Hostname: page-component-848d4c4894-2pzkn Total loading time: 0 Render date: 2024-06-11T19:58:45.984Z Has data issue: false hasContentIssue false
  • English
  • Français

Disruption of the serial position effect as an early marker of Alzheimer’s disease in Spanish–English bilinguals

Published online by Cambridge University Press:  21 June 2023

Reina Mizrahi Open the ORCID record for Reina Mizrahi [Opens in a new window] ,
Oona Cromheecke ,
David P. Salmon  and
Tamar H. Gollan Open the ORCID record for Tamar H. Gollan [Opens in a new window]
Reina Mizrahi*
Affiliation:
Department of Cognitive Science, University of California, San Diego, CA, USA
Oona Cromheecke
Affiliation:
Department of Rehabilitation Sciences, Ghent University, Ghent, Belgium
David P. Salmon
Affiliation:
Department of Neurosciences, University of California, San Diego, CA, USA
Tamar H. Gollan
Affiliation:
Department of Psychiatry, University of California, San Diego, CA, USA
*
Corresponding author: Reina Mizrahi; Email: rmizrahi@ucsd.edu
Get access Rights & Permissions [Opens in a new window]

Abstract

Objectives:

The present study examined if disruption of serial position effects in list recall could serve as an early marker of Alzheimer’s disease (AD) in Spanish–English bilinguals.

Methods:

We tested 20 participants initially diagnosed as cognitively normal or with mild cognitive impairment who declined and eventually received a diagnosis of AD (decliners), and 37 who remained cognitively stable (controls) over at least 2 years. Participants were tested on the Consortium to Establish a Registry for Alzheimer’s Disease (CERAD) Word List Learning Test in English or Spanish as part of an annual neuropsychological evaluation.

Results:

Compared to controls, decliners exhibited significantly reduced recall including reduced primacy scores (i.e., items recalled from the first three list items on Trial 1), whereas recency scores (i.e., items recalled from the last 3 list items on Trial 1) were equivalent in decliners and controls. Further analyses suggested that the sensitivity of the primacy effect to preclinical AD was initially stronger in participants tested in Spanish, a surprising finding given that the CERAD was developed for English speakers. However, in the subsequent year of testing, primacy scores declined to the same level regardless of language of testing.

Conclusions:

Several list learning measures may facilitate early diagnosis of AD in Spanish–English bilinguals, possibly including the relatively understudied primacy effect. Additional studies are needed to investigate the possibility that linguistic or demographic variables might modulate sensitivity of list learning tests to preclinical AD, which could lead to broader improvements in their utility for early diagnosis of AD in all populations.

Keywords

Alzheimer’s diseaseBilingualismSerial position effectsPrimacy effectsList memoryNeuropsychological tests
Type
Research Article
Information
Journal of the International Neuropsychological Society , Volume 30 , Issue 2 , February 2024 , pp. 162 - 171
Copyright
Copyright © INS. Published by Cambridge University Press 2023

