Spatial Navigation in Preclinical Alzheimer's Disease

Journal of Alzheimer's Disease

Volumn 52, Issue 1, 2016, Pages 77-90

  Allison, Samantha L ^a   Fagan, Anne M ^b   Morris, John C ^b   Head, Denise ^a,b,c  

^a WASHINGTON UNIVERSITY   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Aging; allocentric; amyloid; caudate nucleus; egocentric; hippocampus

Indexed keywords

AMYLOID BETA PROTEIN[1-42]; BIOLOGICAL MARKER; MAPT PROTEIN, HUMAN; TAU PROTEIN;

ADULT; AGED; ALZHEIMER DISEASE; ARTICLE; CEREBROSPINAL FLUID; CLINICAL DEMENTIA RATING; COMPARATIVE STUDY; CONTROLLED STUDY; DIAGNOSTIC TEST ACCURACY STUDY; EPISODIC MEMORY; FEMALE; HUMAN; LEARNING; LIKERT SCALE; LUMBAR PUNCTURE; MAJOR CLINICAL STUDY; MALE; MAZE TEST; PRACTICE GUIDELINE; PRIORITY JOURNAL; QUESTIONNAIRE; SENSITIVITY AND SPECIFICITY; SPATIAL ORIENTATION; VIRTUAL REALITY; YOUDEN INDEX; COMPUTER INTERFACE; EDUCATIONAL STATUS; NEUROPSYCHOLOGICAL TEST; PRODROMAL SYMPTOM; PSYCHOLOGY; PSYCHOMOTOR PERFORMANCE; RECEIVER OPERATING CHARACTERISTIC;

AGED; ALZHEIMER DISEASE; BIOMARKERS; EDUCATIONAL STATUS; FEMALE; HUMANS; LEARNING; MALE; NEUROPSYCHOLOGICAL TESTS; PRODROMAL SYMPTOMS; PSYCHOMOTOR PERFORMANCE; ROC CURVE; SPATIAL NAVIGATION; TAU PROTEINS; USER-COMPUTER INTERFACE;

EID: 84973169179     PISSN: 13872877     EISSN: 18758908     Source Type: Journal    
DOI: 10.3233/JAD-150855     Document Type: Article

References (72)

