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Age-Related Decline in Verbal Learning Is Moderated by Demographic Factors, Working Memory Capacity, and Presence of Amnestic Mild Cognitive Impairment

Published online by Cambridge University Press:  22 August 2014

Fofi Constantinidou ,
Ioannis Zaganas ,
Emmanouil Papastefanakis ,
Dimitrios Kasselimis ,
Andreas Nidos  and
Panagiotis G Simos
Fofi Constantinidou*
Affiliation:
Department of Psychology and Center for Applied Neuroscience, University of Cyprus, Nicosia, Cyprus
Ioannis Zaganas
Affiliation:
School of Medicine, University of Crete, Herakleion, Greece
Emmanouil Papastefanakis
Affiliation:
Department of Psychology, University of Crete, Rethymnon, Greece
Dimitrios Kasselimis
Affiliation:
Department of Psychology, University of Crete, Rethymnon, Greece
Andreas Nidos
Affiliation:
Neuropsychology Department, Metropolitan Hospital, Athens, Greece
Panagiotis G Simos
Affiliation:
School of Medicine, University of Crete, Herakleion, Greece
*
Correspondence and reprint requests to: Fofi Constantinidou, Center for Applied Neuroscience, University of Cyprus, 1678 Nicosia, Cyprus. E-mail: fofic@ucy.ac.cy
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Abstract

Age-related memory changes are highly varied and heterogeneous. The study examined the rate of decline in verbal episodic memory as a function of education level, auditory attention span and verbal working memory capacity, and diagnosis of amnestic mild cognitive impairment (a-MCI). Data were available on a community sample of 653 adults aged 17–86 years and 70 patients with a-MCI recruited from eight broad geographic areas in Greece and Cyprus. Measures of auditory attention span and working memory capacity (digits forward and backward) and verbal episodic memory (Auditory Verbal Learning Test [AVLT]) were used. Moderated mediation regressions on data from the community sample did not reveal significant effects of education level on the rate of age-related decline in AVLT indices. The presence of a-MCI was a significant moderator of the direct effect of Age on both immediate and delayed episodic memory indices. The rate of age-related decline in verbal episodic memory is normally mediated by working memory capacity. Moreover, in persons who display poor episodic memory capacity (a-MCI group), age-related memory decline is expected to advance more rapidly for those who also display relatively poor verbal working memory capacity. (JINS, 2014, 20, 1–14)

Keywords

Episodic memoryAttention spanDementiaAgingWorking memoryMCI
Type
Research Articles
Information
Journal of the International Neuropsychological Society , Volume 20 , Issue 8 , September 2014 , pp. 822 - 835
Copyright
Copyright © The International Neuropsychological Society 2014 

