Assessment of Memory Impairment in Early Diagnosis of Alzheimer’s Disease

Author(s): Martin Vyhnálek*, Hana Marková, Jan Laczó, Rossana De Beni, Santo Di Nuovo.

Journal Name: Current Alzheimer Research

Volume 16 , Issue 11 , 2019

  Journal Home
Translate in Chinese
Become EABM
Become Reviewer


Memory impairment has been considered as one of the earliest clinical hallmarks of Alzheimer’s disease. This paper summarizes recent progress in the assessment of memory impairment in predementia stages. New promising approaches of memory assessment include evaluation of longitudinal cognitive changes, assessment of long-term memory loss, evaluation of subjective cognitive concerns and testing of other memory modalities, such as spatial memory. In addition, we describe new challenging memory tests based on memory binding paradigms that have been recently developed and are currently being validated.

Keywords: Elderly, memory impairment, Alzheimer's disease, mild cognitive impairment, subjective cognitive decline, neuropsychological assessment, memory binding, spatial memory.

Albert MS, DeKosky ST, Dickson D, Dubois B, Feldman HH, Fox NC, et al. The diagnosis of mild cognitive impairment due to Alzheimer’s disease: recommendations from the National Institute on Aging and Alzheimer’s Association workgroup. Alzheimers Dement 7: 270-9.(2011);
Gainotti G, Quaranta D, Vita MG, Marra C. Neuropsychological predictors of conversion from mild cognitive impairment to Alzheimer’s disease. J Alzheimers Dis 38(3): 481-95.(2014);
Sperling R, Aisen P, Beckett L, Bennett D, Craft S, Fagan A, et al. Toward defining the preclinical stages of Alzheimer’s disease: Recommendations from the National Institute on Aging and the Alzheimer’s Association workgroup. Alzheimers Dement 7: 280-92.(2011);
Sperling RA, Jack CR, Aisen PS. Testing the right target and right drug at the right stage. Sci Transl Med 3(111): 111-33.(2011);
Vellas B, Bateman R, Blennow K, Frisoni G, Johnson K, Katz R, et al. Endpoints for Pre-Dementia AD Trials A Report from the EU/US/CTAD Task Force 2(2): 128-35.(2015);
Braak H, Braak E. Neuropathological staging of Alzheimer-related changes. Acta Neuropathol 82: 239-59.(1991);
Jack CR, Knopman DS, Jagust WJ, Petersen RC, Weiner MW, Aisen PS, et al. Tracking pathophysiological processes in Alzheimer’s disease: an updated hypothetical model of dynamic biomarkers. Lancet Neurol 12(2): 207-16.(2013);
Clark CM, Schneider JA, Bedell BJ, Beach TG, Bilker WB, Mintun MA, et al. Use of florbetapir-PET for imaging beta-amyloid pathology. JAMA 305(3): 275-83.(2011);
Blennow K, Hampel H. CSF markers for incipient Alzheimer’s disease. Lancet Neurol 2(10): 605-13.(2003);
Bondareff W, Mountjoy CQ, Roth M, Rossor MN, Iversen LL, Reynolds GP, et al. Neuronal degeneration in locus ceruleus and cortical correlates of Alzheimer disease. Alzheimer Dis Assoc Disord 1(4): 256-62.(1987);
Bondareff W, Mountjoy CQ, Roth M. Loss of neurons of origin of the adrenergic projection to cerebral cortex (nucleus locus ceruleus) in senile dementia. Neurology 32(2): 164-8.(1982);
Court J, Martin-Ruiz C, Piggott M, Spurden D, Griffiths M, Perry E. Nicotinic receptor abnormalities in Alzheimer’s disease. Biol Psychiatry 49(3): 175-84.(2001);
Theofilas P, Ehrenberg AJ, Dunlop S, Di Lorenzo Alho AT, Nguy A, Leite REP, et al. Locus coeruleus volume and cell population changes during Alzheimer’s disease progression: a stereological study in human postmortem brains with potential implication for early-stage biomarker discovery. Alzheimers Dement 13(3): 236-46.(2017);
Aisen PS, Cummings J, Schneider LS. Symptomatic and nonamyloid/tau based pharmacologic treatment for Alzheimer disease. Cold Spring Harb Perspect Med 2(3) a006395(2012);
Albert MS, Moss MB, Tanzi R, Jones K. Preclinical prediction of AD using neuropsychological tests. J Int Neuropsychol Soc 7(5): 631-9.(2001);
Grober E, An Y, Lipton RB, Kawas C, Resnick SM. Timing of onset and rate of decline in learning and retention in the pre-dementia phase of Alzheimer’s disease. J Int Neuropsychol Soc 25(7): 699-705.(2019);
Larrabee GJ, Youngjohn JR, Sudilovsky A, Crook TH. Accelerated forgetting in Alzheimer-type dementia. J Clin Exp Neuropsychol 15(5): 701-12.(1993);
Lezak M, Howieson D, Bigler E, Tranel D. Neuropsychological assessment. 5th ed. New York: Oxford University Press (2012).