1. Henderson VW, Mack W, Williams BW (1989) Spatial disorientation in Alzheimer's disease. Arch Neurol 46, 391-394
2. Pai MC, Jacobs WJ (2004) Topographical disorientation in community-residing patients with Alzheimer's disease. Int J Geriatr Psychiatry 19, 250-255
3. Tu MC, Pai MC (2006) Getting lost for the first time in patients with Alzheimer's disease. Int Psychogeriatr 18, 567-570
4. Dubinsky RM, Stein AC, Lyons K (2000) Practice parameter: Risk of driving and Alzheimer's disease (an evidence-based review): Report of the quality standards subcommittee of the American Academy of Neurology. Neurology 54, 2205-2211
5. Hunt LA, BrownAE, Gilman IP (2010) Drivers with dementia and outcomes of becoming lost while driving. Am J Occup Ther 64, 225-232
6. Jack CR Jr, Knopman DS, Jagust WJ, Petersen RC, Weiner MW, Aisen PS, Shaw LM, Vemuri P, Wiste HJ, Weigand SD, Lesnick TG, Pankratz VS, Donohue MC, Trojanowski JQ (2013) Tracking pathophysiological processes in Alzheimer's disease: An updated hypothetical model of dynamic biomarkers. Lancet Neurol 12, 207-216
7. Sperling RA, Aisen PS, Beckett LA, Bennett DA, Craft S, Fagan AM, Iwatsubo T, Jack CR Jr, Kaye J, Montine TJ, Park DC, Reiman EM, Rowe CC, Siemers E, Stern Y, Yaffe K, Carrillo MC, Thies B, Morrison-Bogorad M,Wagster MV, Phelps CH (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. Alzheimers Dement 7, 280-292
8. Thal DR, Rüb U, Orantes M, Braak H (2002) Phases of A-deposition in the human brain and its relevance for the development of AD. Neurology 58, 1791-1800
9. Selkoe DJ (2000) The origins of Alzheimer disease: A is for amyloid. JAMA 283, 1615-1617
10. Price JL, McKeel DW Jr, Buckles VD, Roe CM, Xiong C, Grundman M, Hansen LA, Petersen RC, Parisi JE, Dickson DW, Smith CD, Davis DG, Schmitt FA, Markesbery WR, Kaye J, Kurlan R, Hulette C, Kurland BF, Higdon R, Kukull W, Morris JC (2009) Neuropathology of nondemented aging: Presumptive evidence for preclinical Alzheimer disease. Neurobiol Aging 30, 1026-1036
11. Price JL, Morris JC (1999) Tangles and plaques in nondemented aging and "preclinical" Alzheimer's disease. Ann Neurol 45, 358-368
12. Strozyk D, Blennow K, White LR, Launer LJ (2003) CSF Abeta 42 levels correlate with amyloid-neuropathology in a population-based autopsy study. Neurology 60, 652-656
13. Fagan AM, Mintun MA, Mach RH, Lee SY, Dence CS, Shah AR, LaRossa GN, Spinner ML, Klunk WE, Mathis CA, DeKosky ST, Morris JC, Holtzman DM (2006) Inverse relation between in vivo amyloid imaging load and cerebrospinal fluid Abeta42 in humans. Ann Neurol 59, 512-519
14. Becker JA, Hedden T, Carmasin J, Maye J, Rentz DM, Putcha D, Fischl B, Greve DN, Marshall GA, Salloway S, Marks D, Buckner RL, Sperling RA, Johnson KA (2011) Amyloid-associated cortical thinning in clinically normal elderly. Ann Neurol 69, 1032-1042
15. Drzezga A, Becker JA, Van Dijk KR, Sreenivasan A, Talukdar T, Sullivan C, Schultz AP, Sepulcre J, Putcha D, Greve D, Johnson KA, Sperling RA (2011) Neuronal dysfunction and disconnection of cortical hubs in non-demented subjects with elevated amyloid burden. Brain 134, 1635-1646
16. Fjell AM, Walhovd KB, Fennema-Notestine C, McEvoy LK, Hagler DJ, Holland D, Brewer JB, Dale AM, Alzheimer's Disease Neuroimaging Initiative (2010) CSF biomarkers in prediction of cerebral and clinical change in mild cognitive impairment and Alzheimer's disease. J Neurosci 30, 2088-2101
17. Sheline YI, Raichle ME, Snyder AZ, Morris JC, Head D, Wang S, Mintun MA (2010) Amyloid plaques disrupt resting state default mode network connectivity in cognitively normal elderly. Biol Psychiatry 67, 584-587
