Hostname: page-component-78c5997874-8bhkd Total loading time: 0 Render date: 2024-11-10T09:55:07.417Z Has data issue: false hasContentIssue false
  • English
  • Français

Episodic Memory Impairment in Parkinson’s Disease: Disentangling the Role of Encoding and Retrieval

Published online by Cambridge University Press:  24 September 2020

Antònia Siquier Open the ORCID record for Antònia Siquier [Opens in a new window]  and
Pilar Andrés
Antònia Siquier*
Affiliation:
Neuropsychology and Cognition Research Group, Department of Psychology, University of the Balearic Islands, Balearic Islands, Spain Research Institute on Health Sciences (IUNICS), University of the Balearic Islands, Balearic Islands, Spain Balearic Islands Health Research Institute (IdISBa), Balearic Islands, Spain
Pilar Andrés
Affiliation:
Neuropsychology and Cognition Research Group, Department of Psychology, University of the Balearic Islands, Balearic Islands, Spain Research Institute on Health Sciences (IUNICS), University of the Balearic Islands, Balearic Islands, Spain Balearic Islands Health Research Institute (IdISBa), Balearic Islands, Spain
*
*Correspondence and reprint requests to: Antònia Siquier, Department of Psychology, University of the Balearic Islands, Cra Valldemossa, Km 7.5, Palma01722, Spain. E-mail: a.siquier@uib.es
Get access Rights & Permissions [Opens in a new window]

Abstract

Objective:

The source of episodic memory (EM) impairment in Parkinson’s disease (PD) is still unclear. In the present study, we sought to quantify specifically encoding, consolidation, and retrieval process deficits in a list-learning paradigm by a novel method, the item-specific deficit approach (ISDA).

Methods:

We applied the ISDA method to the Free and Cued Selective Reminding Test (FCSRT) in a sample of 15 PD patients and 15 healthy participants.

Results:

The results revealed differences in free recall performance between PD patients and controls. These patients, however, benefited from cues as much as controls did, and total recall did not differ between groups. When analyzing the ISDA indices for encoding, consolidation, and retrieval deficits, the results showed a general memory deficit, but with a clear focus on encoding and retrieval, as revealed by the sensitivity values. Moreover, controlling for initial learning did not eliminate group effects in retrieval.

Conclusions:

Our findings reveal a mixed pattern in PD patients, with deficits in both encoding and retrieval processes in memory. Also, despite the fact that an encoding dysfunction may explain some of the deficits observed at retrieval, it cannot fully account for the differences, highlighting that both encoding and retrieval factors are necessary to understand memory deficits in PD.

Keywords

Movement disordersISDA methodLearningFCSRTFree recallCued recall
Type
Regular Research
Information
Journal of the International Neuropsychological Society , Volume 27 , Issue 3 , March 2021 , pp. 261 - 269
Copyright
Copyright © INS. Published by Cambridge University Press, 2020