Buschke H, Sliwinski MJ, Kuslansky G, Lipton RB. Diagnosis of early dementia by the Double Memory Test: encoding specificity improves diagnostic sensitivity and specificity. Neurology 48(4): 989-97.(1997);
Carlesimo GA, Mauri M, Graceffa AM, Fadda L, Loasses A, Lorusso S, et al. Memory performances in young, elderly, and very old healthy individuals versus patients with Alzheimer’s disease: evidence for discontinuity between normal and pathological aging. J Clin Exp Neuropsychol 20(1): 14-29.(1998);
Clark LR, Stricker NH, Libon DJ, Delano-Wood L, Salmon DP, Delis DC, et al. Yes/no versus forced-choice recognition memory in mild cognitive impairment and Alzheimer’s disease: patterns of impairment and associations with dementia severity. Clin Neuropsychol 26(7): 1201-16.(2012);
Westerberg C, Mayes A, Florczak SM, Chen Y, Creery J, Parrish T, et al. Distinct medial temporal contributions to different forms of recognition in amnestic mild cognitive impairment and Alzheimer’s disease. Neuropsychologia 51(12): 2450-61.(2013);
Westerberg CE, Paller KA, Weintraub S, Mesulam M-M, Holdstock JS, Mayes AR, et al. When memory does not fail: Familiarity-based recognition in mild cognitive impairment and Alzheimer’s disease. Neuropsychology 20(2): 193-205.(2006);
Teichmann M, Epelbaum S, Samri D, Levy NM, Michon A, Hampel H, et al. Free and Cued Selective Reminding Test - accuracy for the differential diagnosis of Alzheimer’s and neurodegenerative diseases: a large-scale biomarker-characterized monocenter cohort study (ClinAD). Alzheimers Dement 13(8): 913-23.(2017);
Addis DR, Tippett LJ. Memory of myself: autobiographical memory and identity in Alzheimer’s disease. Memory 12(1): 56-74.(2004);
Frankland PW, Bontempi B. The organization of recent and remote memories. Nat Rev Neurosci 6(2): 119-30.(2005);
Smith CN, Squire LR. Medial temporal lobe activity during retrieval of semantic memory is related to the age of the memory. J Neurosci 29(4): 930-8.(2009);
Squire LR, Bayley PJ. The neuroscience of remote memory. Curr Opin Neurobiol 17(2): 185-96.(2007);
Kopelman MD. Remote and autobiographical memory, temporal context memory and frontal atrophy in Korsakoff and Alzheimer patients. Neuropsychologia 27(4): 437-60.(1989);
Maruta C, Guerreiro M, de Mendonça A, Hort J, Scheltens P. The use of neuropsychological tests across Europe: the need for a consensus in the use of assessment tools for dementia. Eur J Neurol 18(2): 279-85.(2011);
Busse A, Bischkopf J, Riedel-Heller SG, Angermeyer MC. Subclassifications for mild cognitive impairment: prevalence and predictive validity. Psychol Med 33(6): 1029-38.(2003);
Dubois B, Feldman HH, Jacova C, DeKosky ST, Barberger-Gateau P, Cummings J, et al. Research criteria for the diagnosis of Alzheimer’s disease: revising the NINCDS-ADRDA criteria. Lancet Neurol 6: 734-46.(2007);
Hort J, O’Brien JT, Gainotti G, Pirttila T, Popescu BO, Rektorova I, et al. EFNS guidelines for the diagnosis and management of Alzheimer’s disease. Eur J Neurol 17(10): 1236-48.(2010);
Tulving E, Thomson DM. Encoding specificity and retrieval processes in episodic memory. Psychol Rev 80(5): 352-73.(1973);
Carlesimo GA, Perri R, Caltagirone C. Category cued recall following controlled encoding as a neuropsychological tool in the diagnosis of Alzheimer’s disease: a review of the evidence. Neuropsychol Rev 21: 54-65.(2011);