18. Chételat G, Villemagne VL, Pike KE, Ellis KA, Ames D, Masters CL, Rowe CC; Australian Imaging Biomarkers and Lifestyle Study of Ageing Research Group (2012) Relationship between memory performance and-amyloid deposition at different stages of Alzheimer's disease. Neurodegener Dis 10, 141-144
19. Doraiswamy PM, Sperling RA, Coleman RE, Johnson KA, Reiman EM, Davis MD, Grundman M, Sabbagh MN, Sadowsky CH, Fleisher AS, Carpenter A, Clark CM, Joshi AD, Mintun MA, Skovronsky DM, Pontecorvo MJ, AV45-A11 Study Group (2012) Amyloid-assessed by florbetapir F 18 PET and 18-month cognitive decline: A multicenter study. Neurology 79, 1636-1644
20. Knopman DS, Jack CR Jr, Wiste HJ, Weigand SD, Vemuri P, Lowe V, Kantarci K, Gunter JL, Senjem ML, Ivnik RJ, Roberts RO, Boeve BF, Petersen RC (2012) Short-term clinical outcomes for stages of NIA-AA preclinical Alzheimer disease. Neurology 78, 1576-1582
21. Roe CM, Fagan AM, Grant EA, Hassenstab J, Moulder KL, Maue Dreyfus D, Sutphen CL, Benzinger TL, Mintun MA, HoltzmanDM,Morris JC (2013) Amyloid imaging and CSF biomarkers in predicting cognitive impairment up to 7.5 years later. Neurology 80, 1784-1791
22. Vos SJ, Xiong C, Visser PJ, Jasielec MS, Hassenstab J, Grant EA, Cairns NJ, Morris JC, Holtzman DM, Fagan AM (2013) Preclinical Alzheimer's disease and its outcome: A longitudinal cohort study. Lancet Neurol 12, 957-965
23. Morris JC, Storandt M, Miller JP, McKeel DW, Price JL, Rubin EH, Berg L (2001) Mild cognitive impairment represents early-stage Alzheimer disease. Arch Neurol 58, 397-405
24. Petersen RC, Smith GE, Waring SC, Ivnik RJ, Tangalos EG, Kokmen E (1999) Mild cognitive impairment: Clinical characterization and outcome. Arch Neurol 56, 303-308
25. Pennanen C, Kivipelto M, Tuomainen S, Hartikainen P, Hänninen T, Laakso MP, Hallikainen M, Vanhanen M, Nissinen A, Helkala EL, Vainio P, Vanninen R, Partanen K, Soininen H (2004) Hippocampus and entorhinal cortex in mild cognitive impairment and early AD. Neurobiol Aging 25, 303-310
26. Mormino EC, Kluth JT, Madison CM, Rabinovici GD, Baker SL, Miller BL, Koeppe RA, Mathis CA,WeinerMW, Jagust WJ; Alzheimer's Disease Neuroimaging Initiative (2009) Episodic memory loss is related to hippocampalmediated beta-amyloid deposition in elderly subjects. Brain 132, 1310-1323
27. Storandt M, Mintun MA, Head D, Morris JC (2009) Cognitive decline and brain volume loss as signatures of cerebral amyloid-beta peptide deposition identified with Pittsburgh compound B: Cognitive decline associated with Abeta deposition. Arch Neurol 66, 1476-1481
28. Madsen SK, Ho AJ, Hua X, Saharan PS, Toga AW, Jack CR Jr, Weiner MW, Thompson PM, Alzheimer's Disease Neuroimaging Initiative (2010) 3D maps localize caudate nucleus atrophy in 400 Alzheimer's disease, mild cognitive impairment, and healthy elderly subjects. Neurobiol Aging 31, 1312-1325
29. Hedden T, Oh H, Younger AP, Patel TA (2013) Metaanalysis of amyloid-cognition relations in cognitively normal older adults. Neurology 80, 1341-1348
30. Moffat SD(2009) Aging and spatial navigation: What do we know and where do we go? Neuropsychol Rev 19, 478-489
31. O'Keefe J, Nadel L (1978) The Hippocampus as aCognitive Map, University Press, Oxford
32. Iaria G, Chen JK, Guariglia C, Ptito A, Petrides M (2007) Retrosplenial and hippocampal brain regions in human navigation: Complementary functional contributions to the formation and use of cognitive maps. Eur J Neurosci 25, 890-899
33. Maguire EA, Burgess N, Donnett JG, Frackowiak RS, Frith CD, O'Keefe J (1998) Knowing where and getting there: A human navigation network. Science 280, 921-924