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

Andrés, P., Vico, H., Yañez, A., Siquier, A., & Ferrer, G.A. (2019). Quantifying memory deficits in amnestic mild cognitive impairment. Alzheimer’s & Dementia: Diagnosis, Assessment & Disease Monitoring, 11, 108–114. https://doi.org/10.1016/j.dadm.2018.12.002 Google ScholarPubMed
Baiano, C., Barone, P., Trojano, L., & Santangelo, G. (2019). Prevalence and clinical aspects of mild cognitive impairment in Parkinson’s disease: a meta-analysis. Movement Disorder, 35, 45–54. https://doi.org/10.1002/mds.27902 CrossRefGoogle ScholarPubMed
Balthazar, M.L.F., Yasuda, C.L., Cendes, F., & Damasceno, B.P. (2010). Learning, retrieval, and recognition are compromised in aMCI and mild AD: Are distinct episodic memory processes mediated by the same anatomical structures? Journal of the International Neuropsychological Society, 16(1), 205–209. https://doi.org/10.1017/S1355617709990956 CrossRefGoogle ScholarPubMed
Baran, B., Tekcan, A.I., Gürvit, H., & Boduroglu, A. (2009). Episodic memory and metamemory in Parkinson’s disease patients. Neuropsychology, 23(6), 736–745. https://doi.org/10.1037/a0016631 CrossRefGoogle ScholarPubMed
Bezdicek, O., Ballarini, T., Buschke, H., Růžicka, F., Roth, J., Albrecht, F., & Jech, R. (2019). Memory impairment in Parkinson’s disease: the retrieval versus associative deficit hypothesis revisited and reconciled. Neuropsychology, 33(3), 391–405. https://doi.org/10.1037/neu0000503 CrossRefGoogle ScholarPubMed
Biundo, R., Weis, L., & Antonini, A. (2016). Cognitive decline in Parkinson’s disease: the complex picture. Npj Parkinson’s Disease, 2(1), 16018. https://doi.org/10.1038/npjparkd.2016.18 CrossRefGoogle ScholarPubMed
Blake, R.V., Wroe, S.J., Breen, E.K., & McCarthy, R.A. (2000). Accelerated forgetting in patients with epilepsy: evidence for an impairment in memory consolidation. Brain, 123(3), 472–483. https://doi.org/10.1093/brain/123.3.472 CrossRefGoogle ScholarPubMed
Broeders, M., Velseboer, D.C., De Bie, R., Speelman, J.D., Muslimovic, D., Post, B., & Schmand, B. (2013). Cognitive change in newly-diagnosed patients with Parkinson’s disease: a 5-year follow-up study. Journal of the International Neuropsychological Society, 19(6), 695–708. https://doi.org/10.1017/S1355617713000295 CrossRefGoogle ScholarPubMed
Brønnick, K., Alves, G., Aarsland, D., Tysnes, O.B., & Larsen, J.P. (2011). Verbal memory in drug-naive, newly diagnosed Parkinson’s disease. The retrieval deficit hypothesis revisited. Neuropsychology, 25(1), 114–124. https://doi.org/10.1037/a0020857 CrossRefGoogle ScholarPubMed
Buschke, H., Sliwinski, M.J., Kuslansky, G., & Lipton, R.B. (1997). Diagnosis of early dementia by the Double Memory Test. Neurology, 48(4), 989 LP-996. https://doi.org/10.1212/WNL.48.4.989 CrossRefGoogle ScholarPubMed
Bussè, C., Caffarra, P., Rossi, A., Zorzi, G., Fragiacomo, F., Camporese, G., & Cagnin, A. (2018). Testing Hippocampal memory in prodromal dementia with Lewy bodies. Journal of Alzheimer’s Disease. 64(2), 349–353. https://doi.org/10.3233/JAD-180166 CrossRefGoogle ScholarPubMed
Cattie, J.E., Woods, S.P., Arce, M., Weber, E., Delis, D.C., & Grant, I. (2012). Construct validity of the item-specific deficit approach to the California verbal learning Test (2nd Ed) in HIV infection. The Clinical Neuropsychologist, 26(2), 288–304. https://doi.org/10.1080/13854046.2011.653404 CrossRefGoogle Scholar