Brooks BL, Iverson GL, Lanting SC, Horton AM, Reynolds CR. Improving test interpretation for detecting executive dysfunction in adults and older adults: prevalence of low scores on the test of verbal conceptualization and fluency. Appl Neuropsychol 19(1): 61-70.(2012);
Loewenstein DA, Acevedo A, Potter E, Schinka JA, Raj A, Greig MT, et al. Severity of medial temporal atrophy and amnestic mild cognitive impairment: selecting type and number of memory tests. Am J Geriatr Psychiatry 17(12): 1050-8.(2009);
Perri R, Carlesimo GA, Serra L, Caltagirone C. When the amnestic mild cognitive impairment disappears. Cogn Behav Neurol 22(2): 109-16.(2009);
Sarazin M, Berr C, De Rotrou J, Fabrigoule C, Pasquier F, Legrain S, et al. Amnestic syndrome of the medial temporal type identifies prodromal AD: a longitudinal study. Neurology 69(19): 1859-67.(2007);
Auriacombe S, Helmer C, Amieva H, Berr C, Dubois B, Dartigues JF. Validity of the free and cued selective reminding test in predicting dementia: the 3C study. Neurology 74(22): 1760-7.(2010);
Grober E, Hall CB, Lipton RB, Zonderman AB, Resnick SM, Kawas C. Memory impairment, executive dysfunction, and intellectual decline in preclinical Alzheimer’s disease. J Int Neuropsychol Soc 14(2): 266-78.(2008);
Grober E, Veroff AE, Lipton RB. Temporal unfolding of declining episodic memory on the Free and Cued Selective Reminding Test in the predementia phase of Alzheimer’s disease: Implications for clinical trials. Alzheimers Dement 10: 161-71.(2018);
Vyhnalek M, Nikolai T, Andel R, Nedelska Z, Rubínová E, Marková H, et al. Neuropsychological correlates of hippocampal atrophy in memory testing in nondemented older adults. J Alzheimers Dis 42(3): S81-90.(2014);
Caraci F, Castellano S, Salomone S, Drago F, Bosco P, Di Nuovo S. Searching for disease-modifying drugs in AD: can we combine neuropsychological tools with biological markers? CNS Neurol Disord Drug Targets 13(1): 173-86.(2014);
Amieva H, Mokri H, Le Goff M, Meillon C, Jacqmin-Gadda H, Foubert-Samier A, et al. Compensatory mechanisms in higher-educated subjects with Alzheimer’s disease: a study of 20 years of cognitive decline. Brain 137(Pt 4): 1167-75.(2014);
Stern Y. Cognitive reserve. Neuropsychologia 47: 2015-28.(2009);
Loewenstein DA, Curiel RE, Duara R, Buschke H. Novel cognitive paradigms for the detection of memory impairment in preclinical Alzheimer’s disease. Assessment 25(3): 348-59.(2017);
Rentz DM, Parra Rodriguez MA, Amariglio R, Stern Y, Sperling R, Ferris S. Promising developments in neuropsychological approaches for the detection of preclinical Alzheimer’s disease: a selective review. Alzheimers Res Ther 5(6): 58.(2013);
Jacobson NS, Truax P. Clinical significance: a statistical approach to defining meaningful change in psychotherapy research. J Consult Clin Psychol 59(1): 12-9.(1991);
Jessen F, Amariglio RE, van Boxtel M, Breteler M, Ceccaldi M, Chételat G, et al. A conceptual framework for research on subjective cognitive decline in preclinical Alzheimer’s disease. Alzheimers Dement 10(6): 844-52.(2014);
Jessen F. Subjective and objective cognitive decline at the pre-dementia stage of Alzheimer’s disease. Eur Arch Psychiatry Clin Neurosci 264(S1): 3-7.(2014);