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

(2022). Alzheimer’s disease facts and figures. Alzheimer’s & Dementia: the Journal of the Alzheimer’s Association, 18(4), 700–789.Google Scholar
Albert, M. S., DeKosky, S. T., Dickson, D., Dubois, B., Feldman, H. H., Fox, N. C., Gamst, A., Holtzman, D. M., Jagust, W. J., Petersen, R. C., Snyder, P. J., Carrillo, M. C., Thies, B., 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. Alzheimer’s & Dementia, 7(3), 270–279.Google Scholar
Alonso, M. A., Fernandez, A., & Díez, E. (2011). Oral frequency norms for 67,979 Spanish words. Behavior Research Methods, 43(2), 449–458.Google Scholar
Ardila, A., Rosselli, M., & Puente, A. E. (1994). Neuropsychological evaluation of the Spanish speaker. Springer Science & Business Media.CrossRefGoogle Scholar
Atkinson, R. C., & Shiffrin, R. M. (1968). Human memory: A proposed system and its control processes. In Psychology of learning and motivation (vol. vol. 2, p. 89–195). Academic Press.Google Scholar
Bayley, P. J., Salmon, D. P., Bondi, M. W., Bui, B. K., Olichney, J., Delis, D. C., Thomas, R., & Thal, L. J. (2000). Comparison of the serial position effect in very mild Alzheimer’s disease, mild Alzheimer’s disease, and amnesia associated with electroconvulsive therapy. Journal of the International Neuropsychological Society, 6(3), 290–298.Google Scholar
Belleville, S., Fouquet, C., Hudon, C., Zomahoun, H. T. V., Croteau, J., & the Consortium for the Early Identification of Alzheimer’s Disease-Quebec (2017). Neuropsychological measures that predict progression from mild cognitive impairment to Alzheimer’s type dementia in older adults: A systematic review and meta-analysis. Neuropsychology Review, 27(4), 328–353.Google Scholar
Bondi, M. W., Monsch, A. U., Galasko, D., Butters, N., Salmon, D. P., & Delis, D. C. (1994). Preclinical cognitive markers of dementia of the Alzheimer type. Neuropsychology, 8(3), 374–384.Google Scholar
Breton, J., Stickel, A. M., Tarraf, W., Gonzalez, K. A., Keamy, A. J., Schneiderman, N., Marquine, M. J., Zlatar, Z. Z., Salmon, D. P., Lamar, M., Daviglus, M. L., Lipton, R. B., Gallo, L. C., Goodman, Z. T., & González, H. M. (2021). Normative data for the Brief Spanish-English Verbal Learning Test for representative and diverse Hispanics/Latinos:Results from the Hispanic Community Health Study/Study of Latinos (HCHS/SOL). Alzheimer’s & Dementia: Diagnosis, Assessment & Disease Monitoring, 13(1), e12260.Google Scholar
Bruno, D., Grothe, M. J., Nierenberg, J., Zetterberg, H., Blennow, K., Teipel, S. J., & Pomara, N. (2015). A study on the specificity of the association between hippocampal volume and delayed primacy performance in cognitively intact elderly individuals. Neuropsychologia, 69, 1–8.Google Scholar
Brysbaert, M., & New, B. (2009). Moving beyond Kučera and Francis: A critical evaluation of current word frequency norms and the introduction of a new and improved word frequency measure for American English. Behavior Research Methods, 41(4), 977–990. https://doi.org/10.3758/BRM.41.4.977 CrossRefGoogle Scholar
Carrión-Baralt, J. R., Meléndez-Cabrero, J., Beeri, M. S., Sano, M., & Silverman, J. M. (2009). The neuropsychological performance of nondemented Puerto Rican nonagenarians. Dementia and Geriatric Cognitive Disorders, 27(4), 353–360.CrossRefGoogle ScholarPubMed
Cuetos, F., Glez-Nosti, M., Barbón, A., & Brysbaert, M. (2012). SUBTLEX-ESP: Spanish word frequencies based on film subtitles. Psicológica, 33(2), 133–143.Google Scholar
Cummings, J. L., Mega, M., Gray, K., Rosenberg-Thompson, S., Carusi, D. A., & Gornbein, J. (1994). The Neuropsychiatric Inventory: comprehensive assessment of psychopathology in dementia. Neurology, 44(12), 2308–2308.Google Scholar