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References

Altmeyer, M., Schweizer, K., Reiss, S., Ren, X., & Schreiner, M. (2013). An account of performance in accessing information stored in long-term memory. A fixed-links model approach. Learning and Individual Differences, 24, 126–133.Google Scholar
Baddeley, A. (1995). Working memory. In M.S. Gazzaniga (Ed.), The cognitive neurosciences (pp. 755–764). Cambridge, MA: The MIT Press.Google Scholar
Baddeley, A.D. (1986). Working memory. New York: Oxford University Press.Google Scholar
Baddeley, A.D. (2000). The episodic buffer: A new component of working memory? Trends in Cognitive Sciences, 4, 417–423.Google Scholar
Baddeley, A.D. (2001). Is working memory still working? American Psychologist, 56, 851–863.Google Scholar
Belleville, S., Gauthier, S., Lepage, E., Kergoat, M.J., & Gilbert, B. (2014). Predicting decline in mild cognitive impairment: A prospective cognitive study. Neuropsychology, 28, 643–652.Google Scholar
Blachstein, H., Greenstein, Y., & Vakil, E. (2012). Aging and temporal order memory: A comparison of direct and indirect measures. Journal of Clinical and Experimental Neuropsychology, 34(1), 107–112.Google Scholar
Bopp, K.L., & Verhaeghen, P. (2005). Aging and verbal memory span: A meta-analysis. The Journals of Gerontology: Series B, 60(5), 223–233.Google Scholar
Chang, Y.L., Jacobson, M.W., Fennema-Notestine, C., Hagler, D.J. Jr., Jennings, R.G., Dale, A.M., &McEvoy, L.K. (2010). Level of executive function influences verbal memory in amnestic mild cognitive impairment and predicts prefrontal and posterior cingulate thickness. Cerebral Cortex, 20, 1305–1313.Google Scholar
Colflesh, G.J.H., & Conway, A.R.A. (2007). Individual differences in working memory capacity and divided attention in dichotic listening. Psychonomic Bulletin & Review, 14(4), 699–703.CrossRefGoogle ScholarPubMed
Constantinidou, F., & Baker, S. (2002). Stimulus modality and verbal learning in normal aging. Brain and Language, 82(3), 296–311.CrossRefGoogle ScholarPubMed
Constantinidou, F., Christodoulou, M., & Prokopiou, J. (2012). The effects of age and education on executive functioning and oral naming performance in Greek Cypriot adults: The neurocognitive study for the aging. Folia-Phoniatrica et Logopaedica, 64(4), 29–40.CrossRefGoogle ScholarPubMed
Conway, A.R.A., Kane, M.J., Bunting, M.F., Hambrick, D.Z., Wilhelm, O., & Engle, R.W. (2005). Working memory span tasks: A methodological review and user’s guide. Psychonomic Bulletin & Review, 12(5), 769–786.Google Scholar
Craik, F.I.M. (1991). Memory functions in normal aging. In T. Yanagihara & R.C. Petersen (Eds.), Memory disorders: Research and clinical practice. New York: Marcel Dekker.Google Scholar
DeCarli, C., Mungas, D., Harvey, D., Reed, B., Weiner, M., Chui, H., &Jagust, W. (2004). Memory impairment, but not cerebrovascular disease, predicts progression of MCI to dementia. Neurology, 63, 220–227.Google Scholar
Devanand, D.P., Liu, X., Brown, P.J., Huey, E.D., Stern, Y., & Pelton, G.H. (2012). A two-study comparison of clinical and MRI markers of transition from mild cognitive impairment to Alzheimer’s disease. International Journal of Alzheimer’s Disease, 2012, 483469.Google Scholar
Economou, A., Papageorgiou, S.G., Karageorgiou, C., & Vassilopoulos, D. (2007). Nonepisodic memory deficits in amnestic MCI. Cognitive and Behavioral Neurology, 20, 99–106.Google Scholar
Facal, D., Juncos-Rabadán, O., Pereiro, A.X., & Lojo-Seoane, C. (2014). Working memory span in mild cognitive impairment. Influence of processing speed and cognitive reserve. International Psychogeriatrics, 26, 615–625.Google Scholar
Fountoulakis, K.N., Tsolaki, M., Chantzi, H., & Kazis, A. (2000). Mini Mental State Examination (MMSE). A validation study in Greek patients with dementia. American Journal of Alzheimer’s Disease and Other Dementias, 15(6), 342–345.Google Scholar
Fountoulakis, K.N., Tsolaki, M., Iacovides, A., Yesavage, J., O’Hara, R., Kazis, A., &Ierodiakonou, C. (1999). The validation of the short form of the Geriatric Depression Scale (GDS) in Greece. Aging (Milano), 11(6), 367–372.Google Scholar
Fountoulakis, K., Iacovides, A., Kleanthous, S., Samolis, S., Kaprinis, S.G., Sitzoglou, K., & Bech, P. (2001). Reliability, validity and psychometric properties of the Greek translation of the Center for Epidemiological Studies-Depression (CES-D) Scale. BMC Psychiatry [Epub ahead of print].Google Scholar
Geffen, G.M., Butterworth, P., Forrester, G.M., & Geffen, L.B. (1994). Auditory verbal learning test components as measures of the severity of closed head Injury. Brain Injury, 8, 405–411.Google Scholar
Geffen, G., & Geffen, L.B., (Laurence Basil), 1937- & Australian Council for Educational Research (2000). Auditory Verbal Learning Test (AVLT) computerized scoring program and population norms. Melbourne: ACER Press.Google Scholar