Dubois B, Hampel H, Feldman H, Scheltens P, Aisen P, Andrieu S, et al. Preclinical Alzheimer’s disease: definition, natural history, and diagnostic criteria. Alzheimers Dement 12(3): 292-323.(2016);
Glodzik-Sobanska L, Reisberg B, De Santi S, Babb JS, Pirraglia E, Rich KE, et al. Subjective memory complaints: presence, severity and future outcome in normal older subjects. Dement Geriatr Cogn Disord 24(3): 177-84.(2007);
Jorm AF, Butterworth P, Anstey KJ, Christensen H, Easteal S, Maller J, et al. Memory complaints in a community sample aged 60-64 years: associations with cognitive functioning, psychiatric symptoms, medical conditions, APOE genotype, hippocampus and amygdala volumes, and white-matter hyperintensities. Psychol Med 34(8): 1495-506.(2004);
Jungwirth S, Fischer P, Weissgram S, Kirchmeyr W, Bauer P, Tragl K-H. Subjective memory complaints and objective memory impairment in the Vienna-Transdanube aging community. J Am Geriatr Soc 52(2): 263-8.(2004);
Jonker C, Launer LJ, Hooijer C, Lindeboom J. Memory complaints and memory impairment in older individuals. J Am Geriatr Soc 44(1): 44-9.(1996);
Snitz BE, Morrow LA, Rodriguez EG, Huber KA, Saxton JA. Subjective memory complaints and concurrent memory performance in older patients of primary care providers. J Int Neuropsychol Soc 14(6): 1004-13.(2008);
Balash Y, Mordechovich M, Shabtai H, Giladi N, Gurevich T, Korczyn AD. Subjective memory complaints in elders: depression, anxiety, or cognitive decline? Acta Neurol Scand 127(5): 344-50.(2013);
Zlatar ZZ, Moore RC, Palmer BW, Thompson WK, Jeste DV. Cognitive complaints correlate with depression rather than concurrent objective cognitive impairment in the successful aging evaluation baseline sample. J Geriatr Psychiatry Neurol 27(3): 181-7.(2014);
Zlatar ZZ, Muniz M, Galasko D, Salmon DP. Subjective cognitive decline correlates with depression symptoms and not with concurrent objective cognition in a clinic-based sample of older adults. J Gerontol B Psychol Sci Soc Sci 73(7): 1198-202.(2017);
Donovan NJ, Amariglio RE, Zoller AS, Rudel RK, Gomez-Isla T, Blacker D, et al. Subjective cognitive concerns and neuropsychiatric predictors of progression to the early clinical stages of Alzheimer disease. Am J Geriatr Psychiatry 22(12): 1642-51.(2014);
Jessen F, Wiese B, Bachmann C, Eifflaender-Gorfer S, Haller F, Kölsch H, et al. Prediction of dementia by subjective memory impairment: effects of severity and temporal association with cognitive impairment. Arch Gen Psychiatry 67(4): 414-22.(2010);
Mendonça MD, Alves L, Bugalho P. From subjective cognitive complaints to dementia: who is at risk?: a systematic review. Am J Alzheimers Dis Other Demen 31(2): 105-14.(2016);
Reisberg B, Shulman MB, Torossian C, Leng L, Zhu W. Outcome over seven years of healthy adults with and without subjective cognitive impairment. Alzheimers Dement 6(1): 11-24.(2010);
Howieson DB, Mattek N, Dodge HH, Erten-Lyons D, Zitzelberger T, Kaye JA. Memory complaints in older adults: prognostic value and stability in reporting over time. SAGE Open Med 3(3)(2015);
Amariglio RE, Mormino EC, Pietras AC, Marshall GA, Vannini P, Johnson KA, et al. Subjective cognitive concerns, amyloid-β, and neurodegeneration in clinically normal elderly. Neurology 85(1): 56-62.(2015);
