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Visual versus Verbal Working Memory in Statistically Determined Patients with Mild Cognitive Impairment: On behalf of the Consortium for Clinical and Epidemiological Neuropsychological Data Analysis (CENDA)

Published online by Cambridge University Press:  23 September 2019

Sheina Emrani
Department of Psychology, Rowan University, 201 Mullica Hill Rd, Glassboro, NJ 08028, USA
Victor Wasserman
Department of Psychology, Rowan University, 201 Mullica Hill Rd, Glassboro, NJ 08028, USA
Emily Matusz
Department of Geriatrics and Gerontology, New Jersey Institute for Successful Aging, School of Osteopathic Medicine, Rowan University, 42 E Laurel Rd, Stratford, NJ 08084, USA
David Miller
South Jersey Radiology Associates, 1307 White Horse Rd, Ste A102, Voorhees, NJ, 08043, USA
Melissa Lamar
Department of Behavioral Sciences and the Rush Alzheimer’s Disease Center, Rush University Medical Center, 600 S. Paulina St. Chicago, Illinois 60612, USA
Catherine C. Price
Department of Clinical and Health Psychology, University of Florida, 1225 Center Dr, Gainesville, FL 32603, USA
Terrie Beth Ginsberg
Department of Geriatrics and Gerontology, New Jersey Institute for Successful Aging, School of Osteopathic Medicine, Rowan University, 42 E Laurel Rd, Stratford, NJ 08084, USA
Rhoda Au
Departments of Anatomy & Neurobiology, Neurology and Framingham Heart Study, Boston University School of Medicine, 72 E Concord St (L 1004) Boston, Massachusetts 02118, USA Department of Epidemiology, Boston University School of Public Health, 72 E. Concord St Housman (R) Boston, Massachusetts 02118, USA
Rod Swenson
University of North Dakota School of Medicine and Health Sciences, 1301 N Columbia Rd Stop 9037 Grand Forks, ND 58202, USA
David J. Libon*
Department of Psychology, Rowan University, 201 Mullica Hill Rd, Glassboro, NJ 08028, USA Department of Geriatrics and Gerontology, New Jersey Institute for Successful Aging, School of Osteopathic Medicine, Rowan University, 42 E Laurel Rd, Stratford, NJ 08084, USA
*Correspondence and reprint requests to: David J. Libon, Rowan University, School of Osteopathic Medicine, Glassboro, NJ, USA; New Jersey Institute for Successful Aging, 42 E Laurel Rd, Stratford, NJ 08084, USA. E-mail:



Previous research in mild cognitive impairment (MCI) suggests that visual episodic memory impairment may emerge before analogous verbal episodic memory impairment. The current study examined working memory (WM) test performance in MCI to assess whether patients present with greater visual versus verbal WM impairment. WM performance was also assessed in relation to hippocampal occupancy (HO), a ratio of hippocampal volume to ventricular dilation adjusted for demographic variables and intracranial volume.


Jak et al. (2009) (The American Journal of Geriatric Psychiatry, 17, 368–375) and Edmonds, Delano-Wood, Galasko, Salmon, & Bondi (2015) (Journal of Alzheimer’s Disease47(1), 231–242) criteria classify patients into four groups: little to no cognitive impairment (non-MCI); subtle cognitive impairment (SCI); amnestic MCI (aMCI); and a combined mixed/dysexecutive MCI (mixed/dys MCI). WM was assessed using co-normed Wechsler Adult Intelligence Scale-IV (WAIS-IV) Digit Span Backwards and Wechsler Memory Scale-IV (WMS-IV) Symbol Span Z-scores.


Between-group analyses found worse WMS-IV Symbol Span and WAIS-IV Digit Span Backwards performance for mixed/dys MCI compared to non-MCI patients. Within-group analyses found no differences for non-MCI patients; however, all other groups scored lower on WMS-IV Symbol Span than WAIS-IV Digit Span Backwards. Regression analysis with HO as the dependent variable was statistically significant for WMS-IV Symbol Span performance. WAIS-IV Digit Span Backwards performance failed to reach statistical significance.


Worse WMS-IV Symbol Span performance was observed in patient groups with measurable neuropsychological impairment and better WMS-IV Symbol Span performance was associated with higher HO ratios. These results suggest that visual WM may be particularly sensitive to emergent illness compared to analogous verbal WM tests.

