Using virtual reality to characterize episodic memory profiles in amnestic mild cognitive impairment and Alzheimer's disease: Influence of active and passive encoding

Neuropsychologia

Volumn 50, Issue 5, 2012, Pages 592-602

  Plancher, G ^a   Tirard, A ^a   Gyselinck, V ^a   Nicolas, S ^a   Piolino, P ^a  

^a UNIVERSITÉ PARIS DESCARTES   (France)

Author keywords

Aging; Dementia; Encoding; Episodic memory; Long term binding; Mild cognitive impairment; Virtual reality

Indexed keywords

ACTIVE MEMORY; AGED; AGING; ALZHEIMER DISEASE; AMNESTIC MILD COGNITIVE IMPAIRMENT; ARTICLE; BRAIN FUNCTION; CLINICAL ARTICLE; CONTROLLED STUDY; DEPRESSION; DISEASE SEVERITY; EPISODIC MEMORY; EXECUTIVE FUNCTION; FEMALE; HUMAN; MALE; MEMORY; MILD COGNITIVE IMPAIRMENT; MINI MENTAL STATE EXAMINATION; NEUROPSYCHOLOGICAL TEST; PASSIVE MEMORY; RECALL; RECOGNITION; SCORING SYSTEM; SEMANTIC MEMORY; SPATIAL MEMORY; TASK PERFORMANCE; VERBAL MEMORY; VIRTUAL REALITY;

AGED; AGED, 80 AND OVER; ALZHEIMER DISEASE; ANALYSIS OF VARIANCE; COMPUTER SIMULATION; FEMALE; HUMANS; MALE; MEMORY DISORDERS; MEMORY, EPISODIC; MENTAL RECALL; MILD COGNITIVE IMPAIRMENT; NEUROPSYCHOLOGICAL TESTS; PSYCHIATRIC STATUS RATING SCALES; REACTION TIME; RECOGNITION (PSYCHOLOGY); USER-COMPUTER INTERFACE;

EID: 84858447093     PISSN: 00283932     EISSN: 18733514     Source Type: Journal    
DOI: 10.1016/j.neuropsychologia.2011.12.013     Document Type: Article

References (111)

