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Verbal learning in Alzheimer’s disease: Cumulative word knowledge gains across learning trials

Published online by Cambridge University Press:  01 September 2009

PAUL S. FOSTER*
Affiliation:
Psychology Department, Middle Tennessee State University, Murfreesboro, Tennessee Department of Neurology, University of Florida, Gainesville, Florida
VALERIA DRAGO
Affiliation:
Department of Neurology, University of Florida, Gainesville, Florida Oasi Institute for Research on Brain Aging and Mental Retardation, Troina, Italy
GREGORY P. CRUCIAN
Affiliation:
Psychology Department, University of Canterbury, Christchurch, New Zealand Brain Injury Rehabilitation Service, Burwood Hospital, Christchurch, New Zealand
ROBERT D. RHODES
Affiliation:
Psychology Department, Concord University, Athens, West Virginia
BRIAN V. SHENAL
Affiliation:
Mental Health Service Line, Salem VA Medical Center, Salem, Virginia
KENNETH M. HEILMAN
Affiliation:
Department of Neurology, University of Florida, Gainesville, Florida Department of Neurology, Malcom Randall VAMC, Gainesville, Florida
*
*Correspondence and reprint requests: Paul S. Foster, Psychology Department, Middle Tennessee State University, 1500 Greenland Drive, Murfreesboro, Tennessee 37132. E-mail: paul.foster@neurology.ufl.edu

Abstract

Research regarding learning in Alzheimer’s disease (AD) patients has been mixed. Learning capacity might be better indexed using a score that reflects the interaction between the learning slope and total recall, referred to as the Cumulative Word Learning (CWL) score. We compared a group of AD patients to normal participants using a traditional index of learning and the CWL score that were derived from the Hopkins Verbal Learning Test – Revised (HVLT-R). The HVLT-R is a supra-span, list-learning test containing 12 words from three semantic categories. The results indicated that the sample of AD patients performed within the average range, using the traditional learning z score. Although mild AD patients were not found to differ from controls in the traditional learning z score, a significant difference was noted for the CWL score. The moderate AD patients differed from the normal controls in both learning measures. Furthermore, unlike the traditional learning score, the CWL score was a significant predictor of overall cognitive functioning, as indexed using their Mini-Mental State Examination (MMSE) score. Thus, the CWL score might be a more sensitive indicator overall of total learning capacity and may be useful in staging Alzheimer’s disease because of increased resilience to floor effects. (JINS, 2009, 15, 730–739.)

Type
Research Articles
Copyright
Copyright © The International Neuropsychological Society 2009

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References

REFERENCES

Alessio, A., Damasceno, B.P., Camargo, C.H.P., Kobayashi, E., Guerreiro, C.A.M., & Cendes, F. (2004). Differences in memory performance and other clinical characteristics in patients with mesial temporal lobe epilepsy with and without hippocampal atrophy. Epilepsy and Behavior, 5, 2227.CrossRefGoogle ScholarPubMed
Au, A., Chan, A.S., & Chiu, H. (2003). Verbal learning in Alzheimer’s dementia. Journal of the International Neuropsychological Society, 9, 363375.CrossRefGoogle ScholarPubMed