Amariglio RE, Becker JA, Carmasin J, Wadsworth LP, Lorius N, Sullivan C, et al. Subjective cognitive complaints and amyloid burden in cognitively normal older individuals. Neuropsychologia 50(12): 2880-6.(2012);
Perrotin A, La Joie R, de La Sayette V, Barré L, Mézenge F, Mutlu J, et al. Subjective cognitive decline in cognitively normal elders from the community or from a memory clinic: differential affective and imaging correlates. Alzheimers Dement 13(5): 550-60.(2017);
Cantero JL, Iglesias JE, Van Leemput K, Atienza M. Regional hippocampal atrophy and higher levels of plasma amyloid-beta are associated with subjective memory complaints in nondemented elderly subjects. J Gerontol A Biol Sci Med Sci 71(9): 1210-5.(2016);
van der Flier WM, van Buchem MA, Weverling-Rijnsburger AWE, Mutsaers ER, Bollen ELEM, Admiraal-Behloul F, et al. Memory complaints in patients with normal cognition are associated with smaller hippocampal volumes. J Neurol 251(6): 671-5.(2004);
Mosconi L, De Santi S, Brys M, Tsui WH, Pirraglia E, Glodzik-Sobanska L, et al. Hypometabolism and altered cerebrospinal fluid markers in normal apolipoprotein E E4 carriers with subjective memory complaints. Biol Psychiatry 63(6): 609-18.(2008);
Scheef L, Spottke A, Daerr M, Joe A, Striepens N, Kölsch H, et al. Glucose metabolism, gray matter structure, and memory decline in subjective memory impairment. Neurology 79(13): 1332-9.(2012);
Hollands S, Lim YY, Buckley R, Pietrzak RH, Snyder PJ, Ames D, et al. Amyloid-β related memory decline is not associated with subjective or informant rated cognitive impairment in healthy adults. J Alzheimers Dis 43(2): 677-86.(2015);
Amariglio RE, Townsend MK, Grodstein F, Sperling RA, Rentz DM. Specific subjective memory complaints in older persons may indicate poor cognitive function. J Am Geriatr Soc 59(9): 1612-7.(2011);
Caselli RJ, Chen K, Locke DEC, Lee W, Roontiva A, Bandy D, et al. Subjective cognitive decline: self and informant comparisons. Alzheimers Dement 10(1): 93-8.(2014);
Markova H, Andel R, Stepankova H, Kopecek M, Nikolai T, Hort J, et al. Subjective cognitive complaints in cognitively healthy older adults and their relationship to cognitive performance and depressive symptoms. J Alzheimers Dis 59(3): 871-81.(2017);
Rabin LA, Smart CM, Crane PK, Amariglio RE, Berman LM, Boada M, et al. Subjective cognitive decline in older adults: an overview of self-report measures used across 19 international research studies. J Alzheimers Dis 48(1): S63-86.(2015);
Rodríguez-Gómez O, Abdelnour C, Jessen F, Valero S, Boada M. Influence of sampling and recruitment methods in studies of subjective cognitive decline Tales A, Jessen F, Butler C, Wilcock G, Phillips J, Bayer T. J Alzheimer’s Dis. 48(s1): S99-107.(2015);
Abdelnour C, Rodríguez-Gómez O, Alegret M, Valero S, Moreno-Grau S, Sanabria Á, et al. Impact of recruitment methods in subjective cognitive decline. J Alzheimers Dis 57(2): 625-32.(2017);
Mayes A, Montaldi D, Migo E. Associative memory and the medial temporal lobes. Trends Cogn Sci 11(3): 126-35.(2007);
Zimmer H, Mecklinger A, Lindenberger U. Handbook of Binding and Memory: Perspectives from Cognitive Neuroscience. Oxford University Press (2006).
