Spatial navigation in normal aging and the prodromal stage of Alzheimer's disease: Insights from imaging and behavioral studies

Ageing Research Reviews

Volumn 12, Issue 1, 2013, Pages 201-213

  Lithfous, Ségolène ^a   Dufour, André ^a   Després, Olivier ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

Author keywords

AD; Behavioral studies; Imaging; MCI; MRI; Normal aging; Spatial navigation

Indexed keywords

AMYLOID PRECURSOR PROTEIN; APOLIPOPROTEIN E4; NEUROTRANSMITTER; PRESENILIN 1; PRESENILIN 2;

AGING; ALZHEIMER DISEASE; CAUDATE NUCLEUS; COGNITION; CORPUS STRIATUM; DEGENERATIVE DISEASE; DEMENTIA; DISEASE COURSE; ELECTROENCEPHALOGRAPHY; FRACTIONAL ANISOTROPY; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUNCTIONAL NEUROIMAGING; GRAY MATTER; HIGH RISK POPULATION; HIPPOCAMPUS; HISTOPATHOLOGY; HUMAN; LONGITUDINAL STUDY; MEMORY; NEURONAVIGATION; NEUROPSYCHOLOGY; PARIETAL CORTEX; POSTERIOR PARIETAL CORTEX; PROTEIN EXPRESSION; REVIEW; RISK FACTOR; SPATIAL MEMORY; SUPERIOR TEMPORAL GYRUS; TASK PERFORMANCE; TEMPORAL LOBE; VISUAL CORTEX; WORKING MEMORY;

AGING; ALZHEIMER DISEASE; ANIMALS; BRAIN; DISEASE PROGRESSION; HUMANS; MICE; MILD COGNITIVE IMPAIRMENT; NEUROIMAGING; PRODROMAL SYMPTOMS; RATS; SPACE PERCEPTION;

EID: 84867346155     PISSN: 15681637     EISSN: 18729649     Source Type: Journal    
DOI: 10.1016/j.arr.2012.04.007     Document Type: Review

References (110)