Barr, W.B. (1997). Examining the right temporal lobe’s role in nonverbal memory. Brain and Cognition, 35, 2641.CrossRefGoogle ScholarPubMed
Barr, W.B., Chelune, G.J., Hermann, B.P., Loring, D.W., Perrine, K., Strauss, E. et al. , (1997). The use of figural reproduction tests as measures of nonverbal memory in epilepsy surgery candidates. Journal of the International Neuropsychological Society, 3, 435443.CrossRefGoogle ScholarPubMed
Barr, W., Morrison, C., Zaroff, C., & Devinsky, O. (2004). Use of the Brief Visuospatial Memory Test–Revised in neuropsychological evaluation of epilepsy surgery candidates. Epilepsy and Behavior, 5, 175179.CrossRefGoogle ScholarPubMed
Bayley, P.J., Salmon, D.P., Bondi, M.W., Bui, B.K., Olichney, J., Delis, D.C., et al. (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, 290298.CrossRefGoogle ScholarPubMed
Baxendale, S.A., van Paesschen, W., Thompson, P.J., Connelly, A., Duncan, J.S., Harkness, W.F., & Shorvon, S.D. (1998). The relationship between quantitative MRI and neuropsychological functioning in temporal lobe epilepsy. Epilepsia, 39, 158166.CrossRefGoogle ScholarPubMed
Beeson, P.M., Bayles, K.A., Rubens, A.B., & Kaszniak, A.W. (1993). Memory impairment and executive control in individuals with stroke-induced aphasia. Brain and Language, 45, 253275.CrossRefGoogle ScholarPubMed
Benedict, R.H.B., Schretlen, D., Groninger, L., & Brandt, J. (1998). Hopkins Verbal Learning Test–Revised: Normative data and analysis of inter-form and test-retest reliability. Clinical Neuropsychologist, 12, 4355.CrossRefGoogle Scholar
Bigler, E.D., Rosa, L., Schultz, F., Hall, S., & Harris, J. (1989). Rey-auditory verbal learning and Rey-Osterrieth complex figure design performance in Alzheimer’s disease and closed head injury. Journal of Clinical Psychology, 45, 277280.3.0.CO;2-M>CrossRefGoogle ScholarPubMed
Bohbot, V.D., Kalina, M., Stepankova, K., Spackova, N., Petrides, M., & Nadel, L. (1998). Spatial memory deficits in patients with lesions to the right hippocampus and to the right parahippocampal cortex. Neuropsychologia, 36, 12171238.CrossRefGoogle Scholar
Bornstein, R.A., Pakalnis, A., & Drake, M.E. (1988). Verbal and nonverbal memory and learning in patients with complex partial seizures of temporal lobe origin. Journal of Epilepsy, 1, 203208.CrossRefGoogle Scholar
Brandt, J., Corwin, J., & Krafft, L. (1992). Is verbal recognition memory really different in Huntington’s and Alzheimer’s disease? Journal of Clinical and Experimental Neuropsychology, 14, 773784.CrossRefGoogle ScholarPubMed
Chen, P., Ratcliff, G., Belle, S.H., Cauley, J.A., DeKosky, S.T., & Ganguli, M. (2000). Cognitive tests that best discriminate between presymptomatic AD and those who remain nondemented. Neurology, 55, 18471853.CrossRefGoogle ScholarPubMed
Chiaravalloti, N.D., & Glosser, G. (2001). Material-specific memory changes after anterior temporal lobectomy as predicted by the intracarotid amobarbital test. Epilepsia, 42, 902911.CrossRefGoogle ScholarPubMed
Coughlan, A.K. (1979). Effects of localized cerebral lesions and dysphasia on verbal memory. Journal of Neurology, Neurosurgery, and Psychiatry, 42, 914923.CrossRefGoogle ScholarPubMed
Degenszajin, J., Caramelli, P., Caixeta, L., Nitrini, R. (2001). Encoding process in delayed recall impairment and rate of forgetting in Alzheimer’s disease. Arquivos de Neuro-Psiquiatria, 59, 171174.CrossRefGoogle Scholar
