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Investigating Associative Learning Effects in Patients with Prodromal Alzheimer’s Disease Using the Temporal Context Model

Published online by Cambridge University Press:  28 September 2015

Lisa Quenon ,
Jean-Jacques Orban de Xivry ,
Bernard Hanseeuw  and
Adrian Ivanoiu
Lisa Quenon*
Affiliation:
Institute of Neuroscience, Université Catholique de Louvain, Brussels, Belgium
Jean-Jacques Orban de Xivry
Affiliation:
Institute of Neuroscience, Université Catholique de Louvain, Brussels, Belgium Institute of Information and Communication Technologies, Electronics and Applied Mathematics, Université Catholique de Louvain, Louvain-la-Neuve, Belgium Department of Kinesiology, Movement Control and Neuroplasticity Research Group, K.U. Leuven, Leuven, Belgium
Bernard Hanseeuw
Affiliation:
Institute of Neuroscience, Université Catholique de Louvain, Brussels, Belgium Neurology Department, Cliniques universitaires Saint-Luc, Brussels, Belgium
Adrian Ivanoiu
Affiliation:
Institute of Neuroscience, Université Catholique de Louvain, Brussels, Belgium Neurology Department, Cliniques universitaires Saint-Luc, Brussels, Belgium
*
Correspondence and reprint requests to: Lisa Quenon, Clinique universitaires Saint-Luc, Centre de Revalidation Neuropsychologique, Avenue Hippocrate 10, 1200 Woluwe-Saint-Lambert, Belgium. E-mail: lisa.quenon@uclouvain.be
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Abstract

The purpose of this study was to investigate associative learning effects in patients with prodromal Alzheimer’s disease (prAD) by referring to the Temporal Context Model (TCM; Howard, Jing, Rao, Provyn, & Datey, 2009), in an attempt to enhance the understanding of their associative memory impairment. TCM explains fundamental effects described in classical free-recall tasks and cued-recall tasks involving overlapping word pairs (e.g., A-B, B-C), namely (1) the contiguity effect, which is the tendency to successively recall nearby items in a list, and (2) the observation of backward (i.e., B-A) and transitive associations (i.e., A-C) between items. In TCM, these effects are hypothesized to rely on contextual representation, binding and retrieval processes, which supposedly depend on hippocampal and parahippocampal regions. As these regions are affected in prAD, the current study investigated whether prAD patients would show reduced proportions of backward and transitive associations in free and cued-recall, coupled to a reduced contiguity effect in free-recall. Seventeen older controls and 17 prAD patients performed a cued-recall task involving overlapping word pairs and a final free-recall task. Proportions of backward and transitive intrusions in cued-recall did not significantly differ between groups. However, in free-recall, prAD patients demonstrated a reduced contiguity effect as well as reduced proportions of backward and transitive associations compared to older controls. These findings are discussed within the hypothesis that the contextual representation, binding and/or retrieval processes are affected in prAD patients compared to healthy older individuals. (JINS, 2015, 21, 699–708)

Keywords

Memory impairmentAssociative memoryContiguity effectContextual bindingRecall transitionsProdromal Alzheimer’s disease
Type
Research Articles
Information
Journal of the International Neuropsychological Society , Volume 21 , Issue 9 , October 2015 , pp. 699 - 708
Copyright
Copyright © The International Neuropsychological Society 2015 