Cunha, C., Guerreiro, M., de Mendonça, A., Oliveira, P. E., & Santana, I. (2012). Serial position effects in Alzheimer’s disease, mild cognitive impairment, and normal aging: Predictive value for conversion to dementia. Journal of Clinical and Experimental Neuropsychology, 34(8), 841–852.Google Scholar
Delis, D. C., Fine, E. M., Stricker, J. L., Houston, W. S., Wetter, S. R., Cobell, K., Jacobson, M. W., Salmon, D. P., Bondi, M. W. (2010). Comparison of the traditional recall-based versus a new list-based method for computing semantic clustering on the California Verbal Learning Test: Evidence from Alzheimer’s disease. The Clinical Neuropsychologist, 24(1), 70–79.Google Scholar
Delis, D. C., Kramer, J. H., Kaplan, E., & Ober, B. A. (1987). California Verbal Learning Test. Assessment.Google Scholar
Fillenbaum, G. G., Kuchibhatla, M., Henderson, V. W., Clark, C. M., & Taussig, I. M. (2007). Comparison of performance on the CERAD neuropsychological battery of Hispanic patients and cognitively normal controls at two sites. Clinical Gerontologist, 30(3), 1–22.Google Scholar
Fillenbaum, G. G., Mccurry, S. M., Kuchibhatla, M., Masaki, K. H., Borenstein, A. R., Foley, D. J., Heyman, A., Larson, E., & White, L. (2005). Performance on the CERAD neuropsychology battery of two samples of Japanese-American elders: Norms for persons with and without dementia. Journal of the International Neuropsychological Society, 11(2), 192–201.Google Scholar
Foldi, N. S., Brickman, A. M., Schaefer, L. A., & Knutelska, M. E. (2003). Distinct serial position profiles and neuropsychological measures differentiate late life depression from normal aging and Alzheimer’s disease. Psychiatry Research, 120(1), 71–84.CrossRefGoogle ScholarPubMed
Galasko, D., Hansen, L. A., Katzman, R., Wiederholt, W., Masliah, E., Terry, R., Hill, L. R., Lessin, P., & Thal, L. J. (1994). Clinical-Neuropathological correlations in Alzheimer's disease and related dementias. Archives of neurology, 51(9), 888–895.CrossRefGoogle ScholarPubMed
Gasquoine, P. G., & Gonzalez, C. D. (2012). Using monolingual neuropsychological test norms with bilingual Hispanic Americans: Application of an individual comparison standard. Archives of Clinical Neuropsychology, 27(3), 268–276.Google Scholar
Gicas, K. M., Honer, W. G., Wilson, R. S., Boyle, P. A., Leurgans, S. E., Schneider, J. A., & Bennett, D. A. (2020). Association of serial position scores on memory tests and hippocampal-related neuropathologic outcomes. Neurology, 95(24), e3303–e3312.CrossRefGoogle ScholarPubMed
Gollan, T. H., & Acenas, L.-A. R. (2004). What is a TOT? Cognate and translation effects on tip-of-the-tongue states in Spanish-English and Tagalog-English Bilinguals. Journal of Experimental Psychology: Learning, Memory, and Cognition, 30(1), 246–269. DOI: https://doi.org/10.1037/0278-7393.30.1.246 Google Scholar
Gollan, T. H., Montoya, R. I., Fennema-Notestine, C., & Morris, S. K. (2005). Bilingualism affects picture naming but not picture classification. Memory & Cognition, 33(7), 1220–1234.Google Scholar
Gollan, T. H., Salmon, D. P., Montoya, R. I., & da Pena, E. (2010). Accessibility of the nondominant language in picture naming: A counterintuitive effect of dementia on bilingual language production. Neuropsychologia, 48(5), 1356–1366.Google Scholar
Gollan, T. H., & Silverberg, N. B. (2001). Tip-of-the-tongue states in Hebrew-English bilinguals. Bilingualism: Language and Cognition, 4(1), 63–83.Google Scholar