Parra MA, Abrahams S, Fabi K, Logie R, Luzzi S, Della SS. Short-term memory binding deficits in Alzheimer’s disease. Brain 132(Pt 4): 1057-66.(2009);
Villeneuve S, Belleville S. The nature of memory failure in mild cognitive impairment: examining association with neurobiological markers and effect of progression. Neurobiol Aging 33(9): 1967-78.(2012);
Papp KV, Amariglio RE, Mormino EC, Hedden T, Dekhytar M, Johnson KA, et al. Free and cued memory in relation to biomarker-defined abnormalities in clinically normal older adults and those at risk for Alzheimer’s disease. Neuropsychologia 73: 169-75.(2015);
Rentz DM, Amariglio RE, Becker JA, Frey M, Olson LE, Frishe K, et al. Face-name associative memory performance is related to amyloid burden in normal elderly. Neuropsychologia 49(9): 2776-83.(2011);
Aizenstein HJ, Nebes RD, Saxton JA, Price JC, Mathis CA, Tsopelas ND, et al. Frequent amyloid deposition without significant cognitive impairment among the elderly. Arch Neurol 65(11): 1509.(2008);
Mowrey WB, Lipton RB, Katz MJ, Ramratan WS, Loewenstein DA, Zimmerman ME, et al. Memory binding test predicts incident amnestic mild cognitive impairment. J Alzheimers Dis 53(4): 1585-95.(2016);
Gramunt N, Sánchez-Benavides G, Buschke H, Lipton RB, Masramon X, Gispert JD, et al. Psychometric properties of the memory binding test: test-retest reliability and convergent validity. J Alzheimers Dis 50(4): 999-1010.(2016);
Amariglio RE, Frishe K, Olson LE, Wadsworth LP, Lorius N, Sperling RA, et al. Validation of the face name associative memory exam in cognitively normal older individuals. J Clin Exp Neuropsychol 34(6): 580-7.(2012);
Rentz DM, Locascio JJ, Becker JA, Moran EK, Eng E, Buckner RL, et al. Cognition, reserve, and amyloid deposition in normal aging. Ann Neurol 67(3): 353-64.(2010);
Parra M a, Abrahams S, Logie RH, Méndez LG, Lopera F, Della SS. Visual short-term memory binding deficits in familial Alzheimer’s disease. Brain 133(9): 2702-13.(2010);
Della Sala S, Parra MA, Fabi K, Luzzi S, Abrahams S. Short-term memory binding is impaired in AD but not in non-AD dementias. Neuropsychologia 50(5): 833-40.(2012);
Parra MA, Abrahams S, Logie RH, Della Sala S. Visual short-term memory binding in Alzheimer’s disease and depression. J Neurol 257(7): 1160-9.(2010);
Colzato LS, Raffone A, Hommel B. What do we learn from binding features? Evidence for multilevel feature integration. J Exp Psychol Hum Percept Perform 32(3): 705-16.(2006);
Rhodes S, Parra MA, Logie RH. Ageing and feature binding in visual working memory: the role of presentation time. Q J Exp Psychol (Hove) 69(4): 654-68.(2016);
Blake RV, Wroe SJ, Breen EK, McCarthy RA. Accelerated forgetting in patients with epilepsy: evidence for an impairment in memory consolidation. Brain 123(Pt 3): 472-83.(2000);
Weston PSJ, Nicholas JM, Henley SMD, Liang Y, Macpherson K, Donnachie E, et al. Accelerated long-term forgetting in presymptomatic autosomal dominant Alzheimer’s disease: a cross-sectional study. Lancet Neurol 17(2): 123-32.(2018);
Amieva H, Le Goff M, Millet X, Orgogozo JM, Pérès K, Barberger-Gateau P, et al. Prodromal Alzheimer’s disease: Successive emergence of the clinical symptoms. Ann Neurol 64(5): 492-8.(2008);