1. Aguirre G.K., Detre J.A., Alsop D.C., D'Esposito M. The parahippocampus subserves topographical learning in man. Cerebral Cortex 1996, 6:823-829.
2. Barnes C.A., McNaughton B.L., O'Keefe J. Loss of place specificity in hippocampal complex spike cells of senescent rat. Neurobiology of Aging 1983, 4:113-119.
3. Barnes C.A., Nadel L., Honig W.K. Spatial memory deficit in senescent rats. Canadian Journal of Psychology 1980, 34:29-39.
4. Barrash J. Age-related decline in route learning ability. Developmental Neuropsychology 1994, 10:189-191.
5. Bartus R.T., Dean R.L., Beer B., Lippa A.S. The cholinergic hypothesis of geriatric memory dysfunction. Science (New York, N.Y.) 1982, 217:408-414.
6. Benson D.F., Davis R.J., Snyder B.D. Posterior cortical atrophy. Archives of Neurology 1988, 45:789-793.
7. Bird C.M., Chan D., Hartley T., Pijnenburg Y.A., Rossor M.N., Burgess N. Topographical short-term memory differentiates Alzheimer's disease from frontotemporal lobar degeneration. Hippocampus 2010, 20:1154-1169.
8. Bohbot V.D., Lerch J., Thorndycraft B., Iaria G., Zijdenbos A.P. Gray matter differences correlate with spontaneous strategies in a human virtual navigation task. Journal of Neuroscience 2007, 27:10078-10083.
9. Braak H., Braak E. Neuropathological staging of Alzheimer-related changes. Acta Neuropathologica 1991, 82:239-259.
10. Braak H., Braak E. Evolution of the neuropathology of Alzheimer's disease. Acta Neurologica Scandinavica 1996, 165:3-12.
11. Burgess N., Maguire E.A., O'Keefe J. The human hippocampus and spatial and episodic memory. Neuron 2002, 35:625-641.
12. Burns P.C. Navigation and the mobility of older drivers. The Journal of Gerontology 1999, 54:S49-S55.
13. Cacucci F., Yi M., Wills T.J., Chapman P., O'Keefe J. Place cell firing correlates with memory deficits and amyloid plaque burden in Tg2576 Alzheimer mouse model. Proceedings of the National Academy of Sciences of the United States of America 2008, 105:7863-7868.
14. Cherrier M.M., Mendez M., Perryman K. Route learning performance in Alzheimer disease patients. Neuropsychiatry, Neuropsychology, and Behavioral Neurology 2001, 14:159-168.
15. Chishti M.A., Yang D.S., Janus C., Phinney A.L., Horne P., Pearson J., Strome R., Zuker N., Loukides J., French J., Turner S., Lozza G., Grilli M., Kunicki S., Morissette C., Paquette J., Gervais F., Bergeron C., Fraser P.E., Carlson G.A., George-Hyslop P.S., Westaway D. Early-onset amyloid deposition and cognitive deficits in transgenic mice expressing a double mutant form of amyloid precursor protein 695. The Journal of Biological Chemistry 2001, 276:21562-21570.
16. Cushman L.A., Stein K., Duffy C.J. Detecting navigational deficits in cognitive aging and Alzheimer disease using virtual reality. Neurology 2008, 71:888-895.
17. de Bruin J.P., Moita M.P., de Brabander H.M., Joosten R.N. Place and response learning of rats in a Morris water maze: differential effects of fimbria fornix and medial prefrontal cortex lesions. Neurobiology of Learning and Memory 2001, 75:164-178.
18. De Leonibus E., Oliverio A., Mele A. A study on the role of the dorsal striatum and the nucleus accumbens in allocentric and egocentric spatial memory consolidation. Learning and Memory (Cold Spring Harbor, N.Y.) 2005, 12:491-503.
19. deIpolyi A.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.
20. deJong B.M., Shipp S., Skidmore B., Frackowiak R.S., Zeki S. The cerebral activity related to the visual perception of forward motion in depth. Brain 1994, 117:1039-1054.
21. Delacourte A., David J.P., Sergeant N., Buee L., Wattez A., Vermersch P., Ghozali F., Fallet-Bianco C., Pasquier F., Lebert F., Petit H., Di Menza C. The biochemical pathway of neurofibrillary degeneration in aging and Alzheimer's disease. Neurology 1999, 52:1158-1165.
22. Epstein R., Kanwisher N. A cortical representation of the local visual environment. Nature 1998, 392:598-601.
23. Epstein R.A., Higgins J.S., Jablonski K., Feiler A.M. Visual scene processing in familiar and unfamiliar environments. Journal of Neurophysiology 2007, 97:3670-3683.
24. Epstein R.A., Parker W.E., Feiler A.M. Where am I now? Distinct roles for parahippocampal and retrosplenial cortices in place recognition. Journal of Neuroscience 2007, 27:6141-6149.
25. Everitt B.J., Robbins T.W. Central cholinergic systems and cognition. Annual Review of Psychology 1997, 48:649-684.
26. Galati G., Committeri G., Sanes J.N., Pizzamiglio L. Spatial coding of visual and somatic sensory information in body-centred coordinates. The European Journal of Neuroscience 2001, 14:737-746.
27. Galati G., Lobel E., Vallar G., Berthoz A., Pizzamiglio L., Le Bihan D. The neural basis of egocentric and allocentric coding of space in humans: a functional magnetic resonance study. Experimental Brain Research. Experimentelle Hirnforschung 2000, 133:156-164.
28. Gramann K., Muller H.J., Schonebeck B., Debus G. The neural basis of ego- and allocentric reference frames in spatial navigation: evidence from spatio-temporal coupled current density reconstruction. Brain Research 2006, 1118:116-129.