Regular Research
Copyright © INS. Published by Cambridge University Press, 2019 

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Belleville, S., Fouquet, C., Hudon, C., Zomahoun, H.T.V., & Croteau, J. (2017). Consortium for the early identification of Alzheimer’s disease-Quebec. 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), 328353.CrossRefGoogle ScholarPubMed
Bohbot, V.D., Kalina, M., Stepankova, K., Spackova, N., Petrides, M., & Nadel, L.Y.N.N. (1998). Spatial memory deficits in patients with lesions to the right hippocampus and to the right parahippocampal cortex. Neuropsychologia, 36(11), 12171238.CrossRefGoogle ScholarPubMed
Bublak, P., Redel, P., Sorg, C., Kurz, A., Förstl, H., Müller, H.J., Schneider, W.X., & Finke, K. (2011). Staged decline of visual processing capacity in mild cognitive impairment and Alzheimer’s disease. Neurobiology of Aging, 32(7), 12191230.CrossRefGoogle ScholarPubMed
Burgess, N., Maguire, E.A., & O’Keefe, J. (2002). The human hippocampus and spatial and episodic memory. Neuron, 35(4), 625641.CrossRefGoogle ScholarPubMed
Carew, T.G., Lamar, M., Cloud, B.S., Grossman, M., & Libon, D.J. (1997). Impairment in category fluency in ischaemic vascular dementia. Neuropsychology 11, 400412.CrossRefGoogle Scholar
Chein, J.M., Moore, A.B., & Conway, A.R. (2011). Domain-general mechanisms of complex working memory span. Neuroimage, 54(1), 550559.CrossRefGoogle ScholarPubMed
Chow, N., Hwang, K.S., Hurtz, S., Green, A.E., Somme, J.H., Thompson, P.M., Elashoff, D.A., Jack, C.R., Weiner, M., & Apostolova, L.G. (2015). Comparing 3T and 1.5 T MRI for mapping hippocampal atrophy in the Alzheimer’s Disease Neuroimaging Initiative. American Journal of Neuroradiology, 36(4), 653660.CrossRefGoogle Scholar
Clare, R., King, V.G., Wirenfeldt, M., & Vinters, H.V. (2010). Synapse loss in dementias. Journal of Neuroscience Research, 88(10), 20832090.CrossRefGoogle ScholarPubMed
Cohen, J. (1988). Statistical Power Analysis for the Behavioral Sciences. New York, NY: Routledge, Academic.Google Scholar
Crane, J. & Milner, B. (2005). What went where? Impaired object-location learning in patients with right hippocampal lesions. Hippocampus, 15(2), 216231.CrossRefGoogle ScholarPubMed
Davachi, L. & Wagner, A.D. (2002). Hippocampal contributions to episodic encoding: insights from relational and item-based learning. Journal of Neurophysiology, 88(2), 982990.CrossRefGoogle ScholarPubMed
De Anna, F., Felician, O., Barbeau, E., Mancini, J., Didic, M., & Ceccaldi, M. (2014). Cognitive changes in mild cognitive impairment patients with impaired visual recognition memory. Neuropsychology, 28(1), 98.CrossRefGoogle ScholarPubMed
de Toledo-Morrell, L., Dickerson, B., Sullivan, M.P., Spanovic, C., Wilson, R., & Bennett, D.A. (2000). Hemispheric differences in hippocampal volume predict verbal and spatial memory performance in patients with Alzheimer’s disease. Hippocampus, 10(2), 136142.3.0.CO;2-J>CrossRefGoogle ScholarPubMed
Delis, D.C., Kramer, J.H., Kaplan, E., & Ober, B.A. (2000). CVLT-II: California Verbal Learning Test: Adult Version. San Antonio, TX: Psychological Corporation.Google Scholar
Delis, D.C., Kramer, J.H., Kaplan, E., & Thompkins, B.A.O. (1987). CVLT: California Verbal Learning Test-Adult Version: Manual. San Antonio, TX: Psychological Corporation.Google Scholar
Didic, M., Felician, O., Barbeau, E.J., Mancini, J., Latger-Florence, C., Tramoni, E., & Ceccaldi, M. (2013). Impaired visual recognition memory predicts Alzheimer’s disease in amnestic mild cognitive impairment. Dementia and Geriatric Cognitive Disorders, 35(5–6), 291299.CrossRefGoogle ScholarPubMed
Edmonds, E.C., Delano-Wood, L., Galasko, D.R., Salmon, D.P., & Bondi, M.W. (2015). Subtle cognitive decline and biomarker staging in preclinical Alzheimer’s disease. Journal of Alzheimer’s Disease, 47(1), 231242.CrossRefGoogle ScholarPubMed