Elias MF, Beiser A, Wolf PA, Au R, White RF, D’Agostino RB. The preclinical phase of Alzheimer disease: a 22-year prospective study of the Framingham Cohort. Arch Neurol 57(6): 808-13.(2000);
Mistridis P, Krumm S, Monsch AU, Berres M, Taylor KI. The 12 years preceding mild cognitive impairment due to Alzheimer’s disease: the temporal emergence of cognitive decline. J Alzheimers Dis 48(4): 1095-107.(2015);
Gavett BE, Ashendorf L, Gurnani AS. Reliable change on neuropsychological tests in the uniform data set. J Int Neuropsychol Soc 21(07): 558-67.(2015);
Knight RG, McMahon J, Skeaff CM, Green TJ. Reliable Change Index scores for persons over the age of 65 tested on alternate forms of the Rey AVLT. Arch Clin Neuropsychol 22(4): 513-8.(2007);
Bird CM, Papadopoulou K, Ricciardelli P, Rossor MN, Cipolotti L. Test-retest reliability, practice effects and reliable change indices for the recognition memory test. Br J Clin Psychol 42(4): 407-25.(2003);
Stein J, Luppa M, Brähler E, König H-H, Riedel-Heller SG. The assessment of changes in cognitive functioning: reliable change indices for neuropsychological instruments in the elderly - a systematic review. Dement Geriatr Cogn Disord 29(3): 275-86.(2010);
Zygouris S, Tsolaki M. Computerized Cognitive Testing for Older Adults. Am J Alzheimers Dis Other Demen 30(1): 13-28.(2015);
Vlček K, Laczó J. Neural correlates of spatial navigation changes in mild cognitive impairment and Alzheimer’s disease. Front Behav Neurosci 8: 89.(2014);
O’Keefe J, Nadel L. The hippocampus as a cognitive map. Oxford: Clarendon Press (1978).
Piber D, Nowacki J, Mueller SC, Wingenfeld K, Otte C. Sex effects on spatial learning but not on spatial memory retrieval in healthy young adults. Behav Brain Res 336: 44-50.(2018);
Barrash J. Age‐related decline in route learning ability. Dev Neuropsychol 10(3): 189-201.(1994);
Gazova I, Vlcek K, Laczó J, Nedelska Z, Hyncicova E, Mokrisova I, et al. Spatial navigation-a unique window into physiological and pathological aging. Front Aging Neurosci 4: 16.(2012);
Gazova I, Laczó J, Rubinova E, Mokrisova I, Hyncicova E, Andel R, et al. Spatial navigation in young versus older adults. Front Aging Neurosci 5: 94.(2013);
Rodgers MK, Sindone JA, Moffat SD. Effects of age on navigation strategy. Neurobiol Aging 33(1): 202.e15-22.(2012);
Hort J, Laczó J, Vyhnálek M, Bojar M, Bures J, Vlcek K. Spatial navigation deficit in amnestic mild cognitive impairment. Proc Natl Acad Sci USA 104(10): 4042-7.(2007);
Pai M-C, Jacobs WJ. Topographical disorientation in community-residing patients with Alzheimer’s disease. Int J Geriatr Psychiatry 19(3): 250-5.(2004);
McShane R, Gedling K, Keene J, Fairburn C, Jacoby R, Hope T. Getting lost in dementia: a longitudinal study of a behavioral symptom. Int Psychogeriatr 10(3): 253-60.(1998);
deIpolyi AR, Rankin KP, Mucke L, Miller BL, Gorno-Tempini ML. Spatial cognition and the human navigation network in AD and MCI. Neurology 69(10): 986-97.(2007);
Bird CM, Chan D, Hartley T, Pijnenburg YA, Rossor MN, Burgess N. Topographical short-term memory differentiates Alzheimer’s disease from frontotemporal lobar degeneration. Hippocampus 20(10): 1154-69.(2010);