29. Gramann K., Onton J., Riccobon D., Mueller H.J., Bardins S., Makeig S. Human brain dynamics accompanying use of egocentric and allocentric reference frames during navigation. Journal of Cognitive Neuroscience 2010, 22:2836-2849.
30. Greenlee M.W. Human cortical areas underlying the perception of optic flow: brain imaging studies. International Review of Neurobiology 2000, 44:269-292.
31. Gron G., Brandenburg I., Wunderlich A.P., Riepe M.W. Inhibition of hippocampal function in mild cognitive impairment: targeting the cholinergic hypothesis. Neurobiology of Aging 2006, 27:78-87.
32. Gron G., Wunderlich A.P., Spitzer M., Tomczak R., Riepe M.W. Brain activation during human navigation: gender-different neural networks as substrate of performance. Nature Neuroscience 2000, 3:404-408.
33. Hartley T., Maguire E.A., Spiers H.J., Burgess N. The well-worn route and the path less traveled: distinct neural bases of route following and wayfinding in humans. Neuron 2003, 37:877-888.
34. Head D., Isom M. Age effects on wayfinding and route learning skills. Behavioural Brain Research 2010, 209:49-58.
35. Hillis A.E., Newhart M., Heidler J., Barker P.B., Herskovits E.H., Degaonkar M. Anatomy of spatial attention: insights from perfusion imaging and hemispatial neglect in acute stroke. Journal of Neuroscience 2005, 25:3161-3167.
36. Hof P.R., Vogt B.A., Bouras C., Morrison J.H. Atypical form of Alzheimer's disease with prominent posterior cortical atrophy: a review of lesion distribution and circuit disconnection in cortical visual pathways. Vision Research 1997, 37:3609-3625.
37. Hort J., Laczo 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.
38. Iachini I., 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.
39. Iachini T., Poderico C., Ruggiero G., Iavarone A. Age differences in mental scanning of locomotor maps. Disability and Rehabilitation 2005, 27:741-752.
40. Iachini T., Ruggiero G., Conson M., Trojano L. Lateralization of egocentric and allocentric spatial processing after parietal brain lesions. Brain and Cognition 2009, 69:514-520.
41. Iaria G., Chen J.K., Guariglia C., Ptito A., Petrides M. Retrosplenial and hippocampal brain regions in human navigation: complementary functional contributions to the formation and use of cognitive maps. The European Journal of Neuroscience 2007, 25:890-899.
42. Iaria G., Lanyon L.J., Fox C.J., Giaschi D., Barton J.J. Navigational skills correlate with hippocampal fractional anisotropy in humans. Hippocampus 2008, 18:335-339.
43. Iaria G., Palermo L., Committeri G., Barton J.J. Age differences in the formation and use of cognitive maps. Behavioural Brain Research 2009, 196:187-191.
44. Iaria G., Petrides M., Dagher A., Pike B., Bohbot V.D. Cognitive strategies dependent on the hippocampus and caudate nucleus in human navigation: variability and change with practice. Journal of Neuroscience 2003, 23:5945-5952.
45. Kalova E., Vlcek K., Jarolimova 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. Behavioural Brain Research 2005, 159:175-186.
46. Kavcic V., Fernandez R., Logan D., Duffy C.J. Neurophysiological and perceptual correlates of navigational impairment in Alzheimer's disease. Brain 2006, 129:736-746.
47. Kearns M.J., Warren W.H., Duchon A.P., Tarr M.J. Path integration from optic flow and body senses in a homing task. Perception 2002, 31:349-374.
48. Kessels R.P., van Doormaal A., Janzen G. Landmark recognition in Alzheimer's dementia: spared implicit memory for objects relevant for navigation. PLoS One 2011, 6:e18611.
49. Kirasic K.C. Spatial cognition and behavior in young and elderly adults: implications for learning new environments. Psychology and Aging 1991, 6:10-18.
50. Konishi S., Uchida I., Okuaki T., Machida T., Shirouzu I., Miyashita Y. Neural correlates of recency judgment. Journal of Neuroscience 2002, 22:9549-9555.
51. Laczo J., Andel R., Vlcek K., Macoska V., Vyhnalek M., Tolar M., Bojar M., Hort J. Spatial navigation and APOE in amnestic mild cognitive impairment. Neuro-degenerative Diseases 2011, 8:169-177.
52. Laczo J., Andel R., Vyhnalek M., Vlcek K., Magerova H., Varjassyova A., Tolar M., Hort J. Human analogue of the Morris water maze for testing subjects at risk of Alzheimer's disease. Neuro-degenerative Diseases 2010, 7:148-152.
53. Laczo J., Vlcek K., Vyhnalek M., Vajnerova O., Ort M., Holmerova I., Tolar M., Andel R., Bojar M., Hort J. Spatial navigation testing discriminates two types of amnestic mild cognitive impairment. Behavioural Brain Research 2009, 202:252-259.
54. Latini-Corazzini L., Nesa M.P., Ceccaldi M., Guedj E., Thinus-Blanc C., Cauda F., Dagata F., Peruch P. Route and survey processing of topographical memory during navigation. Psychological Research 2010, 74:545-559.
55. Lecourtier L., de Vasconcelos A.P., Leroux E., Cosquer B., Geiger K., Lithfous S., Cassel J.C. Septohippocampal pathways contribute to system consolidation of a spatial memory: sequential implication of GABAergic and cholinergic neurons. Hippocampus 2011, 21:1277-1289.
56. Lim T.S., Iaria G., Moon S.Y. Topographical disorientation in mild cognitive impairment: a voxel-based morphometry study. Journal of Clinical Neurology (Seoul, Korea) 2010, 6:204-211.