De Jager, C.A., Hogervorst, E., Combrinck, M., & Budge, M.M. (2003). Sensitivity and specificity of neuropsychological tests for mild cognitive impairment, vascular cognitive impairment and Alzheimer’s disease. Psychological Medicine, 33, 10391050.CrossRefGoogle ScholarPubMed
Deweer, B., Ergis, A.M., Fossati, P., Pillon, B., Boller, F., Agid, Y., & Dubois, B. (1994). Explicit memory, procedural learning and lexical priming in Alzheimer’s disease. Cortex, 30, 113126.CrossRefGoogle ScholarPubMed
Estevez-Gonzalez, A., Kulisevsky, J., Boltes, A., Otermin, P., & Garcia-Sanchez, C. (2003). Rey verbal learning test is a useful tool for differential diagnosis in the preclinical phase of Alzheimer’s disease: Comparison with mild cognitive impairment and normal aging. International Journal of Geriatric Psychiatry, 18, 10211028.CrossRefGoogle ScholarPubMed
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, 189198.CrossRefGoogle Scholar
Foster, P.S., Harrison, D.W., Crucian, G.P., Drago, V., Rhodes, R.D., & Heilman, K.M. (2008). Reduced verbal learning associated with posterior temporal lobe slow wave activity. Developmental Neuropsychology, 33, 2543.CrossRefGoogle ScholarPubMed
Fox, L.S., Olin, J.T., Erblich, J., Ippen, C.G., & Schneider, L.S. (1998). Severity of cognitive impairment in Alzheimer’s disease affects list learning using the California Verbal Learning Test (CVLT). International Journal of Geriatric Psychiatry, 13, 544549.3.0.CO;2-N>CrossRefGoogle ScholarPubMed
Glosser, G., Cole, L., Khatri, U., DellaPietra, L., & Kaplan, E. (2002a). Assessing nonverbal memory with the Biber Figure Learning Test–Extended in temporal lobe epilepsy patients. Archives of Clinical Neuropsychology, 17, 2535.Google ScholarPubMed
Glosser, G., Gallo, J.L., Clark, C.M., & Grossman, M. (2002b). Memory encoding and retrieval in frontotemporal dementia and Alzheimer’s disease. Neuropsychology, 16, 190196.CrossRefGoogle ScholarPubMed
Heilman, K.M., Scholes, R.J., & Watson, R.T. (1976). Defects of immediate memory in Broca’s and conduction aphasia. Brain and Language, 3, 301308.CrossRefGoogle ScholarPubMed
Incalzi, R.A., Capparella, O., Gemma, A., Marra, C., & Carbonin, P.U. (1995). Effects of aging and of Alzheimer’s disease on verbal memory. Journal of Clinical and Experimental Neuropsychology, 17, 580589.CrossRefGoogle Scholar
Janke, A.L., de Zubicaray, G., Rose, S.E., Griffin, M., Chalk, J.B., & Galloway, G.J. (2001). 4D deformation modeling of cortical disease progression in Alzheimer’s dementia. Magnetic Resonance in Medicine, 46, 661666.CrossRefGoogle ScholarPubMed
Jones-Gotman, M., Brulot, M., McMackin, D., Cendes, F., Andermann, F., Olivier, A., et al. (1993). Word and design list learning deficits related to side of hippocampal atrophy as assessed by volumetric MRI measurements. Epilepsia, 34, 71.Google Scholar
Kaltreider, L.B., Cicerello, A.R., Lacritz, L.H., Weiner, M.F., Honig, L.S., Rosenberg, R.N., & Cullum, C.M. (2000). Comparison of the CERAD and CVLT list-learning tasks in Alzheimer’s disease. Clinical Neuropsychologist, 14, 269274.CrossRefGoogle ScholarPubMed
Kaltreider, L.B., Cullum, C.M., Lacritz, L.H., Brewer, K., & Filley, C.M. (1999). Brief recall tasks and memory assessment in Alzheimer’s disease. Applied Neuropsychology, 6, 165169.CrossRefGoogle ScholarPubMed
