogle ScholarPubMed
Dupont, S., Samson, Y., Le Bihan, D., & Baulac, M. (2002). Anatomy of verbal memory: a functional MRI study. Surgical and Radiologic Anatomy, 24(1), 57–63. doi: 10.1007/s00276-002-0005-xCrossRefGoogle ScholarPubMed
Gallo, D.A., Meadow, N.G., Johnson, E.L., & Foster, K.T. (2008). Deep levels of processing elicit a distinctiveness heuristic: evidence from the criterial recollection task. Journal of Memory and Language, 58(4), 1095–1111. doi: 10.1016/j.jml.2007.12.001CrossRefGoogle Scholar
Green, J., McDonald, W.M., Vitek, J.L., Evatt, M., Freeman, A., Haber, M., Bakay, R.A., Triche, S., Sirockman, B., & DeLong, M.R. (2002). Cognitive impairments in advanced PD without dementia. Neurology, 59(9), 1320–1324. doi: 10.1212/01.wnl.0000031426.21683.e2CrossRefGoogle ScholarPubMed
Grogan, J., Bogacz, R., Tsivos, D., Whone, A., & Coulthard, E. (2015). Dopamine and consolidation of episodic memory: timing is everything. Journal of Cognitive Neuroscience, 27(10), 2035–2050. doi: 10.1162/jocn_a_00840CrossRefGoogle ScholarPubMed
Grossman, M., Carvell, S., Gollomp, S., Stern, M.B., Vernon, G., & Hurtig, H.I. (1991). Sentence comprehension and praxis deficits in Parkinson’s disease. Neurology, 41(10), 1620–1626. doi: 10.1212/WNL.41.10.1620Google ScholarPubMed
Haber, S.N. & Knutson, B. (2010). The reward circuit: linking primate anatomy and human imaging. Neuropsychopharmacology, 35(1), 4–26. doi: 10.1038/npp.2009.129CrossRefGoogle ScholarPubMed
Hahn, A.C. & Perrett, D.I. (2014). Neural and behavioral responses to attractiveness in adult and infant faces. Neuroscience and Biobehavioral Reviews, 46 Pt 4, 591–603. doi: 10.1016/j.neubiorev.2014.08.015CrossRefGoogle ScholarPubMed
Henry, J.D. & Crawford, J.R. (2004). Verbal fluency deficits in Parkinson’s disease: a meta-analysis. Journal of the International Neuropsychological Society, 10(4), 608–622. doi: 10.1017/s1355617704104141CrossRefGoogle ScholarPubMed
Ibarretxe-Bilbao, N., Junque, C., Tolosa, E., Marti, M.J., Valldeoriola, F., Bargallo, N., & Zarei, M. (2009). Neuroanatomical correlates of impaired decision-making and facial emotion recognition in early Parkinson’s disease. European Journal of Neuroscience, 30(6), 1162–1171. doi: 10.1111/j.1460-9568.2009.06892.xCrossRefGoogle ScholarPubMed
Ishai, A. (2007). Sex, beauty and the orbitofrontal cortex. International Journal of Psychophysiology, 63(2), 181–185. doi: 10.1016/j.ijpsycho.2006.03.010CrossRefGoogle ScholarPubMed
Kampe, K.K., Frith, C.D., Dolan, R.J., & Frith, U. (2001). Reward value of attractiveness and gaze. Nature, 413(6856), 589. doi: 10.1038/35098149CrossRefGoogle ScholarPubMed
Karrasch, M., Laatu, S., Martikainen, K., & Marttila, R. (2013). CERAD test performance and cognitive impairment in Parkinson’s disease. Acta Neurologica Scandinavica, 128(6), 409–413. doi: 10.1111/ane.12138CrossRefGoogle ScholarPubMed
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. Lancet Neurology, 9(12), 1200–1213. doi: 10.1016/s1474-4422(10)70212-xCrossRefGoogle ScholarPubMed
Kiernan, R.J., Mueller, J., Langston, J.W., & Van Dyke, C. (1987). The Neurobehavioral Cognitive Status Examination: a brief but quantitative approach to cognitive assessment. Annals of Internal Medicine, 107(4), 481–485. doi: 10.7326/0003-4819-107-4-481CrossRefGoogle ScholarPubMed