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References

Albert, M.S., DeKosky, S.T., Dickson, D., Dubois, B., Feldman, H.H., Fox, N.C., & Phelps, C.H. (2011). The diagnosis of mild cognitive impairment due to Alzheimer’s disease: Recommendations from the National Institute on Aging-Alzheimer’s Association workgroups on diagnostic guidelines for Alzheimer’s disease. Alzheimers & Dementia, 7(3), 270–279. doi:10.1016/j.jalz.2011.03.008 Google Scholar
American Psychiatric Association (2000). Diagnostic and statistical manual of mental disorders: DSM-IV-TR (4th ed.). Washington, DC: American Psychiatric Association.Google Scholar
Atienza, M., Atalaia-Silva, K.C., Gonzalez-Escamilla, G., Gil-Neciga, E., Suarez-Gonzalez, A., & Cantero, J.L. (2011). Associative memory deficits in mild cognitive impairment: The role of hippocampal formation. Neuroimage, 57(4), 1331–1342. doi:10.1016/j.neuroimage.2011.05.047 CrossRefGoogle ScholarPubMed
Bianconi, C., & Busigny, T. (Personal communication), Les Séries Graphiques: Cahier d’utilisation. Louvain-la-Neuve: Université catholique de Louvain.Google Scholar
Cardebat, D., Doyon, B., Puel, M., Goulet, P., & Joanette, Y. (1990). [Formal and semantic lexical evocation in normal subjects. Performance and dynamics of production as a function of sex, age and educational level]. Acta Neurologica Belgica, 90(4), 207–217.Google ScholarPubMed
Content, A., Mousty, P., & Radeaux, M. (1990). BRULEX: Une base de données lexicales informatisée pour le français écrit et parlé. L’année Psychologique, 90, 551–566.Google Scholar
Davachi, L., & Wagner, A.D. (2002). Hippocampal contributions to episodic encoding: Insights from relational and item-based learning. Journal of Neurophysiology, 88(2), 982–990.Google Scholar
de Partz, M.P., Bilocq, V., De Wilde, V., Seron, X., & Pillon, A. (2001). LEXIS: Tests pour l’évaluation des troubles lexicaux chez la personne aphasique. Marseille: Solal.Google Scholar
Dickerson, B.C., Goncharova, I., Sullivan, M.P., Forchetti, C., Wilson, R.S., Bennett, D.A., & deToledo-Morrell, L. (2001). MRI-derived entorhinal and hippocampal atrophy in incipient and very mild Alzheimer’s disease. [Research Support, U.S. Gov’t, P.H.S.], Neurobiology of Aging, 22(5), 747–754.Google Scholar
Dickerson, B.C., Salat, D.H., Bates, J.F., Atiya, M., Killiany, R.J., Greve, D.N., & Sperling, R.A. (2004). Medial temporal lobe function and structure in mild cognitive impairment. [Research Support, Non-U.S. Gov’t Research Support, U.S. Gov’t, P.H.S.]. Annals of Neurology, 56(1), 27–35. doi:10.1002/ana.20163 Google Scholar
Dubois, B., Feldman, H.H., Jacova, C., Dekosky, S.T., Barberger-Gateau, P., Cummings, J., & Scheltens, P. (2007). Research criteria for the diagnosis of Alzheimer’s disease: Revising the NINCDS-ADRDA criteria. [Research Support, Non-U.S. Gov’t Review]. Lancet Neurology, 6(8), 734–746. doi:10.1016/S1474-4422(07)70178-3 Google 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. Journal of Psychiatric Research, 12(3), 189–198.Google Scholar
Giovanello, K.S., Schnyer, D.M., & Verfaellie, M. (2004). A critical role for the anterior hippocampus in relational memory: Evidence from an fMRI study comparing associative and item recognition. Hippocampus, 14(1), 5–8. doi:10.1002/hipo.10182 CrossRefGoogle ScholarPubMed
Golomb, J.D., Peelle, J.E., Addis, K.M., Kahana, M.J., & Wingfield, A. (2008). Effects of adult aging on utilization of temporal and semantic associations during free and serial recall. Memory & Cognition, 36(5), 947–956.Google Scholar
Hampstead, B.M., Stringer, A.Y., Stilla, R.F., Amaraneni, A., & Sathian, K. (2011). Where did I put that? Patients with amnestic mild cognitive impairment demonstrate widespread reductions in activity during the encoding of ecologically relevant object-location associations. Neuropsychologia, 49(9), 2349–2361. doi:10.1016/j.neuropsychologia.2011.04.008 Google Scholar
Hanseeuw, B., Dricot, L., Kavec, M., Grandin, C., Seron, X., & Ivanoiu, A. (2011). Associative encoding deficits in amnestic mild cognitive impairment: A volumetric and functional MRI study. Neuroimage, 56(3), 1743–1748. doi:10.1016/j.neuroimage.2011.03.034 Google Scholar
Howard, M.W., Addis, K.M., Jing, B., & Kahana, M.J. (2007). Semantic structure of episodic memory. Handbook of Latent Semantic Analysis, 121–142.Google Scholar
Howard, M.W., Fotedar, M.S., Datey, A.V., & Hasselmo, M.E. (2005). The temporal context model in spatial navigation and relational learning: Toward a common explanation of medial temporal lobe function across domains. Psychology Review, 112(1), 75–116. doi:10.1037/0033-295X.112.1.75 Google Scholar