Kilpatrick, C., Murrie, V., Cook, M., Andrewes, D., Desmond, P., & Hopper, J. (1997). Degree of left hippocampal atrophy correlates with severity of neuropsychological deficits. Seizure, 6, 213218.CrossRefGoogle ScholarPubMed
Kim, H., Yi, S., Son, E.I., & Kim, J. (2003). Material-specific memory in temporal lobe epilepsy: Effects of seizure laterality and language dominance. Neuropsychology, 17, 5968.CrossRefGoogle ScholarPubMed
Kohler, S., Black, S.E., Sinden, M., Szekely, C., Kidron, D., Parker, J.L., et al. (1998). Memory impairments associated with hippocampal versus parahippocampal-gyrus atrophy: An MR volumetry study in Alzheimer’s disease. Neuropsychologia, 36, 901914.CrossRefGoogle Scholar
Kramer, J.H., Schuff, N., Reed, B.R., Mungas, D., Du, A.T., Rosen, H.J., et al. (2004). Hippocampal volume and retention in Alzheimer’s disease. Journal of the International Neuropsychological Society, 10, 639643.CrossRefGoogle ScholarPubMed
Kraybill, M.L., Larson, E.B., Tsuang, D.W., Teri, L., McCormick, W.C., Bowen, J.D., et al. (2005). Cognitive differences in dementia patients with autopsy-verified AD, Lewy body pathology, or both. Neurology, 64, 20692073.CrossRefGoogle ScholarPubMed
Lacritz, L.H., Cullum, C.M., Weiner, M.F., & Rosenberg, R.N. (2001). Comparison of the Hopkins Verbal Learning Test–Revised to the California Verbal Learning Test in Alzheimer’s disease. Applied Neuropsychology, 8, 180184.CrossRefGoogle Scholar
Lee, G.P., Loring, D.W., & Thompson, J.L. (1989). Construct validity of material specific memory measures following unilateral temporal lobe ablations. Psychological Assessment, 1, 192197.CrossRefGoogle Scholar
Libon, D.J., Mattson, R.E., Glosser, G., Kaplan, E., Malamut, B.L., Sands, L.P., Swenson, R., & Cloud, B.S. (1996). A nine-word dementia version of the California Verbal Learning Test. Clinical Neuropsychologist, 10, 237244.CrossRefGoogle Scholar
Lukatela, K., Malloy, P., Jenkins, M., & Cohen, R. (1998). The naming deficit in early Alzheimer’s and vascular dementia. Neuropsychology, 12, 565572.CrossRefGoogle ScholarPubMed
Majdan, A., Sziklas, V., & Jones-Gotman, M. (1996). Performance of healthy subjects and patients with resection from the anterior temporal lobe on matched tests of verbal and visuoperceptual learning. Journal of Clinical and Experimental Neuropsychology, 18, 416430.CrossRefGoogle ScholarPubMed
Martin, A., Brouwers, P., Cox, C., & Fedio, P. (1985). On the nature of the verbal memory deficit in Alzheimer’s disease. Brain and Cognition, 25, 323341.Google ScholarPubMed
McKhann, G., Drachman, D., Folstein, M., Katzman, R., Price, D., & Stadlan, E.M. (1984). Clinical diagnosis of Alzheimer’s disease: Report of the NINCDS-ADRDA Work Group under the auspices of the Department of Health and Human Services Task Force on Alzheimer’s disease. Neurology, 34, 939944.CrossRefGoogle ScholarPubMed
Mori, E., Yoneda, Y., Yamashita, H., Hirono, N., Ikeda, M., Yamadori, A. (1997). Medial temporal structures relate to memory impairment in Alzheimer’s disease: An MRI volumetric study. Journal of Neurology, Neurosurgery, and Psychiatry, 63, 214221.CrossRefGoogle ScholarPubMed