Gollan, T. H., Weissberger, G. H., Runnqvist, E., Montoya, R. I., & Cera, C. M. (2012). Self-ratings of spoken language dominance: A Multilingual Naming Test (MINT) and preliminary norms for young and aging Spanish-English bilinguals. Bilingualism: Language and Cognition, 15(3), 594–615.Google Scholar
González, H. M., Mungas, D., & Haan, M. N. (2002). A verbal learning and memory test for English-And Spanish-Speaking older Mexican-American adults. The Clinical Neuropsychologist, 16(4), 439–451.Google Scholar
Howieson, D. B., Mattek, N., Seeyle, A. M., Dodge, H. H., Wasserman, D., Zitzelberger, T., & Jeffrey, K. (2011). Serial position effects in mild cognitive impairment. Journal of Clinical and Experimental Neuropsychology, 33(3), 292–299.Google Scholar
Ivanova, I., & Costa, A. (2008). Does bilingualism hamper lexical access in speech production? Acta Psychologica, 127(2), 277–288.Google Scholar
Judd, T., Capetillo, D., Carrion-Baralt, J., Marmol, L. M., Miguel-Montes, L. S., Navarrete, M. G., Puente, A. E., Romero, H. R., Valdes, J., and the NAN Policy and Planning Committee (2009). Professional considerations for improving the neuropsychological evaluation of Hispanics: A National Academy of Neuropsychology education paper. Archives of Clinical Neuropsychology, 24(2), 127–135.Google Scholar
Katkov, M., Romani, S., & Tsodyks, M. (2014). Word length effect in free recall of randomly assembled word lists. Frontiers in Computational Neuroscience, 8, 129.Google Scholar
Kloth, N., Lemke, J., Wiendl, H., Meuth, S. G., Duning, T., & Johnen, A. (2020). Serial position effects rapidly distinguish Alzheimer’s from frontotemporal dementia. Journal of Neurology, 267(4), 975–983. DOI: https://doi.org/10.1007/s00415-019-09662-w Google Scholar
Kroll, J. F., & Gollan, T. H. (2013). Speech planning in two languages. In The Oxford Handbook of Language Production Google Scholar
Loewenstein, D. A., Curiel, R. E., Greig, M. T., Bauer, R. M., Rosado, M., Bowers, D., Wicklund, M., Crocco, E., Pontecorvo, M., Joshi, A. D., Rodriguez, R., Barker, W. W., Hidalgo, J., Duara, R. (2016). A novel cognitive stress test for the detection of preclinical Alzheimer disease: Discriminative properties and relation to amyloid load. The American Journal of Geriatric Psychiatry, 24(10), 804–813.Google Scholar
McKhann, G. M., Albert, M. S., & Sperling, R. A. (2012). Changing diagnostic concepts of Alzheimer’s disease. In Alzheimer’s disease-modernizing concept, biological diagnosis and therapy. vol. 28, p. 115–121). Karger Publishers.Google Scholar
Moms, J. C., Heyman, A., Mohs, R. C., Hughes, J. P., van Belle, G., Fillenbaum, G., Mellits, E. D., & Clark, C. (1989). The Consortium to Establish a Registry for Alzheimer’s Disease (CERAD). Part I. Clinical and neuropsychological assessment of Alzheimer’s disease. Neurology, 39(9), 1159–1159.CrossRefGoogle Scholar
Morris, J. C., Heyman, A., Mohs, R. C., Hughes, J. P., van Belle, G., Fillenbaum, G., Mellits, E. D., & Clark, C. (1989). The consortium to establish a registry for Alzheimer’s disease (CERAD). Part I. Clinical and neuropsychological assessment of Alzheimer’s disease. Neurology, 39, 1159–1165.Google Scholar
Moser, B., Deisenhammer, E. A., Marksteiner, J., Papousek, I., Fink, A., & Weiss, E. M. (2014). Serial position effects in patients with mild cognitive impairment and early and moderate Alzheimer’s disease compared with healthy comparison subjects. Dementia and Geriatric Cognitive Disorders, 37(1-2), 19–26.CrossRefGoogle ScholarPubMed
Novak, K., & Riggs, J. A. (2004). Hispanics/Latinos and Alzheimer’s disease. Alzheimer’s Association.Google Scholar