Eichenbaum, H., Cohen, N.J., & Squire, L.R. (2001). Book review-The many faces of memory-From Conditioning to Conscious Recollection: Memory Systems of the Brain. Nature Neuroscience, 4(9), 867868.Google Scholar
Elosúa, M.R., Ciudad, M.J., & Contreras, M.J. (2017). Gender differences in verbal and visuospatial working memory tasks in patients with mild cognitive impairment and Alzheimer disease. Dementia and Geriatric Cognitive Disorders Extra, 7(1), 101108.CrossRefGoogle ScholarPubMed
Emrani, S., Libon, D.J., Lamar, M., Price, C.C., Jefferson, A.L., Gifford, K.A., Hohman, T.J., Nation, D.A., Delano-Wood, L., Jak, A., & Bangen, K.J. (2018). Assessing working memory in mild cognitive impairment with serial order recall. Journal of Alzheimer’s Disease: JAD, 61(3), 917928. CrossRefGoogle ScholarPubMed
Enders, C.K. (2003). Performing multivariate group comparisons following a statistically significant MANOVA. Measurement and Evaluation in Counseling and Development, 36, 4056.CrossRefGoogle Scholar
Eppig, J., Wambach, D., Nieves, C., Price, C.C., Lamar, M., Delano-Wood, L., … & Lippa, C. (2012). Dysexecutive functioning in mild cognitive impairment: Derailment in temporal gradients. Journal of the International Neuropsychological Society, 18(1), 2028.CrossRefGoogle ScholarPubMed
Ezzati, A., Katz, M.J., Zammit, A.R., Lipton, M.L., Zimmerman, M.E., Sliwinski, M.J., & Lipton, R.B. (2016). Differential association of left and right hippocampal volumes with verbal episodic and spatial memory in older adults. Neuropsychologia, 93, 380385.CrossRefGoogle ScholarPubMed
Farid, N., Girard, H.M., Kemmotsu, K., Smith, M.E., Magda, S.W., Lim, W.Y., Lee, R.R., & McDonald, C.R. (2012). Temporal lobe epilepsy: quantitative MR volumetry in detection of hippocampal atrophy. Radiology, 264(2), 542550.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(3), 189198.CrossRefGoogle ScholarPubMed
Fu, H., Rodriguez, G.A., Herman, M., Emrani, S., Nahmani, E., Barrett, G., Figueroa, H.Y., Goldberg, E., Hussaini, S.A., & Duff, K.E. (2017). Tau pathology induces excitatory neuron loss, grid cell dysfunction, and spatial memory deficits reminiscent of early Alzheimer’s disease. Neuron, 93(3), 533541.CrossRefGoogle ScholarPubMed
Gillick, B.T. & Zirpel, L. (2012). Neuroplasticity: an appreciation from synapse to system. Archives of Physical Medicine and Rehabilitation, 93(10), 18461855.CrossRefGoogle Scholar
Habeck, C., Rakitin, B., Steffener, J., & Stern, Y. (2012). Contrasting visual working memory for verbal and non-verbal material with multivariate analysis of fMRI. Brain research, 1467, 2741.CrossRefGoogle ScholarPubMed
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, 23492361.CrossRefGoogle ScholarPubMed
Heister, D., Brewer, J.B., Magda, S., Blennow, K., & McEvoy, L.K. (2011). Alzheimer’s Disease Neuroimaging Initiative. Predicting MCI outcome with clinically available MRI and CSF biomarkers. Neurology, 77(17), 16191628.CrossRefGoogle Scholar
Huberty, C.J. & Morris, J.D. (1989). Multivariate analysis versus multiple univariate analyses. Psychological Bulletin, 105, 302308.CrossRefGoogle Scholar
Hultsch, D.F., Hertzog, C., Small, B.J., & Dixon, R.A. (1999). Use it or lose it: engaged lifestyle as a buffer of cognitive decline in aging? Psychology and Aging, 14(2), 245.CrossRefGoogle Scholar
Jak, A.J., Bondi, M.W., Delano-Wood, L., Wierenga, C., Corey-Bloom, J., Salmon, D.P., Delis, D. C. (2009). Quantification of five neuropsychological approaches to defining mild cognitive impairment. The American Journal of Geriatric Psychiatry, 17, 368375.CrossRefGoogle ScholarPubMed
Jak, A.J., Panizzon, M.S., Spoon, K.M., Fennema-Notestine, C., Franz, C.E., Thompson, … & Kremen, W.S., (2015). Hippocampal atrophy varies by neuropsychologically-defined MCI among men in their 50s. American Journal of Geriatric Psychiatry, 23(5), 456465.CrossRefGoogle ScholarPubMed