Morris, J.C., Edland, S., Clark, C., Galasko, D., Koss, E., Mohs, R., et al. (1993). The Consortium to Establish a Registry for Alzheimer’s Disease (CERAD): Part IV. Rates of cognitive change in the longitudinal assessment of probable Alzheimer’s disease. Neurology, 43, 24572465.CrossRefGoogle Scholar
Moscovitch, D.A., & McAndrews, M.P. (2002). Material-specific deficits in “remembering” in patients with unilateral temporal lobe epilepsy and excisions. Neuropsychologia, 40, 13351342.CrossRefGoogle ScholarPubMed
Moulin, C.J.A., James, N., Freeman, J.E., & Jones, R.W. (2004). Deficient acquisition and consolidation: Intertrial free recall performance in Alzheimer’s disease and mild cognitive impairment. Journal of Clinical and Experimental Neuropsychology, 26, 110.CrossRefGoogle ScholarPubMed
Nobili, F., Brugnolo, A., Calvini, P., Copello, F., De Leo, C., Girtler, N., et al. (2005). Resting SPECT-neuropsychology correlation in very mild Alzheimer’s disease. Clinical Neurophysiology, 116, 364375.CrossRefGoogle ScholarPubMed
Owen, A.M., Sahakian, B.J., Semple, J., Polkey, C.E., & Robbins, T.W. (1995). Visuo-spatial short-term recognition memory and learning after temporal lobe excisions, frontal lobe excisions or amygdalo-hippocampectomy in man. Neuropsychologia, 33, 124.CrossRefGoogle ScholarPubMed
Parslow, D.M., Morris, R.G., Fleminger, S., Rahman, Q., Abrahams, S., & Recce, M. (2005). Allocentric spatial memory in humans with hippocampal lesions. Acta Psychologica, 118, 123147.CrossRefGoogle ScholarPubMed
Pasquier, F., Grymonprez, L., Lebert, F., & Van der Linden, M. (2001). Memory impairment differs in frontotemporal dementia and Alzheimer’s disease. Neurocase, 7, 161171.CrossRefGoogle ScholarPubMed
Petersen, R.C., Smith, G.E., Ivnik, R.J., Kokmen, E., & Tangalos, E.G. (1994). Memory function in very early Alzheimer’s disease. Neurology, 44, 867872.CrossRefGoogle ScholarPubMed
Raspall, T., Donate, M., Boget, T., Carreno, M., Donaire, A., Agudo, R., et al. (2005). Neuropsychological tests with lateralizing value in patients with temporal lobe epilepsy: Reconsidering material-specific theory. Seizure, 14, 569576.CrossRefGoogle ScholarPubMed
Remy, F., Mirrashed, F., Campbell, B., & Richter, W. (2005). Verbal episodic memory impairment in Alzheimer’s disease: A combined structural and functional MRI study. NeuroImage, 25, 253266.CrossRefGoogle ScholarPubMed
Scahill, R.I., Schott, J.M., Stevens, J.M., Rossor, M.N., & Fox, N.C. (2002). Mapping the evolution of regional atrophy in Alzheimer’s disease: Unbiased analysis of fluid-registered serial MRI. Proceedings of the National Academy of Sciences, 99, 47034707.CrossRefGoogle ScholarPubMed
Shapiro, A.M., Benedict, R.H.B., Schretlen, D., & Brandt, J. (1999). Construct and concurrent validity of the Hopkins Verbal Learning Test–Revised. Clinical Neuropsychologist, 13, 348358.CrossRefGoogle ScholarPubMed
Simon, E., Leach, L., Winocur, G., & Moscovitch, M. (1994). Intact primary memory in mild to moderate Alzheimer disease: Indices from the California Verbal Learning Test. Journal of Clinical and Experimental Neuropsychology, 16, 414422.CrossRefGoogle ScholarPubMed
Smith, M.L., & Milner, B. (1981). The role of the right hippocampus in the recall of spatial location. Neuropsychologia, 19, 781793.CrossRefGoogle ScholarPubMed