Chahine, L.M., Weintraub, D., Hawkins, K.A., Siderowf, A., Eberly, S., & Oakes, D. (2016). Cognition in individuals at risk for Parkinson’s: Parkinson associated risk syndrome (PARS) study findings. Movement Disorders, 31(1), 86–94. https://doi.org/10.1002/mds.26373 CrossRefGoogle ScholarPubMed
Chen, F.X., Kang, D.Z., Chen, F.Y., Liu, Y., Wu, G., Li, X., & Lin, Z.Y. (2016). Gray matter atrophy associated with mild cognitive impairment in Parkinson’s disease. Neuroscience Letters, 617, 160–165. https://doi.org/10.1016/j.neulet.2015.12.055 CrossRefGoogle ScholarPubMed
Chiaravalloti, N.D., Ibarretxe-Bilbao, N., Deluca, J., Rusu, O., Pena, J., García-Gorostiaga, I., & Ojeda, N. (2014). The source of the memory impairment in Parkinson’s disease: acquisition versus retrieval. Movement Disorders, 29(6), 765–771. https://doi.org/10.1002/mds.25842 CrossRefGoogle ScholarPubMed
Chiaravalloti, N.D., Sandry, J., Moore, N.B., & Deluca, J. (2016). An RCT to treat learning impairment in traumatic brain injury. Neurorehabilitation and Neural Repair, 30(6), 539–550. https://doi.org/10.1177/1545968315604395 CrossRefGoogle ScholarPubMed
Costa, A., Monaco, M., Zabberoni, S., Peppe, A., Perri, R., Fadda, L., & Carlesimo, G.A. (2014). Free and cued recall memory in Parkinson’s disease associated with amnestic mild cognitive impairment. PLoS ONE, 9(1), e86233. https://doi.org/10.1371/journal.pone.0086233 CrossRefGoogle ScholarPubMed
Diez-Quevedo, C., Rangil, T., Sanchez-Planell, L., Kroenke, K., & Spitzer, R.L. (2001). Validation and utility of the patient health questionnaire in diagnosing mental disorders in 1003 general hospital Spanish inpatients. Psychosomatic Medicine, 63(4), 679–686.CrossRefGoogle ScholarPubMed
Dubois, B., Burn, D., Goetz, C., Aarsland, D., Brown, R.G., Broe, G.A., & Gauthier, S. (2007). Diagnostic procedures for Parkinson’s disease dementia: recommendations from the movement disorder society task force. Movement Disorders, 22(16), 2314–2324.CrossRefGoogle ScholarPubMed
Dubois, B., Feldman, H.H., Jacova, C., DeKosky, S.T., Barberger-Gateau, P., Cummings, J., & Jicha, G. (2007). Research criteria for the diagnosis of Alzheimer’s disease: revising the NINCDS–ADRDA criteria. The Lancet Neurology, 6(8), 734–746.CrossRefGoogle Scholar
Dujardin, K., Defebvre, L., Grunberg, C., Becquet, E., & Destée, A. (2001). Memory and executive function in sporadic and familial Parkinson’s disease. Brain, 124(2), 389–398.CrossRefGoogle ScholarPubMed
Economou, A., Routsis, C., & Papageorgiou, S.G. (2016). Episodic memory in Alzheimer disease, frontotemporal dementia, and dementia with Lewy bodies/Parkinson disease dementia: disentangling retrieval from consolidation. Alzheimer Disease & Associated Disorders, 30(1), 47–52.CrossRefGoogle ScholarPubMed
Fombuena, N.G. (2008). Normalización y validación de un test de memoria en envejecimiento normal, deterioro cognitivo leve y enfermedad de Alzheimer. Universitat Ramon Llull.Google Scholar
Foo, H., Mak, E., Chander, R.J., Ng, A., Au, W.L., Sitoh, Y.Y., & Kandiah, N. (2016). Associations of hippocampal subfields in the progression of cognitive decline related to Parkinson’s disease. NeuroImage: Clinical, 14, 37–42. https://doi.org/10.1016/j.nicl.2016.12.008 CrossRefGoogle ScholarPubMed