1. Aggleton J.P., Brown M. Episodic memory, amnesia, and the hippocampal-anterior thalamic axis. Behavioural Brain Science 1999, 22:425-489.
2. Atienza M., Atalaia-Silva K.C., Gonzalez-Escamilla G., Gil-Neciga E., Suarez-Gonzalez A., Cantero J.L. Associative memory deficits in mild cognitive impairment: The role of hippocampal formation. NeuroImage 2011, 57:1331-1342.
3. Belleville S., Sylvain-Roy S., de Boysson C., Ménard M.C. Characterizing the memory changes in persons with mild cognitive impairment. Progress in Brain Research 2008, 169:365-375.
4. Brooks B.M., Attree E.A., Rose F.D., Clifford B.R., Leadbetter A.G. The specificity of memory enhancement during interaction with a virtual environment. Memory 1999, 7:65-78.
5. Buchner A., Wippich W. Differences and commonalities between implicit learning and implicit memory. Handbook of implicit learning 1998, 3-46. Sage Publications, Thousand Oaks, CA. M.A. Stadler, P.A. Frensch (Eds.).
6. Burgess N., Trinkler I., King J., Kennedy A., Cipolotti L. Impaired allocentric spatial memory underlying topographical disorientation. Reviews in the Neurosciences 2006, 17:239-251.
7. Carassa A., Geminiani G., Morganti F., Varotto D. Active and passive spatial learning in a complex virtual environment: The effect of efficient exploration. Cognitive Processing 2002, 3-4:65-81.
8. Chase T.N., Foster N.L., Fedio P., Brooks R., Mansi L., Di Chiro G. Regional cortical dysfunction in Alzheimer's disease as determined by positron emission tomography. Annals of Neurology 1984, 15:170-174.
9. Clément F., Belleville S., Mellah S. Functional neuroanatomy of the encoding and retrieval processes of verbal episodic memory in MCI. Cortex 2010, 46:1005-1015.
10. Chételat G., Desgranges B., de la Sayette V., Viader F., Eustache F., Baron J.C. Mapping gray matter loss with voxel-based morphometry in mild cognitive impairment. Neuroreport 2002, 13:1939-1943.
11. Chételat G., Desgranges B., Eustache F. Brain profile of hypometabolism in early Alzheimer's disease: Relationships with cognitive deficits and atrophy. Revue de Neurologie 2006, 162:945-951.
12. Chételat G., Villain N., Desgranges B., Eustache F., Baron J.C. Posterior cingulate hypometabolism in early Alzheimer's disease: What is the contribution of local atrophy versus disconnection?. Brain 2009, 132:e133.
13. Clément J.P., Nassif R., Léger J.M., Marchan F. Mise au point et contribution à la validation d'une version française brève de la Geriatric depression scale de Yesavage. L'Encéphale 1997, 23:91-99.
14. Cohen G. Memory in the real world 1989, Erlbaum, Hillsdall.
15. Cohen R.L. On the generality of some memory laws. Scandinavian Journal of Psychology 1981, 22:267-281.
16. Craik F.I.M. On the transfer of information from temporary to permanent memory. Philosophical Transactions of the Royal Society of London 1983, 302:341-359.
17. Craik F.I.M. A functional account of age differences in memory. Human memory and cognitive capabilities, mechanisms and performance 1986, 409-422. Elsevier, New York. F. Klix, H. Hagendorf (Eds.).
18. Craik F.I.M., Moroz T.M., Moscovitch M., Stuss D.T., Winocur G., Tulving E., et al. In search of the self: a positron emission tomography study. Psychological Science 1999, 10:26-34.
19. Detecting navigational deficits in cognitive aging and Alzheimer disease using virtual reality. Neurology 2008, 71:888-895.
20. DeIpolyi R., Rankin K.P., Mucke L., Miller B.L., Gorno-Tempini M.L. Spatial cognition and the human navigation network in AD and MCI. Neurology 2007, 69:986-997.
21. De Leon M., DeSanti S., Zinkowski R., Mehta P., Pratico D., Segal S., et al. Longitudinal CSF and MRI biomarkers improve the diagnosis of mild cognitive impairment. Neurobiology of Aging 2006, 27:394-401.
22. Deltour J.J. Echelle de vocabulaire de Mill Hill de J. C. Raven: Adaptation française et normes comparées du Mill Hill et du Standard progressive matrices (PM 38). Manuel Editions l'Application des Techniques Modernes, Braine-le-Château 1993.