O’Bryant, S. E., Edwards, M., Johnson, L., Hall, J., Gamboa, A., & O’jile, J. (2018). Texas Mexican American adult normative studies: Normative data for commonly used clinical neuropsychological measures for English-and Spanish-speakers. Developmental neuropsychology, 43(1), 1–26.Google Scholar
Ostrosky-Solís, F., Ardila, A., & Rosselli, M. (1999). NEUROPSI: A brief neuropsychological test battery in Spanish with norms by age and educational level. Journal of the International Neuropsychological Society, 5(5), 413–433.CrossRefGoogle ScholarPubMed
Pedraza, O., & Mungas, D. (2008). Measurement in cross-cultural neuropsychology. Neuropsychology Review, 18(3), 184–193.Google Scholar
Peña, E. D. (2007). Lost in translation: Methodological considerations in cross-cultural research. Child Development, 78(4), 1255–1264.Google Scholar
Restrepo, M. A., & Silverman, S. W. (2001). Validity of the Spanish Preschool Language Scale – 3 for use with bilingual children. American Journal of Speech-Language Pathology, 10(4), 382–393.Google Scholar
Roberts, P. M., Garcia, L. J., Desrochers, A., & Hernandez, D. (2002). English performance of proficient bilingual adults on the Boston Naming Test. Aphasiology, 16(4-6), 635–645.Google Scholar
Rosselli, M., Loewenstein, D. A., Curiel, R. E., Penate, A., Torres, V. L., Lang, M., Greig, M. T., Barker, W. W., Duara, R. (2019). Effects of bilingualism on verbal and nonverbal memory measures in mild cognitive impairment. Journal of the International Neuropsychological Society, 25(1), 15–28.Google Scholar
Siedlecki, K. L., Manly, J. J., Brickman, A. M., Schupf, N., Tang, M. X., & Stern, Y. (2010). Do neuropsychological tests have the same meaning in Spanish speakers as they do in English speakers? Neuropsychology, 24(3), 402–411.Google Scholar
Sperling, R. A., Aisen, P. S., Beckett, L. A., Bennett, D. A., Craft, S., Fagan, A. M., Iwatsubo, T., Jack, C. R. Jr., Kaye, J., Montine, T. J., Park, D. C., Reiman, E. M., Rowe, C. C., Siemers, E., Stern, Y., Yaffe, K., Carrillo, M. C., Thies, B., Morrison‐Bogorad, M., Wagster, M. V., Phelps, C. H. (2011). Toward defining the preclinical stages of Alzheimer’s disease: Recommendations from the National Institute on Aging-Alzheimer’s Association workgroups on diagnostic guidelines for Alzheimer’s disease. Alzheimer’s & dementia, 7(3), 280–292.Google Scholar
Twamley, E. W., Ropacki, S. A. L., & Bondi, M. W. (2006). Neuropsychological and neuroimaging changes in preclinical Alzheimer’s disease. Journal of the International Neuropsychological Society, 12(5), 707–735.Google Scholar
US Census Bureau (2004). American factfinder (Vol. 3). US Department of Commerce, Economics and Statistics Administration, US Census Bureau.Google Scholar
Ward, G., Tan, L., & Grenfell-Essam, R. (2010). Examining the relationship between free recall and immediate serial recall: The effects of list length and output order. Journal of Experimental Psychology: Learning, Memory, and Cognition, 36(5), 1207–41.Google Scholar
Weissberger, G. H., Salmon, D. P., Bondi, M. W., & Gollan, T. H. (2013). Which neuropsychological tests predict progression to Alzheimer’s disease in Hispanics? Neuropsychology, 27(3), 343–355.Google Scholar
Weissberger, G. H., Strong, J. V., Stefanidis, K. B., Summers, M. J., Bondi, M. W., & Stricker, N. H. (2017). Diagnostic accuracy of memory measures in Alzheimer’s dementia and mild cognitive impairment: A systematic review and meta-analysis. Neuropsychology Review, 27(4), 354–388.Google Scholar
Welsh, K. A., Butters, N., Mohs, R. C., Beekly, D., Edland, S., Fillenbaum, G., & Heyman, A. (1994). The Consortium to Establish a Registry for Alzheimer’s Disease (CERAD). Part V. A normative study of the neuropsychological battery. Neurology, 44(4), 609–609.Google Scholar