Kobayakawa, M., Koyama, S., Mimura, M., & Kawamura, M. (2008). Decision making in Parkinson’s disease: analysis of behavioral and physiological patterns in the Iowa gambling task. Movement Disorders, 23(4), 547–552. doi: 10.1002/mds.21865CrossRefGoogle ScholarPubMed
Koerts, J., Meijer, H.A., Colman, K.S., Tucha, L., Lange, K.W., & Tucha, O. (2013). What is measured with verbal fluency tests in Parkinson’s disease patients at different stages of the disease? Journal of Neural Transmission, 120(3), 403–411. doi: 10.1007/s00702-012-0885-9CrossRefGoogle ScholarPubMed
Lees, A.J. & Smith, E. (1983). Cognitive deficits in the early stages of Parkinson’s disease. Brain, 106 (Pt 2), 257–270. doi: 10.1093/brain/106.2.257CrossRefGoogle ScholarPubMed
Lewis, S.J., Cools, R., Robbins, T.W., Dove, A., Barker, R.A., & Owen, A.M. (2003). Using executive heterogeneity to explore the nature of working memory deficits in Parkinson’s disease. Neuropsychologia, 41(6), 645–654. doi: 10.1016/S0028-3932(02)00257-9CrossRefGoogle ScholarPubMed
Lezak, M.D. (1983). Neuropsychological Assessment (2nd ed.). New York: Oxford University Press.Google Scholar
Lezak, M.D. (1995). Neuropsychological Assessment (3rd ed.). New York: Oxford University Press.Google Scholar
Marzi, T. & Viggiano, M.P. (2010). Deep and shallow encoding effects on face recognition: an ERP study. International Journal of Psychophysiology, 78(3), 239–250. doi: 10.1016/j.ijpsycho.2010.08.005CrossRefGoogle ScholarPubMed
Matsuda, O. & Nakatani, M. (2004). Manual for Japanese version of the Neurobehavioral Cognitive Status Examination (COGNISTAT). Tokyo: World Planning.Google Scholar
Matsumoto, D. & Ekman, P. (1988). Japanese and Caucasian facial expressions of emotion and neutral faces (JACFEE and JACNeuF). San Francisco: Intercultural and Emotion Research Laboratory, Department of Psychology, San Francisco State University.Google Scholar
McKinlay, A., Grace, R.C., Dalrymple-Alford, J.C., & Roger, D. (2010). Characteristics of executive function impairment in Parkinson’s disease patients without dementia. Journal of the International Neuropsychological Society, 16(2), 268–277. doi: 10.1017/s1355617709991299CrossRefGoogle ScholarPubMed
Mimura, M., Oeda, R., & Kawamura, M. (2006). Impaired decision-making in Parkinson’s disease. Parkinsonism & Related Disorders, 12(3), 169–175. doi: 10.1016/j.parkreldis.2005.12.003CrossRefGoogle ScholarPubMed
Morris, R.G., Downes, J.J., Sahakian, B.J., Evenden, J.L., Heald, A., & Robbins, T.W. (1988). Planning and spatial working memory in Parkinson’s disease. Journal of Neurology, Neurosurgery and Psychiatry, 51(6), 757–766. doi: 10.1136/jnnp.51.6.757CrossRefGoogle ScholarPubMed
Muslimovic, D., Post, B., Speelman, J.D., & Schmand, B. (2005). Cognitive profile of patients with newly diagnosed Parkinson disease. Neurology, 65(8), 1239–1245. doi: 10.1212/01.wnl.0000180516.69442.95CrossRefGoogle ScholarPubMed
O’Doherty, J., Winston, J., Critchley, H., Perrett, D., Burt, D.M., & Dolan, R.J. (2003). Beauty in a smile: the role of medial orbitofrontal cortex in facial attractiveness. Neuropsychologia, 41(2), 147–155. doi: 10.1016/S0028-3932(02)00145-8CrossRefGoogle Scholar
Otten, L.J., Henson, R.N., & Rugg, M.D. (2001). Depth of processing effects on neural correlates of memory encoding: relationship between findings from across- and within-task comparisons. Brain, 124(Pt 2), 399–412. doi: 10.1093/brain/124.2.399CrossRefGoogle ScholarPubMed