34. Ohnishi T, Matsuda H, Hirakata M, Ugawa Y (2007) Navigation ability dependent neural activation in the human brain: An fMRI study. Neurosci Res 55, 361-369
35. Bruin JP, Swinkels WA, de Brabander JM (1997) Response learning of rats in a Morris water maze: Involvement of the medial prefrontal cortex. Behav Brain Res 85, 47-55
36. Hartley T, Maguire EA, Spiers HJ, Burgess N (2003) The well-worn route and the path less traveled: Distinct neural bases of route following and wayfinding in humans. Neuron 37, 877-888
37. Iaria G, Petrides M, Dagher A, Pike B, Bohbot VD (2003) Cognitive strategies dependent on the hippocampus and caudate nucleus in human navigation: Variability and change with practice. J Neurosci 23, 5945-5952
38. Kalová E, Vlcek K, Jarolímová E, Bures J (2005) 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, 175-186
39. Laczó J, Andel R, Vlcek K, Macǒska V, Vyhnálek M, Tolar M, Bojar M, Hort J (2011) Spatial navigation and APOE in amnestic mild cognitive impairment. Neurodegener Dis 8, 169-177
40. Hort J, Laczó J, Vyhnálek M, Bojar M, Bures J, Vlcek K (2007) Spatial navigation deficit in amnestic mild cognitive impairment. Proc Natl Acad Sci U S A 104, 4042-4047
41. Cherrier MM, Mendez M, Perryman K (2001) Route learning performance in Alzheimer disease patients. Neuropsychiatry Neuropsychol Behav Neurol 14, 159-168
42. Cushman LA, Stein K, Duffy CJ (2008) Detecting navigational deficits in cognitive aging and Alzheimer disease using virtual reality. Neurology 71, 888-895
43. deIpolyi AR, Rankin KP, Mucke L, Miller BL, Gorno-Tempini ML (2007) Spatial cognition and the human navigation network inADand MCI. Neurology 69, 986-997
44. Lithfous S, Dufour A, Després O (2013) Spatial navigation in normal aging and the prodromal stage of Alzheimer's disease: Insights from imaging and behavioral studies. Ageing Res Rev 12, 201-213
45. Barnes J, Bartlett JW, van Pol LA, Loy CT, Scahill RI, Frost C, Thompson P, Fox NC (2009) A meta-analysis of hippocampal atrophy rates in Alzheimer's disease. Neurobiol Aging 30, 1711-1723
46. Nedelska Z, Andel R, Laczó J, Vlcek K, Horinek D, Lisy J, Sheardova K, Bures J, Hort J (2012) Spatial navigation impairment is proportional to right hippocampal volume. Proc Natl Acad Sci U S A 109, 2590-2594
47. Weniger G, Ruhleder M, Lange C, Wolf S, Irle E (2011) Egocentric and allocentric memory as assessed by virtual reality in individuals with amnestic mild cognitive impairment. Neuropsychologia 49, 518-527
48. Head D, IsomM(2010) Age effects onwayfinding and route learning skills. Behav Brain Res 209, 49-58
49. Morris JC (1993) The Clinical Dementia Rating (CDR): Current version and scoring rules. Neurology 43, 2412-2414
50. McKhann G, Drachman D, Folstein M, Katzman R, Price D, Stadlan EM (1984) Clinical diagnosis of Alzheimer's disease: Report of the NINCDS-ADRDA Work Group under the auspices of Department of Health and Human Services Task Force on Alzheimer's Disease. Neurology 34, 939-944
51. Berg L, McKeel DW, Miller JP, Miller P, Storandt M, Rubin EH, Morris JC, Baty J, Coats M, Northon J, Goate AM, Price JL, Gearing M, Mirra SS, Saunders AM (1998) Clinicopathologic studies in cognitively healthy aging and Alzheimer's disease: Relation of histologic markers to dementia severity, age, sex, and apoE genotype. Arch Neurol 55, 326-335
52. Storandt M, Grant EA, Miller JP, Morris JC (2006) Longitudinal course and neuropathologic outcomes in original and revised MCI and in pre-MCI. Neurology 67, 467-473
53. Gustafson DR, Skoog I, Rosengren L, Zetterberg H, Blennow K (2007) Cerebrospinal fluid beta-amyloid 1-42 concentration may predict cognitive decline in older women. J Neurol Neurosurg Psychiatry 78, 461-464