23. Deweer B., Ergis A.M., Fossati P., Pillon B., Boller F., Agid Y., et al. Explicit memory, procedural learning and lexical priming in Alzheimer's disease. Cortex 1994, 30:113-126.
24. Deweer B., Pillon B., Michon A., Dubois B. Mirror reading in Alzheimer's disease: Normal skill learning and acquisition of item-specific information. Journal of Clinical Experimental Neuropsychology 1993, 15:789-804.
25. Dickerson B.C., Goncharova I., Sullivan M.P., Forchetti C., Wilson R.S., Bennett D.A., et al. MRIderived entorhinal and hippocampal atrophy in incipient and very mild Alzheimer's disease. Neurobiology of Aging 2001, 22:747-754.
26. Drzezga A., Grimmer T., Peller M., Wermke M., Siebner H., Rauschecker J.P., et al. Impaired cross-modal inhibition in Alzheimer disease. PLoS Medicine 2005, 2:e288.
27. Dubois B., Albert M.L. Amnestic MCI or prodromal Alzheimer's disease?. Lancet Neurology 2004, 3:246-248.
28. Eichenbaum H. A cortical-hippocampal system for declarative memory. Nature Review Neuroscience 2000, 1:41-50.
29. Evans M.C., Barnes J., Nielsen C., Kim L.G., Clegg S.L., Blair M., et al. Volume changes in Alzheimer's disease and mild cognitive impairment: Cognitive associations. European Radiology 2010, 20:674-682.
30. Farias S.T., Harrell E., Neumann C., Houtz A. The relationship between neuropsychological performance and daily functioning in individuals with Alzheimer's disease: Ecological validity of neuropsychological tests. Archives of Clinical Neuropsychology 2003, 18:655-672.
31. Fischer P., Jungwirth S., Zehetmayer S., Weissgram S., Hoenigschnabl S., Gelpi E., et al. Conversion from subtypes of mild cognitive impairment to Alzheimer dementia. Neurology 2007, 23:288-291.
32. Folstein M.F., Folstein S., McHugh P.R. Mini Mental State: A practical method for grading the cognitive state of patients for the clinician. Journal of Psychiatric Research 1975, 121:189-198.
33. Fowler K.S., Saling M.M., Conway E.L., Semple J.M., Louis W.J. Paired associate performance in the early detection of DAT. Journal of International Neuropsychology Society 2002, 8:58-71.
34. Fox N., Schott J. Imaging cerebral atrophy: Normal ageing to Alzheimer's disease. Lancet 2004, 363:392-394.
35. Gabrieli J.D., Corkin S., Mickel S.F., Growdon J.H. Intact acquisition and long-term retention of mirror-tracing skill in Alzheimer's disease and in global amnesia. Behavioral Neuroscience 1993, 107:899-910.
36. Gardiner J.M. Functional aspects of recollective experience. Memory and Cognition 1988, 16:309-313.
37. Gardiner J.M. Episodic memory and autonoetic consciousness: A first-person approach. Philosophical Transactions of the Royal Society B 2001, 356:1351-1361.
38. Gerardin E., Chételat G., Chupin M., Cuingnet R., Desgranges B., Kim H.S., et al. Multidimensional classification of hippocampal shape features discriminates Alzheimer's disease and mild cognitive impairment from normal aging. NeuroImage 2009, 47:1476-1486.
39. Grady C.L., McIntosh A.R., Beig S., Keightley M.L., Burian H., Black S.E. Evidence from functional neuroimaging of a compensatory prefrontal network in Alzheimer's disease. The Journal of Neuroscience 2003, 23:986-993.
40. Greene J.D.W., Baddeley A.D., Hodges J.R. Analysis of the episodic memory deficit in early Alzheimer's disease: Evidence from the doors and people test. Neuropsychologia 1996, 34:537-551.
41. Grober E., Buschke H. Genuine memory deficits in dementia. Developmental Neuropsychology 1987, 3:13-36.
42. Gutchess A.H., Kensinger E.A., Schacter D.L. Functional neuroimaging of self-referential encoding with age. Neuropsychologia 2010, 48:211-219.
43. Hirono N., Mori E., Ikejiri Y., Imamura T., Shimomura T., Ikeda M., et al. Procedural memory in patients with mild Alzheimer's disease. Dementia and Geriatric Cognitive Disorders 1997, 8:210-216.