Howard, M.W., Jing, B., Rao, V.A., Provyn, J.P., & Datey, A.V. (2009). Bridging the gap: Transitive associations between items presented in similar temporal contexts. Journal of Expimental Psychology. Learning, Memory, and Cognition, 35(2), 391–407. doi:10.1037/a0015002 Google Scholar
Howard, M.W., & Kahana, M.J. (1999). Contextual variability and serial position effects in free recall. Journal of Expimental Psychology. Learning, Memory, and Cognition, 25(4), 923–941.Google Scholar
Howard, M.W., & Kahana, M.J. (2002). A distributed representation of temporal context. Journal of Mathematical Psychology, 46, 269–299.Google Scholar
Howard, M.W., Kahana, M.J., & Wingfield, A. (2006). Aging and contextual binding: Modeling recency and lag recency effects with the temporal context model. Psychonomic Bulletin & Review, 13(3), 439–445.Google Scholar
Ivanoiu, A., Dricot, L., Gilis, N., Grandin, C., Lhommel, R., Quenon, L., & Hanseeuw, B. (2015). Classification of non-demented patients attending a memory clinic using the new diagnostic criteria for Alzheimer’s disease with disease-related biomarkers. Journal of Alzheimers Disease, 43(3), 835–847. doi:10.3233/JAD-140651 CrossRefGoogle ScholarPubMed
Kahana, M.J. (1996). Associative retrieval processes in free recall. Memory & Cognition, 24(1), 103–109.CrossRefGoogle ScholarPubMed
Kahana, M.J., Howard, M.W., Zaromb, F., & Wingfield, A. (2002). Age dissociates recency and lag recency effects in free recall. Journal of Expimental Psychology. Learning, Memory, and Cognition, 28(3), 530–540.Google Scholar
Morris, J.C., Mohs, R.C., Rogers, H., Fillenbaum, G., & Heyman, A. (1988). Consortium to establish a registry for Alzheimer’s disease (CERAD) clinical and neuropsychological assessment of Alzheimer’s disease. [Research Support, U.S. Gov’t, P.H.S.], Psychopharmacology Bulletin, 24(4), 641–652.Google ScholarPubMed
Naveh-Benjamin, M. (2000). Adult age differences in memory performance: Tests of an associative deficit hypothesis. Journal of Expimental Psychology. Learning, Memory, and Cognition, 26(5), 1170–1187.Google Scholar
New, B., Pallier, C., Ferrand, L., & Matos, R. (2001). Une base de données lexicales du français contemporain sur internet: Lexique. L’Année Psychologique, 101, 447–462.Google Scholar
Provyn, J.P., Sliwinski, M.J., & Howard, M.W. (2007). Effects of age on contextually mediated associations in paired associate learning. [Research Support, N.I.H., Extramural], Psychology and Aging, 22(4), 846–857. doi:10.1037/0882-7974.22.4.846 Google Scholar
Reitan, R.M. (1955). The relation of the trail making test to organic brain damage. Journal of Consulting Psychology, 19(5), 393–394.Google Scholar
Ries, M.L., Carlsson, C.M., Rowley, H.A., Sager, M.A., Gleason, C.E., Asthana, S., & Johnson, S.C. (2008). Magnetic resonance imaging characterization of brain structure and function in mild cognitive impairment: A review. [Research Support, N.I.H., Extramural Review], Journal of the American Geriatric Society, 56(5), 920–934. doi:10.1111/j.1532-5415.2008.01684.x Google Scholar
Rouleau, I., Salmon, D.P., Butters, N., Kennedy, C., & McGuire, K. (1992). Quantitative and qualitative analyses of clock drawings in Alzheimer’s and Huntington’s disease. Brain and Cognition, 18(1), 70–87.Google Scholar
Sederberg, P.B., Howard, M.W., & Kahana, M.J. (2008). A context-based theory of recency and contiguity in free recall. Psychology Review, 115(4), 893–912. doi:10.1037/a0013396 Google Scholar
Sperling, R. (2007). Functional MRI studies of associative encoding in normal aging, mild cognitive impairment, and Alzheimer’s disease. Annals of the New York Academy of Sciences, 1097, 146–155. doi:10.1196/annals.1379.009 Google Scholar
Troyer, A.K., Murphy, K.J., Anderson, N.D., Craik, F.I., Moscovitch, M., Maione, A., & Gao, F. (2012). Associative recognition in mild cognitive impairment: Relationship to hippocampal volume and apolipoprotein E. Neuropsychologia, 50(14), 3721–3728. doi:10.1016/j.neuropsychologia.2012.10.018 Google Scholar
Troyer, A.K., Murphy, K.J., Anderson, N.D., Hayman-Abello, B.A., Craik, F.I., & Moscovitch, M. (2008). Item and associative memory in amnestic mild cognitive impairment: Performance on standardized memory tests. Neuropsychology, 22(1), 10–16. doi:10.1037/0894-4105.22.1.10 Google Scholar
van der Linden, M., Coyette, F., Poitrenaud, J., Kalafat, M., Calicis, F., & Wyns, C., GRENEM (2004). L’épreuve de rappel libre/rappel indicé à 16 items (RL/RI-16), L’évaluation des troubles de la mémoire: Présentation de quatre tests de mémoire épisodique (avec leur étalonnage). Marseille: Solal.Google Scholar