54. Lewis J, DicksonDW, Lin WL, Chisholm L, Corral A, Jones G,Yen SH, Sahara N, Skipper L,Yager D, Eckman C, Hardy J, Hutton M, McGowan E (2001) Enhanced neurofibrillary degeneration in transgenic mice expressing mutant tau and APP. Science 293, 1487-1491
55. Skoog I, Davidsson P, Aevarsson O, Vanderstichele H, Vanmechelen E, Blennow K (2003) Cerebrospinal fluid beta-amyloid 42 is reduced before the onset of sporadic dementia: A population-based study in 85-year-olds. Dement Geriatr Cogn Disord 15, 169-176
56. Stomrud E, Hansson O, Blennow K, Minthon L, Londos E (2007) Cerebrospinal fluid biomarkers predict decline in subjective cognitive function over 3 years in healthy elderly. Dement Geriatr Cogn Disord 24, 118-124
57. Richardson AE, Montello DR, Hegarty M (1999) Spatial knowledge acquisition from maps and from navigation in real and virtual environments. Mem Cognit 27, 741-750
58. Iaria G, Palermo L, Committeri G, Barton JJS (2009) Age differences in the formation and use of cognitive maps. Beh Brain Res 196, 187-191
59. Cohen J, Cohen P, West S, Aiken L (2003) Applied Multiple Regression/Correlations Analysis for the Behavioral Sciences, Lawrence Erlbaum Associates, Mahwah
60. Holm S (1979) A simple sequentially rejective multiple test procedure. Scand J Statist 6, 65-70
61. Ludbrook J (1998) Multiple comparison procedures updated. Clin Exp Pharm Physiol 25, 1032-1037
62. Grober E, Buschke H, Crystal H, Bang S, Dresner R (1998) Screening for dementia by memory testing. Neurology 38, 900-903
63. Zweig MH, Campbell G (1993) Receiver operating characteristic (ROC) plots: A fundamental evaluation tool in clinical medicine. Clin Chem 39, 561-577
64. DeLong ER, DeLong DM, Clarke-PearsonDL(1998) Comparing the areas under two or more correlated receiver operating characteristic curves: A nonparametric approach. Biometrics 44, 837-845
65. Pike KE, Savage G,Villemagne VL, Ng S, Moss SA, Maruff P, Mathis CA, Klunk WE, Masters CL, Rowe CC (2007) Beta-amyloid imaging and memory in non-demented individuals: Evidence for preclinical Alzheimer's disease. Brain 130, 2837-2844
66. Laczó J, Andel R, Vyhnálek M, Vlcek K, Magerova H, Varjassyova A, Tolar M, Hort J (2010) Human analogue of the Morriswater maze for testing subjects at risk of Alzheimer's disease. Neurodegener Dis 7, 148-152
67. Bellassen V, Iglói K, Souza LC, Dubois B, Rondi-Reig L (2012) Temporal order memory assessed during spatiotemporal navigation as a behavioral cognitive marker for differential Alzheimer's disease diagnosis. J Neurosci 32, 1942-1952
68. Pengas G, Patterson K, Arnold RJ, Bird CM, Burgess N, Nestor PJ (2010) Lost and found: Bespoke memory testing for Alzheimer's disease and semantic dementia. J Alzheimers Dis 21, 1347-1365
69. Shen L, Saykin AJ, Kim S, Firpi HA, West JD, Risacher SL, McDonald BC, McHugh TL, Wishart HA, Flashman LA (2010) Comparison of manual and automated determination of hippocampal volumes in MCI and early AD. Brain Imaging Behav 4, 86-95
70. Minoshima S, Giordani B, Berent S, Frey KA, Foster NL, Kuhl DE (1997) Metabolic reduction in the posterior cingulate cortex in very early Alzheimer's disease. Ann Neurol 42, 85-94
71. Walhovd KB, Fjell AM, Brewer J, McEvoy LK, Fennema-Notestine C, Hagler DJ Jr, Jennings RG, Karow D, Dale AM, Alzheimer's Disease Neuroimaging, Initiative (2010) Combining MR imaging, positron-emission tomography, and CSF biomarkers in the diagnosis and prognosis of Alzheimer disease. AJNR Am J Neuroradiol 31, 347-354
72. Wolbers T, Hegarty M, Büchel C, Loomis JM (2008) Spatial updating: How the brain keeps track of changing object locations during observer motion. Nat Neurosci 11, 1223-1230