Forsaa, E.B., Larsen, J.P., Wentzel-Larsen, T., & Alves, G. (2010). What predicts mortality in Parkinson disease? A prospective population-based long-term study. Neurology, 75(14), 1270–1276.CrossRefGoogle ScholarPubMed
Goverover, Y., Chiaravalloti, N., Genova, H., & DeLuca, J. (2018). A randomized controlled trial to treat impaired learning and memory in multiple sclerosis: the self-GEN trial. Multiple Sclerosis Journal, 24(8), 1096–1104. https://doi.org/10.1016/S1474-4422(10)70212-X CrossRefGoogle ScholarPubMed
Grober, E., Lipton, R.B., Hall, C., & Crystal, H. (2000). Memory impairment on free and cued selective reminding predicts dementia. Neurology, 54(4), 827–832. https://doi.org/10.1212/WNL.54.4.827 CrossRefGoogle ScholarPubMed
Higginson, C.I., King, D.S., Levine, D., Wheelock, V.L., Khamphay, N.O., & Sigvardt, K.A. (2003). The relationship between executive function and verbal memory in Parkinson’s disease. Brain and Cognition, 52(3), 343–352. https://doi.org/10.1016/S0278-2626(03)00180-5 CrossRefGoogle ScholarPubMed
Higginson, C.I., Wheelock, V.L., Carroll, K.E., & Sigvardt, K.A. (2005). Recognition memory in Parkinson’s disease with and without dementia: evidence inconsistent with the retrieval deficit hypothesis. Journal of Clinical and Experimental Neuropsychology, 27(4), 516–528. https://doi.org/10.1080/13803390490515469 CrossRefGoogle ScholarPubMed
Hoogland, J., Boel, J.A., de Bie, R.M.A., Geskus, R.B., Schmand, B.A., Dalrymple-Alford, J.C., & Geurtsen, G.J. (2017). Mild cognitive impairment as a risk factor for Parkinson’s disease dementia. Movement Disorders, 32(7), 1056–1065. https://doi.org/10.1002/mds.27002 CrossRefGoogle ScholarPubMed
Ibarretxe-Bilbao, N., Zarei, M., Junque, C., Marti, M.J., Segura, B., Vendrell, P., & Tolosa, E. (2011). Dysfunctions of cerebral networks precede recognition memory deficits in early Parkinson’s disease. NeuroImage, 57(2), 589–597. https://doi.org/10.1016/j.neuroimage.2011.04.049 CrossRefGoogle ScholarPubMed
Ivory, S.-J., Knight, R., Longmore, B., & Caradoc-Davies, T. (1999). Verbal memory in non-demented patients withidiopathic Parkinsons disease. Neuropsychologia, 37(7), 817–828. https://doi.org/10.1016/S0028-3932(98)00131-6 CrossRefGoogle Scholar
Junqué, C., Ramírez-Ruiz, B., Tolosa, E., Summerfield, C., Martí, M.J., Pastor, P., & Mercader, J.M. (2005). Amygdalar and hippocampal MRI volumetric reductions in Parkinson’s disease with dementia. Movement Disorders, 20(5), 540–544. https://doi.org/10.1002/mds.20371 CrossRefGoogle ScholarPubMed
Kudlicka, A., Clare, L., & Hindle, J.V. (2011). Executive functions in Parkinson’s disease: systematic review and meta-analysis. Movement Disorders, 26(13), 2305–2315. https://doi.org/10.1002/mds.23868 CrossRefGoogle ScholarPubMed
Lemos, R., Duro, D., Simões, M.R., & Santana, I. (2014). Longitudinal studies should be performed to verify the sensitivity of above paradigm in predicting dementia in PDaMCI patient. Archives of Clinical Neuropsychology, 29(7), 670–679. https://doi.org/10.1093/arclin/acu031 CrossRefGoogle Scholar
Leroi, I., McDonald, K., Pantula, H., & Harbishettar, V. (2012). Cognitive impairment in Parkinson disease: impact on quality of life, disability, and caregiver burden. Journal of Geriatric Psychiatry and Neurology, 25(4), 208–214.CrossRefGoogle ScholarPubMed
McKinlay, A., 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. https://doi.org/10.1017/S1355617709991299 CrossRefGoogle ScholarPubMed