Owen, A.M., James, M., Leigh, P.N., Summers, B.A., Marsden, C.D., Quinn, N.P., Lange, K.W., & Robbins, T.W. (1992). Fronto-striatal cognitive deficits at different stages of Parkinson’s disease. Brain, 115 (Pt 6), 1727–1751. doi: 10.1093/brain/115.6.1727CrossRefGoogle ScholarPubMed
Pereira, J.B., Junque, C., Marti, M.J., Ramirez-Ruiz, B., Bartres-Faz, D., & Tolosa, E. (2009). Structural brain correlates of verbal fluency in Parkinson’s disease. Neuroreport, 20(8), 741–744. doi: 10.1097/WNR.0b013e328329370bCrossRefGoogle ScholarPubMed
Pitarque, A., Melendez, J.C., Sales, A., Satorres, E., Escudero, J., & Algarabel, S. (2017). The role of recollection and familiarity in nondemented Parkinson’s patients. Journal of General Psychology, 144(3), 230–243. doi: 10.1080/00221309.2017.1319793CrossRefGoogle ScholarPubMed
Raskin, S.A., Sliwinski, M., & Borod, J.C. (1992). Clustering strategies on tasks of verbal fluency in Parkinson’s disease. Neuropsychologia, 30(1), 95–99. doi: 10.1016/0028-3932(92)90018-HCrossRefGoogle ScholarPubMed
Sato, W., Kubota, Y., Okada, T., Murai, T., Yoshikawa, S., & Sengoku, A. (2002). Seeing happy emotion in fearful and angry faces: qualitative analysis of facial expression recognition in a bilateral amygdala-damaged patient. Cortex, 38(5), 727–742. doi: 10.1016/S0010-9452(08)70040-6CrossRefGoogle Scholar
Schultz, W. (2000). Multiple reward signals in the brain. Nature Reviews Neuroscience, 1, 199–207. doi: 10.1038/35044563CrossRefGoogle Scholar
Shigemune, Y., Tsukiura, T., Kambara, T., & Kawashima, R. (2014). Remembering with gains and losses: effects of monetary reward and punishment on successful encoding activation of source memories. Cerebral Cortex, 24(5), 1319–1331. doi: 10.1093/cercor/bhs415CrossRefGoogle ScholarPubMed
Shimamura, A.P., Ross, J.G., & Bennett, H.D. (2006). Memory for facial expressions: the power of a smile. Psychonomic Bulletin & Review, 13(2), 217–222. doi: 10.3758/BF03193833CrossRefGoogle Scholar
Sugishita, M. & Asada, T. (2009). About making of a depressed linear measure reduction edition for senior citizens – a Japanese edition (Geriatric Depression Scale-Short Version-Japanese, GDS-S-J). Japanese Journal of Cognitive Neuroscience, 11(1), 87–90. doi: 10.11253/ninchishinkeikagaku.11.87Google Scholar
Tanaka, Y. (1998). Neuropsychological inspection method for memory failure. Annual Review Shinkei, 50–88.Google Scholar
Thompson-Schill, S.L., D’Esposito, M., Aguirre, G.K., & Farah, M.J. (1997). Role of left inferior prefrontal cortex in retrieval of semantic knowledge: a reevaluation. Proceedings of the National Academy of Sciences of the United States of America, 94(26), 14792–14797. doi: 10.1073/pnas.94.26.14792CrossRefGoogle Scholar
Thompson-Schill, S.L., Swick, D., Farah, M.J., D’Esposito, M., Kan, I.P., & Knight, R.T. (1998). Verb generation in patients with focal frontal lesions: a neuropsychological test of neuroimaging findings. Proceedings of the National Academy of Sciences of the United States of America, 95(26), 15855–15860. doi: 10.1073/pnas.95.26.15855CrossRefGoogle ScholarPubMed
Tsukiura, T. & Cabeza, R. (2011a). Remembering beauty: roles of orbitofrontal and hippocampal regions in successful memory encoding of attractive faces. Neuroimage, 54(1), 653–660. doi: 10.1016/j.neuroimage.2010.07.046CrossRefGoogle ScholarPubMed