Kalová E, Vlcek K, Jarolímová E, Bures J. Allothetic orientation and sequential ordering of places is impaired in early stages of Alzheimer’s disease: corresponding results in real space tests and computer tests. Behav Brain Res 159(2): 175-86.(2005);
Nedelska Z, Andel R, Laczó J, Vlcek K, Horinek D, Lisy J, et al. Spatial navigation impairment is proportional to right hippocampal volume. Proc Natl Acad Sci USA 109(7): 2590-4.(2012);
Weniger G, Ruhleder M, Lange C, Wolf S, Irle E. Egocentric and allocentric memory as assessed by virtual reality in individuals with amnestic mild cognitive impairment. Neuropsychologia 49(3): 518-27.(2011);
Kerbler GM, Nedelska Z, Fripp J, Laczó J, Vyhnalek M, Lisý J, et al. Basal forebrain atrophy contributes to allocentric navigation impairment in Alzheimer’s disease patients. Front Aging Neurosci 7: 185.(2015);
Laczó J, Vlček K, Vyhnálek M, Vajnerová O, Ort M, Holmerová I, et al. Spatial navigation testing discriminates two types of amnestic mild cognitive impairment. Behav Brain Res 202(2): 252-9.(2009);
Laczó J, Andel R, Vlček K, Macoška V, Vyhnálek M, Tolar M, et al. Spatial Navigation and APOE in Amnestic Mild Cognitive Impairment. Neurodegener Dis 8(4): 169-77.(2011);
Laczó J, Andel R, Vyhnalek M, Vlcek K, Nedelska Z, Matoska V, et al. APOE and spatial navigation in amnestic MCI: results from a computer-based test. Neuropsychology 28(5): 676-84.(2014);
Laczó J, Andel R, Vyhnalek M, Matoska V, Kaplan V, Nedelska Z, et al. The effect of TOMM40 on spatial navigation in amnestic mild cognitive impairment. Neurobiol Aging 36(6): 2024-33.(2015);
Allison SL, Fagan AM, Morris JC, Head D. Spatial navigation in preclinical Alzheimer’s disease. J Alzheimers Dis 52(1): 77-90.(2016);
Kunz L, Schröder TN, Lee H, Montag C, Lachmann B, Sariyska R, et al. Reduced grid-cell-like representations in adults at genetic risk for Alzheimer’s disease. Science 350(6259): 430-3.(2015);
Laczó J, Andel R, Nedelska Z, Vyhnalek M, Vlcek K, Crutch S, et al. Exploring the contribution of spatial navigation to cognitive functioning in older adults. Neurobiol Aging 51: 67-70.(2017);
Keogh R, Pearson J. Mental imagery and visual working memory. PLoS One 6(12) e29221(2011);
Albers AM, Kok P, Toni I, Dijkerman HC, de Lange FP. Shared representations for working memory and mental imagery in early visual cortex. Curr Biol 23(15): 1427-31.(2013);
Di Nuovo S, Castellano S, Guarnera M. Mental Imagery Test. Florence: Hogrefe (2014).
Castellano S, Guarnera M, Di Nuovo S. Imagery in Healthy and in Cognitively Impaired Aging. Clin Gerontol 38(2): 103-13.(2015);
Campos A. Gender differences in imagery. Pers Individ Dif 59: 107-11.(2014);
Buschke H, Mowrey WB, Ramratan WS, et al. Memory binding test distinguishes amnestic mild cognitive impairment and dementia from cognitively normal elderly. Arch Clin Neuropsychol 32(1): 29-39.(2017);
Papp KV, Amariglio RE, Dekhtyar M, Roy K, Wigman S, Bamfo R, et al. Development of a psychometrically equivalent short form of the face-name associative memory exam for use along the early Alzheimer’s disease trajectory. Clin Neuropsychol 28(5): 771-85.(2014);

Rights & PermissionsPrintExport Cite as

Article Details

Year: 2019
Page: [975 - 985]
Pages: 11
DOI: 10.2174/1567205016666191113125303
Price: $65

Article Metrics

PDF: 20