44. Hodges J.R. Alzheimer's centennial legacy: Origins, landmarks and the current status of knowledge concerning cognitive aspects. Brain 2006, 129:2811-2822.
45. Hort J., Laczó J., Vyhnalek M., Bojar M., Bures J., Vlcek K. Spatial navigation deficit in amnestic mild cognitive impairment. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:4042-4047.
46. Iachini T., Iavarone A., Senese V.P., Ruotolo F., Ruggiero G. Visuospatial memory in healthy elderly, AD and MCI: A review. Current Aging Science 2009, 2:43-59.
47. Iglói K., Zaoui M., Berthoz A., Rondi-Reig L. Sequential egocentric strategy is acquired as early as allocentric strategy: Parallel acquisition of these two navigation strategies. Hippocampus 2009, 19:1199-1211.
48. Jenkins L.J., Ranganath C. Prefrontal and medial temporal lobe activity at encoding predicts temporal context memory. Journal of Neuroscience 2010, 17:15558-15565.
49. Karlsson T., Backman l., Herlitz A., Nilsson l.G., Winblad B., Osterlind P.O. Memory improvement at different stages of Alzheimer's disease. Neuropsychologia 1989, 27:737-742.
50. Kelley W.M., Macrae C.N., Wyland C., Caglar S., Inati S., Heatherton T.F. Finding the self? An event-related fMRI study. Journal of Cognitive Neuroscience 2002, 14:785-794.
51. Kessels R., Hobbel D., Postma A. Aging, context memory and binding: A comparison of what, where and when in young and older adults. International Journal of Neurosciences 2007, 117:795-810.
52. Lalanne J., Grolleau P., Piolino P. Self-reference effect and episodic memory in normal aging and Alzheimer's disease: Myth or reality?. Psychologie & Neuropsychiatrie du Vieillissement 2010, 8:277-294.
53. 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. Behavioural Brain Research 2009, 202:252-259.
54. Lekeu F., Van der Linden M., Moonen G., Salmon E. Exploring the effect of action familiarity on SPTs recall performance in Alzheimer's disease. Journal of Clinical Experimental Neuropsychology 2002, 24:1057-1069.
55. Lenzi D., Serra L., Perri R., Pantano P., Lenzi G.L., Paulesu E., et al. Single domain amnestic MCI: A multiple cognitive domains fMRI investigation. Neurobiology of Aging 2011, 32:1542-1557.
56. Lezak M.D., Howieson D.B., Loring D.W. Neuropsychological assessment 2004, Oxford University Press, Oxford, England. 4th ed.
57. Lipinska B., Backman L. Encoding-retrieval interactions in mild Alzheimer's disease: The role of access to categorical information. Brain and Cognition 1997, 34:274-286.
58. Luo L., Craik F.I.M. Aging and memory: A cognitive approach. Canadian Journal of Psychiatry 2008, 53:346-353.
59. Mäntylä T. Knowing but not remembering: Adult age differences in recollective experience. Memory & Cognition 1993, 21:379-388.
60. Martinelli, P., Sperduti, M., & Piolino, P. (in press). Neural substrates of the self-memory system: New insights from a meta-analysis. Human Brain Mapping, doi:10.1002/hbm.22008.
61. Mayes A.R. Human organic memory disorders 1988, Cambridge University Press, Cambridge.
62. McKahnn G., Drachman D., Folstein M., Katzman R., Price D., Stadlan E.M. 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 1984, 34:934-939.
63. McNair D., Kahn R. Self-assessment of cognitive deficits. Assessment in geriatric psychopharmacology 1983, 137-143. Powley, New Canaan, CT. T. Crook, S. Ferris, R. Bartus (Eds.).
64. Naveh-Benjamin M., Craik F.I.M., Ben-Shaul L. Age-related differences in cued recall: Effects of support at encoding and retrieval. Aging, Neuropsychology, and Cognition 2002, 9:276-287.
65. Nilsson L.G., Nyberg L., Klingberg T., Åberg C., Persson J., Roland P. Activity in motor areas while remembering action events. NeuroReport 2000, 11:2199-2201.
66. Nyberg L., Petersson K.M., Nilsson L.G., Sandblom J., Aberg C., Ingvar M. Reactivation of motor brain areas during explicit memory for actions. NeuroImage 2001, 14:521-528.
67. Park D.C., Puglisi J.T., Smith A.D. Memory for pictures: Does an age-related decline exist?. Psychology and Aging 1986, 1:11-17.