Snitz, B.E., Roman, D.D., & Beniak, T.E. (1996). Efficacy of the Continuous Visual Memory Test in lateralizing temporal lobe dysfunction in chronic complex-partial epilepsy. Journal of Clinical and Experimental Neuropsychology, 18, 747754.CrossRefGoogle ScholarPubMed
Stepankova, K., Fenton, A.A., Pastalkova, E., Kalina, M., & Bohbot, V.D. (2004). Object-location memory impairment in patients with thermal lesions to the right or left hippocampus. Neuropsychologia, 42, 10171028.CrossRefGoogle ScholarPubMed
Stout, J.C., Bondi, M.W., Jernigan, T.L., Salmon, D.P., Archibald, S.L., & Delis, D.C. (1999). Regional cerebral volume loss associated with verbal learning and memory in dementia of the Alzheimer type. Neuropsychology, 13, 188197.CrossRefGoogle ScholarPubMed
Strang, J.M., Donnelly, K.Z., Grohman, K., & Kleiner, J. (2002). Verbal learning and visuomotor attention in Alzheimer’s disease and geriatric depression. Brain and Cognition, 49, 216220.Google ScholarPubMed
Thompson, P.M., Hayashi, K.M., de Zubicaray, G., Janke, A.L., Rose, S.E., Semple, J., et al. (2003). Dynamics of gray matter loss in Alzheimer’s disease. Journal of Neuroscience, 23, 9941005.CrossRefGoogle ScholarPubMed
Thompson, P.M., Mega, M.S., Woods, R.P., Zoumalan, C.I., Lindshield, C.J., Blanton, R.E., et al. (2001). Cortical change in Alzheimer’s disease detected with a disease-specific population-based brain atlas. Cerebral Cortex, 11, 116.CrossRefGoogle ScholarPubMed
Trenerry, M.R., Jack, C.R. Jr, Ivnik, R.J., Sharbrough, F.W., Cascino, G.D., Hirschorn, K.A., et al. (1993). MRI hippocampal volumes and memory function before and after temporal lobectomy. Neurology, 43, 18001805.CrossRefGoogle ScholarPubMed
Vanderploeg, R.D., Yuspeh, R.L., & Schinka, J.A. (2001). Differential episodic and semantic memory performance in Alzheimer’s disease and vascular dementias. Journal of the International Neuropsychological Society, 7, 563573.CrossRefGoogle Scholar
Vingerhoets, G., Miatton, M., Vonck, K., Seurinck, R., & Boon, P. (2006). Memory performance during the intracarotid amobarbital procedure and neuropsychological assessment in medial temporal lobe epilepsy: The limits of material specificity. Epilepsy and Behavior, 8, 422428.CrossRefGoogle ScholarPubMed
Welsh, K., Butters, N., Hughes, J., Mohs, R., Heyman, A. (1991). Detection of abnormal memory decline in mild cases of Alzheimer’s disease using CERAD neuropsychological measures. Archives of Neurology, 48, 278281.CrossRefGoogle ScholarPubMed
Welsh, K.A., Butters, N., Hughes, J.P., Mohs, R.C., & Heyman, A. (1992). Detection and staging of dementia in Alzheimer’s disease: Use of the neuropsychological measures developed for the Consortium to Establish a Registry for Alzheimer’s Disease. Archives of Neurology, 49, 448452.CrossRefGoogle ScholarPubMed
Woodard, J.L., Dunlosky, J., & Salthouse, T.A. (1999). Task decomposition analysis of intertrial free recall performance on the Rey Auditory Verbal Learning Test in normal aging and Alzheimer’s disease. Journal of Clinical and Experimental Neuropsychology, 21, 666676.CrossRefGoogle ScholarPubMed
Zahn, R., Juengling, F., Bubrowski, P., Jost, E., Dykierek, P., Talazko, J., & Huell, M. (2004). Hemispheric asymmetries of hypometabolism associated with semantic memory impairment in Alzheimer’s disease: A study using positron emission tomography with fluorodeoxyglucose-F18. Psychiatry Research: Neuroimaging, 132, 159172.CrossRefGoogle ScholarPubMed