Kane, M.J., Hambrick, D.Z., Tuholski, S.W., Wilhelm, O., Payne, T.W., & Engle, R.W. (2004). The generality of working memory capacity: a latent-variable approach to verbal and visuospatial memory span and reasoning. Journal of Experimental Psychology: General, 133, 189217.CrossRefGoogle ScholarPubMed
Kaplan, E., Goodglass, H., & Weintraub, S. (1983). The Boston Naming Test. Philadelphia : Lea and Febiger.Google Scholar
Lamar, M., Catani, M., Price, C.C., Heilman, K.M., & Libon, D.J. (2008). The impact of region specific leukoaraiosis on working memory deficits in dementia. Neuropsychologia, 46, 25972601.CrossRefGoogle ScholarPubMed
Lamar, M., Price, C.C., Davis, K.L., Kaplan, E., & Libon, D.J. (2002). Capacity to maintain mental set in dementia. Neuropsychologia, 40(4), 435445.CrossRefGoogle ScholarPubMed
Lamar, M., Price, C.C., Libon, D.J., Penney, D.L., Kaplan, E., Grossman, M., & Heilman, K.M. (2007). Alterations in working memory as a function of leukoaraiosis in dementia. Neuropsychologia, 45, 245254.CrossRefGoogle ScholarPubMed
Lawton, M.P. & Brody, E.M. (1969). Assessment of older people: self-maintaining and instrumental activities of daily living. The Gerontologist, 9(3_Part_1), 179186.CrossRefGoogle ScholarPubMed
Leszczyński, M., Fell, J., & Axmacher, N. (2015). Rhythmic working memory activation in the human hippocampus. Cell Reports, 13(6), 12721282.CrossRefGoogle ScholarPubMed
Liang, Y., Pertzov, Y., Nicholas, J.M., Henley, S.M.D., Crutch, S., Woodward, F., Leung, K., Fox, N.C., & Husain, M. (2016). Visual short-term memory binding deficit in familial Alzheimer’s disease. Cortex, 78, 150164.CrossRefGoogle ScholarPubMed
Markham, J.A. & Greenough, W.T. (2004). Experience-driven brain plasticity: beyond the synapse. Neuron Glia Biology, 1(4), 351363.CrossRefGoogle ScholarPubMed
Maxwell, S.E. (1992). Recent developments in MANOVA applications, In Thompson, B. (Ed.), Advances in social science methodology, Vol. 2, (pp. 137168). Stanford, CT: JAI Press.Google Scholar
McEvoy, L.K. & Brewer, J.B. (2012). Biomarkers for the clinical evaluation of the cognitively impaired elderly: amyloid is not enough. Imaging Medicine, 4(3), 343357.CrossRefGoogle ScholarPubMed
Moses, S. N. & Ryan, J. D. (2006). A comparison and evaluation of the predictions of relational and conjunctive accounts of hippocampal function. Hippocampus, 16(1), 43e65. CrossRefGoogle ScholarPubMed
Murray, M.E., Graff-Radford, N.R., Ross, O.A., Petersen, R.C., Duara, R., & Dickson, D.W. (2011). Neuropathologically defined subtypes of Alzheimer’s disease with distinct clinical characteristics: a retrospective study. Lancet Neurology, 10, 785796.CrossRefGoogle ScholarPubMed
O’Keefe, J., Burgess, N., Donnett, J.G., Jeffery, K.J., & Maguire, E.A. (1998). Place cells, navigational accuracy, and the human hippocampus. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 353(1373), 13331340.CrossRefGoogle ScholarPubMed
Okonkwo, O.C., Oh, J.M., Koscik, R., Jonaitis, E., Cleary, C.A., Dowling, N.M., Bendlin, B.B., LaRue, A., Hermann, B.P., Barnhart, T.E., & Murali, D. (2014). Amyloid burden, neuronal function, and cognitive decline in middle-aged adults at risk for Alzheimer’s disease. Journal of the International Neuropsychological Society, 20(4), 422433.CrossRefGoogle ScholarPubMed
Olson, I.R., Moore, K.S., Stark, M., & Chatterjee, A. (2006). Visual working memory is impaired when the medial temporal lobe is damaged. Journal of Cognitive Neuroscience, 18(7), 10871097.CrossRefGoogle ScholarPubMed
Park, D.C., Lautenschlager, G., Hedden, T., Davidson, N.S., Smith, A.D., & Smith, P.K. (2002). Models of visuospatial and verbal memory across the adult life span. Psychology and Aging, 17(2), 299.CrossRefGoogle ScholarPubMed
Piekema, C., Kessels, R.P., Mars, R.B., Petersson, K.M., & Fernández, G. (2006). The right hippocampus participates in short-term memory maintenance of object–location associations. Neuroimage, 33(1), 374382.CrossRefGoogle ScholarPubMed