Tsukiura, T. & Cabeza, R. (2011b). Shared brain activity for aesthetic and moral judgments: implications for the Beauty-is-Good stereotype. Social Cognitive and Affective Neuroscience, 6(1), 138–148. doi: 10.1093/scan/nsq025CrossRefGoogle ScholarPubMed
Tsukiura, T., Fujii, T., Fukatsu, R., Otsuki, T., Okuda, J., Umetsu, A., Suzuki, K., Tabuchi, M., Yanagawa, I., Nagasaka, T., Kawashima, R., Fukuda, H., Takahashi, S., & Yamadori, A. (2002). Neural basis of the retrieval of people’s names: evidence from brain-damaged patients and fMRI. Journal of Cognitive Neuroscience, 14(6), 922–937. doi: 10.1162/089892902760191144CrossRefGoogle ScholarPubMed
Tsukiura, T., Mochizuki-Kawai, H., & Fujii, T. (2006). Dissociable roles of the bilateral anterior temporal lobe in face−name associations: an event-related fMRI study. Neuroimage, 30(2), 617–626. doi: 10.1016/j.neuroimage.2005.09.043CrossRefGoogle Scholar
Tsukiura, T., Suzuki, C., Shigemune, Y., & Mochizuki-Kawai, H. (2008). Differential contributions of the anterior temporal and medial temporal lobe to the retrieval of memory for person identity information. Human Brain Mapping, 29(12), 1343–1354. doi: 10.1002/hbm.20469CrossRefGoogle ScholarPubMed
Uchida, S. & Kawashima, R. (2008). Reading and solving arithmetic problems improves cognitive functions of normal aged people: a randomized controlled study. Age (Dordr), 30(1), 21–29. doi: 10.1007/s11357-007-9044-xCrossRefGoogle ScholarPubMed
Weiermann, B., Stephan, M.A., Kaelin-Lang, A., & Meier, B. (2010). Is there a recognition memory deficit in Parkinson’s disease? Evidence from estimates of recollection and familiarity. International Journal of Neuroscience, 120(3), 211–216. doi: 10.3109/00207450903506510CrossRefGoogle Scholar
Whittingham, M.J., Stephens, P.A., Bradbury, R.B., & Freckleton, R.P. (2006). Why do we still use stepwise modelling in ecology and behaviour? Journal of Animal Ecology, 75(5), 1182–1189. doi: 10.1111/j.1365-2656.2006.01141.xCrossRefGoogle ScholarPubMed
Winston, J.S., O’Doherty, J., Kilner, J.M., Perrett, D.I., & Dolan, R.J. (2007). Brain systems for assessing facial attractiveness. Neuropsychologia, 45(1), 195–206. doi: 10.1016/j.neuropsychologia.2006.05.009CrossRefGoogle ScholarPubMed
Wittmann, B.C., Schott, B.H., Guderian, S., Frey, J.U., Heinze, H.J., & Duzel, E. (2005). Reward-related FMRI activation of dopaminergic midbrain is associated with enhanced hippocampus-dependent long-term memory formation. Neuron, 45(3), 459–467. doi: 10.1016/j.neuron.2005.01.010CrossRefGoogle ScholarPubMed
Yesavage, J.A. & Sheikh, J.I. (1986). 9/geriatric depression scale (GDS). Clinical Gerontology, 5(1–2), 165–173. doi: 10.1300/J018v05n01_09CrossRefGoogle Scholar
Zec, R.F., Landreth, E.S., Fritz, S., Grames, E., Hasara, A., Fraizer, W., Belman, J., Wainman, S., McCool, M., O’Connell, C., Harris, R., Robbs, R., Elble, R., & Manyam, B. (1999). A comparison of phonemic, semantic, and alternating word fluency in Parkinson’s disease. Archives of Clinical Neuropsychology, 14(3), 255–264. doi: 10.1016/S0887-6177(98)00008-0CrossRefGoogle ScholarPubMed
Zgaljardic, D.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 Neurology, 16(4), 193–210. doi: 10.1097/00146965-200312000-00001CrossRefGoogle ScholarPubMed