Geffen, G., Moar, K.J., O’Hanlon, A.P., Clark, C.R., & Geffen, L.B. (1990). Performance measures of 16-to 86-year-old-males and females on the auditory verbal learning test. Clinical Neuropsychologist, 4(1), 45–63.CrossRefGoogle Scholar
Giogkaraki, E., Michaelides, M., & Constantinidou, F. (2013). The role of cognitive reserve in cognitive aging: Results from the Neurocognitive Study on Aging. Journal of Clinical and Experimental Neuropsychology, 35(10), 1024–1035.Google Scholar
Glisky, E.L., Polster, M.R., & Routhieaux, B.C. (1995). Double dissociation between item and source memory. Neuropsychology, 9(2), 229–235.Google Scholar
Hall, C.B., Derby, C., LeValley, A., Katz, M.J., Verghese, J., & Lipton, R.B. (2007). Education delays accelerated decline on a memory test in persons who develop dementia. Neurology, 69, 1657–1664.CrossRefGoogle ScholarPubMed
Hamalainen, A., Tervo, S., Grau-Olivares, M., Niskanen, E., Pennanen, C., Huuskonen, J., & Soininen, H. (2007). Voxel-based morphometry to detect brain atrophy in progressive mild cognitive impairment. Neuroimage, 37, 1122–1131.CrossRefGoogle ScholarPubMed
Hayes, A.F. (2013). Introduction to mediation, moderation, and conditional process analysis: A regression-based approach. New York: The Guilford Press.Google Scholar
Hertzog, C., Dixon, R.A., Hultsch, D.F., & MacDonald, S.W.S. (2003). Latent change models of adult cognition: Are changes in processing speed and working memory associated with changes in episodic memory? Psychology and Aging, 18, 755–769.Google Scholar
Huang, J., Friedland, R.P., & Auchus, A.P. (2007). Diffusion tensor imaging of normal-appearing white matter in mild cognitive impairment and early Alzheimer disease: Preliminary evidence of axonal degeneration in the temporal lobe. AJNR American Journal of Neuroradiology, 28, 1943–1948.Google Scholar
Johnson, A.S., Flicker, L.J., & Lichtenberg, P.A. (2006). Reading ability mediates the relationship between education and executive function tasks. Journal of the International Neuropsychological Society, 12(01), 64–71.Google Scholar
Kane, M.J., & Engle, R.W. (2002). The role of prefrontal cortex in working-memory capacity, executive attention, and general fluid intelligence: An individual-differences perspective. Psychonomic Bulletin & Review, 9(4), 637–671.Google Scholar
Kane, M.J., & Engle, R.W. (2003). Working-memory capacity and the control of attention: The contributions of goal neglect, response competition, and task set to stroop interference. Journal of Experimental Psychology: General, 132(1), 47–70.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(2), 189–217.Google Scholar
Kasniak, A.W., Poon, L.W., & Riege, W. (1986). Assessing memory deficits: An information-processing approach. In L.W. Poon (Ed.), Handbook for clinical memory assessment of older adults. Washington, DC: American Psychological Association.Google Scholar
Klekociuk, S.Z., & Summers, M.J. (2014). Lowered performance in working memory and attentional sub-processes are most prominent in multi-domain amnestic mild cognitive impairment subtypes. Psychogeriatrics, 14, 63–71.Google Scholar
Kosmidis, M.H., Vlahou, C.H., Panagiotaki, P., & Kiosseoglou, G. (2004). The verbal fluency task in the Greek population: Normative data, and clustering and switching strategies. Journal of the International Neuropsychological Society, 10, 164–172.Google Scholar
Kramer, J.H., Mungas, D., Reed, D.R., Wetzel, M.E., Burnett, M.M., Miller, B.L., & Chui, H.C. (2007). Longitudinal MRI and cognitive change in healthy elderly. Neuropsychology, 21(4), 412–418.Google Scholar
Lee, T.M.C., Yuen, K.S.L., Chu, L.W., & Chi, I. (2004). Differential age-related change of prose memory in older Hong Kong Chinese of higher and lower education. International Journal of Geriatric Psychiatry, 19(3), 216–222.Google Scholar
List, J., Kübke, J.C., Lindenberg, R., Külzow, N., Kerti, L., Witte, V., &Flöel, A. (2013). Relationship between excitability, plasticity and thickness of the motor cortex in older adults. Neuroimage, 83, 809–816.Google Scholar
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, 49–100.Google Scholar
Okusaga, O., Stewart, M.C.W., Butcher, I., Deary, I., Gerry, F., Fowkes, R., &Price, J.F. (2013). Smoking, hypercholesterolaemia and hypertension as risk factors. Age and Ageing, 42(3), 306–311.Google Scholar
Park, D.C., & Reuter-Lorenz, P. (2009). The adaptive brain: Aging and neurocognitive scaffolding. Annual Review of Psychology, 60, 173–196.Google Scholar
Reed, B.R., Mungas, D., Tomaszewski Farias, S., Harvey, D., Beckett, L., Widaman, K., & DeCarli, C. (2010). Measuring cognitive reserve based on the decomposition of episodic memory variance. Brain, 133(8), 2196–2209.Google Scholar
Rönnlund, M., Nyberg, L., Bäckman, L., & Nilsson, L.G. (2005). Stability, growth, and decline in adult life span development of declarative memory: Cross-sectional and longitudinal data from a population-based study. Psychology and Aging, 20(1), 3–18.Google Scholar