Miyake, A., Friedman, N.P., Emerson, M.J., Witzki, A.H., Howerter, A., & Wager, T.D. (2000). The unity and diversity of executive functions and their contributions to complex “Frontal Lobe” tasks: a latent variable analysis. Cognitive psychology, 41(1), 49–100. https://doi.org/10.1006/cogp.1999.0734 CrossRefGoogle ScholarPubMed
Monchi, O., Hanganu, A., & Bellec, P. (2016). Markers of cognitive decline in PD: the case for heterogeneity. Parkinsonism and Related Disorders, 24, 8–14. https://doi.org/10.1016/j.parkreldis.2016.01.002 CrossRefGoogle ScholarPubMed
Nasreddine, Z.S., Phillips, N.A., Bédirian, 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), 695–699.CrossRefGoogle ScholarPubMed
Novellino, F., Vasta, R., Sarica, A., Chiriaco, C., Salsone, M., Morelli, M., & Quattrone, A. (2018). Relationship between hippocampal subfields and category cued recall in AD and PDD: a multimodal MRI study. Neuroscience, 371, 506–517. https://doi.org/10.1016/j.neuroscience.2017.12.028 CrossRefGoogle ScholarPubMed
Oltra-Cucarella, J., Delgado, S., Duque, P., Pérez-Vicente, J.A., & Cabello-Rodríguez, L. (2018). Encoding deficits in low-educated individuals with non-amnestic mild cognitive impairment. Analysis of memory processes using the item specific deficit approach. Psychiatry Research, 268(June), 211–216. https://doi.org/10.1016/j.psychres.2018.07.026 CrossRefGoogle ScholarPubMed
Oltra-Cucarella, J., Pérez-Elvira, R., & Duque, P. (2014). Benefits of deep encoding in Alzheimer’s disease. Analysis of performance in a memory task using the item specific deficit approach. Neurología (English Edition), 29(5), 286–293. https://doi.org/10.1016/j.nrleng.2013.06.002 CrossRefGoogle Scholar
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(6), 1727–1751.CrossRefGoogle ScholarPubMed
Pascual-Leone, A., Press, D., Papagno, C., & Trojano, L. (2018). Cognitive and behavioral disorders in Parkinson disease. Neurological Sciences, 39(2), 215–223. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/10528330 Google Scholar
Pillon, B., Deweer, B., Agid, Y., & Dubois, B. (1993). Explicit memory in Alzheimer’s, Huntington’s, and Parkinson’s diseases. Archives of neurology, 50(4), 374–379. https://doi.org/10.1001/archneur.1993.00540040036010 CrossRefGoogle ScholarPubMed
Pirogovsky-Turk, E., Filoteo, J.V., Litvan, I., & Harrington, D.L. (2015). Structural MRI correlates of episodic memory processes in Parkinson’s disease without mild cognitive impairment. Journal of Parkinson’s Disease, 5(4), 971–981.CrossRefGoogle ScholarPubMed
Recio, L.A., Martín, P., Carvajal, F., Ruiz, M., & Serrano, J.M. (2013). A holistic analysis of relationships between executive function and memory in Parkinson’s disease. Journal of Clinical and Experimental Neuropsychology, 35(2), 147–159. https://doi.org/10.1080/13803395.2012.758240 CrossRefGoogle Scholar
Rodríguez-Ferreiro, J., Cuetos, F., Herrera, E., Menéndez, M., & Ribacoba, R. (2010). Cognitive impairment in Parkinson’s disease without dementia. Movement Disorders, 25(13), 2136–2141. https://doi.org/10.1002/mds.23239 CrossRefGoogle ScholarPubMed
Sahakian, B.J., Morris, R.G., Evenden, J.L., Heald, A., Levy, R., Philpot, M., & Robbins, T.W. (1988). A comparative study of visuospatial memory and learning in Alzheimer-type dementia and Parkinson’s disease. Brain, 111(3), 695–718.CrossRefGoogle ScholarPubMed