68. Park D.C., Smith A.D., Morell R.W., Puglisi J.T., Dudley W.N. Effects of contextual integration on recall of pictures by older adults. Journal of Gerontology: Psychological Sciences 1990, 45:52-57.
69. Pennartz C.M., Ito R., Verschure P.F., Battaglia F.P., Robbins T.W. The hippocampal-striatal axis in learning, prediction and goal-directed behavior. Trends in Neurosciences 2011, 34:548-559.
70. Perani D., Bressi S., Cappa S.F., Vallar G., Alberoni M., Grassi F., et al. Evidence of multiple memory systems in the human brain. A [18F] FDG PET metabolic study. Brain 1993, 116:903-919.
71. Perri R., Carlesimo G.A., Serra L., Caltagirone C. Early diagnosis group of the Italian interdisciplinary network on Alzheimer's disease. Characterisation of memory profile in subjects with mild cognitive impairment. Journal of Clinical and Experimental Neuropsychology 2005, 27:1033-1055.
72. Perri R., Serra L., Carlesimo G.A., Caltagirone C. Italian interdisciplinary network on Alzheimer's disease, early diagnosis group. Neuropsychology 2007, 21:549-558.
73. Petersen R.C., Doody R., Kurz A., Mohs R.C., Morris J.C., Rabins P.V., et al. Current concepts in mild cognitive impairment. Archives of Neurology 2001, 58:1985-1992.
74. Petersen R.C., Smith G.E., Waring S.C., Ivnik R.J., Tangalos E.G., Kokmen E. Mild cognitive impairment: Clinical characterization and outcome. Archives of Neurology 1999, 56:303-308.
75. Piolino P., Desgranges B., Eustache F. Episodic autobiographical memory over the course of time: Cognitive, neuropsychological and neuroimaging findings. Neuropsychologia 2009, 47:2314-2329.
76. Plancher G., Guyard A., Nicolas S., Piolino P. Mechanisms underlying the production of false memories for famous people's names in aging and Alzheimer's disease. Neuropsychologia 2009, 47:2527-2536.
77. Plancher G., Gyselinck V., Nicolas S., Piolino P. Age effect on components of episodic memory and feature binding: A virtual reality study. Neuropsychology 2010, 24:379-390.
78. Plancher G., Nicolas S., Piolino P. Contribution of virtual reality for neuropsychology of memory: Study in ageing. Psychologie et NeuroPsychiatrie du vieillissement 2008, 6:7-22.
79. Putzke J.D., Rickert E.J., Duke L.W., Marson D., Harrell L. Differential automatic processing deficits in early stage Alzheimer's disease. Aging, Neuropsychology and Cognition 2000, 7:112-118.
80. Rabinowitz J.C., Craik F.I.M. Specific enhancement effects associated with word generation. Journal of Memory and Language 1986, 25:226-237.
81. Risacher S.L., Saykin A.J., West J.D., Shen L., Firpi H.A., McDonald B.C. Baseline MRI predictors of conversion from MCI to probable AD in the ADNI cohort. Current Alzheimer Research 2009, 6:347-361.
82. Rösler A., Seifritz E., Kräuchi K., Spoerl D., Brokuslaus I., Proserpi S-M., et al. Skill learning in patients with moderate Alzheimer's disease: A prospective pilot-study of waltz-lessons. International Journal of Geriatric Psychiatry 2002, 17:1155-1156.
83. Ruby P., Collette F., D'Argembeau A.D., Péters F., Degueldre C., Balteau E., et al. Perspective taking to assess self-personality: What's modified in Alzheimer's disease?. Neurobiology of Aging 2009, 30:1637-1651.
84. Salmon D.P., Bondi M.W. Neuropsychological assessment of dementia. Annual Review of Psychology 2009, 60:257-282.
85. Schacter D.L., Israel L., Racine C. Suppressing false recognition in younger and older adults: The distinctiveness heuristic. Journal of Memory and Language 1999, 40:1-24.
86. Schultheis M.T., Himelstein J., Rizzo A.A. Virtual reality and neuropsychology: Upgrading the current tools. Journal of Head Trauma Rehabilitation 2002, 17:379-394.
87. Serra L., Bozzali M., Cercignani M., Perri R., Fadda L., Caltagirone C., et al. Recollection and familiarity in amnesic mild cognitive impairment. Neuropsychology 2010, 24:316-326.