Salthouse, T.A. (2005). Relations between cognitive abilities and measures of executive functioning. Neuropsychology, 19(4), 532–545.Google Scholar
Salthouse, T.A. (2009). When does age-related cognitive decline begin? Neurobiology of Aging, 30(4), 507–514.Google Scholar
Salthouse, T.A., & Ferrer-Caja, E. (2003). What needs to be explained to account for age-related effects on multiple cognitive variables? Psychology and Aging, 18(1), 91–110.CrossRefGoogle ScholarPubMed
Sander, A., Nakase-Richardson, R., Constantinidou, F., Wertheimer, J., & Paul, D. (2007). Memory assessment on an interdisciplinary rehabilitation team: A theoretically based framework. American Journal of Speech-Language Pathology, 16(4), 316–330.Google Scholar
Satz, P., Cole, M.A., Hardy, D.J., & Rassovsky, Y. (2011). Brain and cognitive reserve: Mediator(s) and construct validity, a critique. Journal of Clinical and Experimental Neuropsychology, 33(1), 121–130.Google Scholar
Schneider-Garces, N.J., Gordon, B.A., Brumback-Peltz, C.R., Shin, E., Lee, Y., Sutton, B.P., & Fabiani, M. (2009). Span, CRUNCH, and beyond: Working memory capacity and the aging brain. Journal of Cognitive Neuroscience, 22, 655–669.Google Scholar
Simos, P.G., Papastefanakis, E., Panou, T., & Kasselimis, D. (2011). The Greek memory scale. Rethymno: Laboratory of Applied Psychology, University of Crete.Google Scholar
Simos, P.G., Kasselimis, D., & Mouzaki, A. (2011). Age, gender, and education effects on vocabulary measures in Greek. Aphasiology, 25, 492–504.Google Scholar
Small, S.A., Schobel, S.A., Buxton, R.B., Witter, M.P., & Barnes, C.A. (2011). A pathophysiological framework of hippocampal dysfunction in ageing and disease. Nature Reviews Neuroscience, 12, 585–601.Google Scholar
Squire, L.R. (1992). Declarative and nondeclarative memory: Multiple brain systems supporting learning and memory. Journal of Cognitive Neuroscience, 4(3), 232–243.Google Scholar
Stern, Y. (2011). Elaborating a hypothetical concept: Comments on the special series on cognitive reserve. Journal of the International Neuropsychological Society, 17(4), 639–642.Google Scholar
Stern, Y. (2009). Cognitive reserve. Neuropsychologia, 47, 2015–2028.Google Scholar
Summers, M.J., & Saunders, N.L. (2012). Neuropsychological measures predict decline to Alzheimer’s dementia from mild cognitive impairment. Neuropsychology, 26, 498–508.Google Scholar
Swanson, H.L. (1999). What develops in working memory? A life span perspective. Developmental Psychology, 35(4), 986–1000.CrossRefGoogle ScholarPubMed
Sweller, J., Van Merrienboer, J.J., & Paas, F.G. (1998). Cognitive architecture and instructional design. Educational psychology review, 10(3), 251–296.Google Scholar
Tulving, E. (1985). How many memory systems are there? American Psychologist, 40(4), 385–398.CrossRefGoogle Scholar
Unsworth, N., & Engle, R.W. (2007). On the division of short-term and working memory: An examination of simple and complex span and their relation to higher order abilities. Psychological Bulletin, 133(6), 1038–1066.Google Scholar
Vakil, E., & Blachstein, H. (1997). Rey AVLT: Developmental norms for adults and the sensitivity of different memory measures to age. The Clinical Neuropsychologist, 11(4), 356–369.Google Scholar
Vakil, E., Weise, M., & Enbar, S. (1997). Direct and indirect memory measures of temporal order: Younger versus older adults. International Journal of Aging and Human Development, 45(3), 195–206.Google Scholar
Wilson, R.S., Beckett, L.A., Barnes, L.L., Schneider, J.A., Bach, J., Evans, D.A., &Bennett, D.A. (2002). Individual differences in rates of change in cognitive abilities of older persons. Psychology and Aging, 17(2), 179–193.Google Scholar
Winblad, B., Palmer, K., Kivipelto, M., Jelic, V., Fratiglioni, L., Wahlund, L.O., & Petersen, R.C. (2004). Mild cognitive impairment—beyond controversies, towards a consensus: Report of the International Working Group on Mild Cognitive Impairment. Journal of Internal Medicine, 256, 240–246.Google Scholar
Wu, W.W., Oh, M.M., & Disterhoft, J.F. (2002). Age-related biophysical alterations of hippocampal pyramidal neurons: Implications for learning and memory. Ageing Research Reviews, 1(2), 181–207.Google Scholar
Zalonis, I., Kararizou, E., Triantafyllou, N.I., Kapaki, E., Papageorgiou, S., Sgouropoulos, P., &Vassilopoulos, D. (2008). A normative study of the trail making test A and B in Greek adults. Clinical Neuropsychologist, 22, 842–850.Google Scholar
Zheng, D., Dong, X., Sun, H., Xu, Y., Ma, Y., & Wang, X. (2012). The overall impairment of core executive function components in patients with amnestic mild cognitive impairment: A cross-sectional study. BMC Neurology, 12, 138.Google Scholar
Zheng, D., Sun, H., Dong, X., Liu, B., Xu, Y., Chen, S., & Wang, X. (2014). Executive dysfunction and gray matter atrophy in amnestic mild cognitive impairment. Neurobiology of Aging, 35, 548–555.Google Scholar