Saka, E., & Elibol, B. (2009). Enhanced cued recall and clock drawing test performances differ in Parkinson’s and Alzheimer’s disease-related cognitive dysfunction. Parkinsonism & Related Disorders, 15(9), 688–691. https://doi.org/10.1016/j.parkreldis.2009.04.008 CrossRefGoogle ScholarPubMed
Stebbins, G.T., Gabrieli, J.D.E., Masciari, F., Monti, L., & Goetz, C.G. (1999). Delayed recognition memory in Parkinsons disease: a role for working memory? Neuropsychologia, 37(4), 503–510.CrossRefGoogle ScholarPubMed
Swick, D., & Knight, R.T. (1996). Is prefrontal cortex involved in cued recall? A neuropsychological test of PET findings. Neuropsychologia, 34(10), 1019–1028. https://doi.org/10.1016/0028-3932(96)00011-5 CrossRefGoogle ScholarPubMed
Szeto, J.Y.Y., Mowszowski, L., Gilat, M., Walton, C.C., Naismith, S.L., & Lewis, S.J.G. (2016). Mild cognitive impairment in Parkinson’s disease: impact on caregiver outcomes. Journal of Parkinson’s Disease, 6(3), 589–596.CrossRefGoogle ScholarPubMed
Tanner, J.J., Mareci, T.H., Okun, M.S., Bowers, D., Libon, D.J., & Price, C.C. (2015). Temporal lobe and frontal-subcortical dissociations in non-demented Parkinson’s disease with verbal memory impairment. PLOS One, 10(7), e0133792.CrossRefGoogle ScholarPubMed
Teichmann, M., Epelbaum, S., Samri, D., Levy Nogueira, M., Michon, A., Hampel, H., & Dubois, B. (2017). Free and cued selective reminding test—accuracy for the differential diagnosis of Alzheimer’s and neurodegenerative diseases: a large-scale biomarker-characterized monocenter cohort study (ClinAD). Alzheimer’s & Dementia, 13(8), 913–923. https://doi.org/10.1016/J.JALZ.2016.12.014 CrossRefGoogle Scholar
Weintraub, D., Doshi, J., Koka, D., Davatzikos, C., Siderowf, A.D., Duda, J.E., & Clark, C.M. (2011). Neurodegeneration across stages of cognitive decline in Parkinson disease. Archives of Neurology, 68(12), 1562–1568. https://doi.org/10.1001/archneurol.2011.725 CrossRefGoogle ScholarPubMed
Whittington, C., Podd, J., & Stewart-Williams, S. (2006). Memory deficits in Parkinson’s disease. Journal of Clinical and Experimental Neuropsychology, 28(5), 738–754. https://doi.org/10.1080/13803390590954236 CrossRefGoogle ScholarPubMed
Woods, S.P., & Tröster, A.I. (2003). Prodromal frontal/executive dysfunction predicts incident dementia in Parkinson’s disease. Journal of the International Neuropsychological Society, 9(1), 17–24.CrossRefGoogle ScholarPubMed
Wright, M.J., Schmitter-Edgecombe, M., & Woo, E. (2010). Verbal memory impairment in severe closed head injury: the role of encoding and consolidation. Journal of Clinical and Experimental Neuropsychology, 32(7), 728–736. https://doi.org/10.1080/13803390903512652 CrossRefGoogle ScholarPubMed
Wright, M.J., Woo, E., Schmitter-Edgecombe, M., Hinkin, C.H., Miller, E.N., & Gooding, A.L. (2009). The item-specific deficit approach to evaluating verbal memory dysfunction: rationale, psychometrics, and application. Journal of Clinical and Experimental Neuropsychology, 31(7), 790–802. https://doi.org/10.1080/13803390802508918 CrossRefGoogle ScholarPubMed
Yarnall, A.J., Breen, D.P., Duncan, G.W., Khoo, T.K., Coleman, S.Y., Firbank, M.J., & Rowe, J.B. (2014). Characterizing mild cognitive impairment in incident Parkinson disease: the ICICLE-PD study. Neurology, 82(4), 308–316.CrossRefGoogle ScholarPubMed