88. Slotnick S.D. Does the hippocampus mediate objective binding or subjective remembering?. NeuroImage 2010, 49:1769-1776.
89. Spaan P.E., Raaijmakers J.G., Jonker C. Alzheimer's disease versus normal ageing: A review of the efficiency of clinical and experimental memory measures. Journal of Clinical Experimental Neuropsychology 2003, 25:216-233.
90. Squire L.R. Memory systems of the brain: A brief history and current perspective. Neurobiology of Learning and Memory 2004, 82:171-177.
91. Stroop J.R. Studies of interference in serial verbal reactions. Journal of Experimental Psychology 1935, 18:643-662.
92. Swainson R., Hodges J.R., Galton C.J., Semple J., Michael A., Dunn B.D., et al. Early detection and differential diagnosis of Alzheimer's disease and depression with neuropsychological tasks. Dementia and Geriatric Cognitive Disorders 2001, 12:265-280.
93. Troyer A.K., Murphy K.J., Anderson N.D., Hayman-Abello B.A., Craik F.I., Moscovitch M. Item and associative memory in amnestic mild cognitive impairment: Performance on standardized memory tests. Neuropsychology 2008, 22:10-16.
94. Tulving E. Elements of episodic memory 1983, Oxford University Press, New York.
95. Tulving E. Memory and consciousness. Canadian Psychologist 1985, 26:1-12.
96. Tulving E. Episodic memory: From mind to brain. Annual Review of Psychology 2002, 53:1-25.
97. Tulving E., Thomson D.M. Encoding specificity and retrieval processes in semantic memory. Psychological Review 1973, 80:352-373.
98. Van Halteren-van Tilborg I.A., Scherder E.J., Hulstijn W. Motor-skill learning in Alzheimer's disease: A review with an eye to the clinical practice. Neuropsychology Review 2007, 3:203-212.
99. Wechsler D. Wechsler Adult Intelligence Scale - Third Edition (WAIS III) 2001, EAP, Paris (French version).
100. 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 2011, 49:518-527.
101. Westerberg C.E., Paller K.E., Holdstock J.S., Mayes A.R., Reber P.J. When memory does not fail: Familiarity-based recognition in mild cognitive impairment and Alzheimer's disease. Neuropsychology 2006, 20:193-205.
102. Widmann C.N., Beinhoff U., Riepe M.W. Everyday memory deficits in very mild Alzheimer's disease. Neurobiology of Aging 2012, 33:297-303.
103. Wojtasik V., Olivier C., Lekeu F., Quittre A., Adam S., Salmon E. A grid for a precise analysis of daily activities. Neuropsychological Rehabilitation 2010, 20:120-136.
104. Wolf H., Jelic V., Gertz H.J., Nordberg A., Julin P., Wahlund L.O. A critical discussion of the role of neuroimaging in mild cognitive impairment. Acta Neurologica Scandinavica 2003, 107:52-76.
105. Yesavage J.A. Geriatric depression scale. Psychopharmacology Bulletin 1988, 24:709-711.
106. Yonelinas A.P. The nature of recollection and familiarity: A review of 30 years of research. Journal of Memory and Language 2002, 46:441-517.
107. Yonelinas A.P., Aly M., Wang W.C., Koen J.D. Recollection and familiarity: Examining controversial assumptions and new directions. Hippocampus 2010, 20:1178-1194.
108. Yonelinas A.P., Jacoby L.L. The relation between remembering and knowing as bases for recognition: Effects of size congruency. Journal of Memory and Language 1995, 34:622-643.
109. Yonelinas A.P., Kroll N.E., Dobbins I., Lazzara M., Knight R.T. Recollection and familiarity deficits in amnesia: Convergence of remember-know, process dissociation, and receiver operating characteristic data. Neuropsychology 1998, 12:323-339.
110. Zakzanis K.K., Quintin G., Graham S.J., Mraz R. Age and dementia related differences in spatial navigation within an immersive virtual environment. Medical Science Monitor: International Medical Journal of Experimental and Clinical Research 2009, 15:140-150.
111. Zanetti O., Zanieri G., Di Giovanni G., De Vreese L.P., Pezzini A., Metitieri T., et al. Effectiveness of procedural memory stimulation in mild Alzheimer's disease patients: A controlled study. Neuropsychological Rehabilitation 2001, 11:263-272.