Reitan, R.M. & Wolfson, D. (1985). The Halstead-Reitan Neuropsychological Test Battery: Theory and Clinical Interpretation, Vol. 4. Tucson, AZ: Reitan Neuropsychology.Google Scholar
Ruiz-Rizzo, A.L., Bublak, P., Redel, P., Grimmer, T., Müller, H.J., Sorg, C., & Finke, K. (2017). Simultaneous object perception deficits are related to reduced visual processing speed in amnestic mild cognitive impairment. Neurobiology of Aging, 55, 132142.CrossRefGoogle ScholarPubMed
Scheff, S.W. & Price, D.A. (2003). Synaptic pathology in Alzheimer’s disease: a review of ultrastructural studies. Neurobiol Aging, 24, 10291046.CrossRefGoogle ScholarPubMed
Sheikh, J.I. & Yesavage, J.A. (1986). Geriatric Depression Scale (GDS): recent evidence and development of a shorter version. Clinical Gerontologist: The Journal of Aging and Mental Health, 5, 165172.Google Scholar
Smith, E.E., Geva, A., Jonides, J., Miller, A., Reuter-Lorenz, P., & Koeppe, R.A. (2001). The neural basis of task-switching in working memory: effects of performance and aging. Proceedings of the National Academy of Sciences, 98(4), 20952100.CrossRefGoogle ScholarPubMed
Smith, M. L. & Milner, B. (1981). The role of the right hippocampus in the recall of spatial location. Neuropsychologia, 19(6), 781793.CrossRefGoogle ScholarPubMed
Smith, M. L. & Milner, B. (1989). Right hippocampal impairment in the recall of spatial location: encoding deficit or rapid forgetting? Neuropsychologia, 27(1), 7181.CrossRefGoogle ScholarPubMed
Spellman, T., Rigotti, M., Ahmari, S.E., Fusi, S., Gogos, J.A., & Gordon, J.A. (2015). Hippocampal–prefrontal input supports spatial encoding in working memory. Nature, 522(7556), 309.CrossRefGoogle ScholarPubMed
Spreen, O. & Strauss, E. (1990). Compendium of Neuropsychological Tests. New York : Oxford University Press.Google Scholar
Squire, L.R. (1992). Memory and the hippocampus: a synthesis from findings with rats, monkeys,and humans. Psychological Review, 99(2), 195231.CrossRefGoogle ScholarPubMed
Tabachnick, B.G. & Fidell, L.S. (2013). Using multivariate statistics, 6th edn Boston, MA: Pearson.Google Scholar
Tanpitukpongse, T.P., Mazurowski, M.A., Ikhena, J., Petrella, J.R., & Alzheimer’s Disease Neuroimaging Initiative (2017). Predictive utility of marketed volumetric software tools in subjects at risk for Alzheimer’s: do regions outside the hippocampus matter? American Journal of Neuroradiology, 38, 546552.CrossRefGoogle ScholarPubMed
Terry, R.D., Masliah, E., Salmon, D.P., Butters, N., DeTeresa, R., Hill, R., Hansen, L.A., & Katzman, R. (1991). Physical basis of cognitive alterations in Alzheimer’s disease: synapse loss is the major correlate of cognitive impairment. Annals of Neurology: Official Journal of the American Neurological Association and the Child Neurology Society, 30(4), 572580.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Voyer, D., Voyer, S.D., & Saint-Aubin, J. (2017). Sex differences in visual-spatial working memory: a meta-analysis. Psychonomic Bulletin & Review, 24(2), 307334.CrossRefGoogle ScholarPubMed
Wechsler, D. (1997). WAIS-III: Administration and Scoring Manual: Wechsler Adult Intelligence Scale. San Antonio, TX: Psychological Corporation.Google Scholar
Yau, W.Y.W, Tudorascu, D.L., McDade, E.M., Ikonomovic, S., James, J.A., Minhas, D., Mowrey, W., Sheu, L.K., Snitz, B.E., Weissfeld, L., & Gianaros, P.J., (2015). Longitudinal assessment of neuroimaging and clinical markers in autosomal dominant Alzheimer’s disease: a prospective cohort study. The Lancet Neurology, 14(8), 804813.CrossRefGoogle ScholarPubMed
Yonelinas, A.P. (2013). The hippocampus supports high-resolution binding in the service of perception, working memory and long-term memory. Behavioural Brain Research, 254, 3444.CrossRefGoogle ScholarPubMed