57. Loomis J.M., Klatzky R.L., Golledge R.G., Cicinelli J.G., Pellegrino J.W., Fry P.A. Nonvisual navigation by blind and sighted: assessment of path integration ability. Journal of Experimental Psychology 1993, 122:73-91.
58. Lovden M., Schaefer S., Noack H., Bodammer N.C., Kuhn S., Heinze H.J., Duzel E., Backman L., Lindenberger U. Spatial navigation training protects the hippocampus against age-related changes during early and late adulthood. Neurobiology of Aging 2011, 33:620.e9-620.e22.
59. Maguire E.A. The retrosplenial contribution to human navigation: a review of lesion and neuroimaging findings. Scandinavian Journal of Psychology 2001, 42:225-238.
60. Maguire E.A., Burgess N., Donnett J.G., Frackowiak R.S., Frith C.D., O'Keefe J. Knowing where and getting there: a human navigation network. Science (New York, N.Y.) 1998, 280:921-924.
61. Maguire E.A., Gadian D.G., Johnsrude I.S., Good C.D., Ashburner J., Frackowiak R.S., Frith C.D. Navigation-related structural change in the hippocampi of taxi drivers. Proceedings of the National Academy of Sciences of the United States of America 2000, 97:4398-4403.
62. Maguire E.A., Woollett K., Spiers H.J. London taxi drivers and bus drivers: a structural MRI and neuropsychological analysis. Hippocampus 2006, 16:1091-1101.
63. Mahmood O., Adamo D., Briceno E., Moffat S.D. Age differences in visual path integration. Behavioural Brain Research 2009, 205:88-95.
64. Mapstone M., Steffenella T.M., Duffy C.J. A visuospatial variant of mild cognitive impairment: getting lost between aging and AD. Neurology 2003, 60:802-808.
65. Marsh E.B., Hillis A.E. Dissociation between egocentric and allocentric visuospatial and tactile neglect in acute stroke. Cortex: A Journal Devoted to the Study of the Nervous System and Behavior 2008, 44:1215-1220.
66. McDonald R.J., White N.M. Parallel information processing in the water maze: evidence for independent memory systems involving dorsal striatum and hippocampus. Behavioral and Neural Biology 1994, 61:260-270.
67. McKhann 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 Department of Health and Human Services Task Force on Alzheimer's Disease. Neurology 1984, 34:939-944.
68. Medina J., Kannan V., Pawlak M.A., Kleinman J.T., Newhart M., Davis C., Heidler-Gary J.E., Herskovits E.H., Hillis A.E. Neural substrates of visuospatial processing in distinct reference frames: evidence from unilateral spatial neglect. Journal of Cognitive Neuroscience 2009, 21:2073-2084.
69. Moffat S.D. Aging and spatial navigation: what do we know and where do we go?. Neuropsychology Review 2009, 19:478-489.
70. Moffat S.D., Elkins W., Resnick S.M. Age differences in the neural systems supporting human allocentric spatial navigation. Neurobiology of Aging 2006, 27:965-972.
71. Moffat S.D., Kennedy K.M., Rodrigue K.M., Raz N. Extrahippocampal contributions to age differences in human spatial navigation. Cerebral Cortex 2007, 17:1274-1282.
72. Moffat S.D., Resnick S.M. Effects of age on virtual environment place navigation and allocentric cognitive mapping. Behavioral Neuroscience 2002, 116:851-859.
73. Moffat S.D., Zonderman A.B., Resnick S.M. Age differences in spatial memory in a virtual environment navigation task. Neurobiology of Aging 2001, 22:787-796.
74. Monacelli A.M., Cushman L.A., Kavcic V., Duffy C.J. Spatial disorientation in Alzheimer's disease: the remembrance of things passed. Neurology 2003, 61:1491-1497.
75. Morris R.G., Garrud P., Rawlins J.N., O'Keefe J. Place navigation impaired in rats with hippocampal lesions. Nature 1982, 297:681-683.
76. O'Brien H.L., Tetewsky S.J., Avery L.M., Cushman L.A., Makous W., Duffy C.J. Visual mechanisms of spatial disorientation in Alzheimer's disease. Cerebral Cortex 2001, 11:1083-1092.
77. O'Keefe J., Nadel L. The Hippocampus as a Cognitive Map 1978, Oxford University Press, Oxford.
78. O'Leary T.P., Brown R.E. Visuo-spatial learning and memory deficits on the Barnes maze in the 16-month-old APPswe/PS1dE9 mouse model of Alzheimer's disease. Behavioural Brain Research 2009, 201:120-127.
79. Packard M.G., McGaugh J.L. Inactivation of hippocampus or caudate nucleus with lidocaine differentially affects expression of place and response learning. Neurobiology of Learning and Memory 1996, 65:65-72.
80. Pai M.C., Jacobs W.J. Topographical disorientation in community-residing patients with Alzheimer's disease. International Journal of Geriatric Psychiatry 2004, 19:250-255.
81. Park D.C. Basic mechanisms accounting for age-related decline in cognitive functions. Cognitive Aging: A Primer 2000, Psychology, Philadelphia. D.C. Park, N. Schwarz (Eds.).
82. Petersen R.C. Mild cognitive impairment clinical trials. Nature Reviews 2003, 2:646-653.
83. Petersen R.C., Doody R., Kurz A., Mohs R.C., Morris J.C., Rabins P.V., Ritchie K., Rossor M., Thal L., Winblad B. Current concepts in mild cognitive impairment. Archives of Neurology 2001, 58:1985-1992.
84. 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.
85. Pietrini P., Furey M.L., Graff-Radford N., Freo U., Alexander G.E., Grady C.L., Dani A., Mentis M.J., Schapiro M.B. Preferential metabolic involvement of visual cortical areas in a subtype of Alzheimer's disease: clinical implications. The American Journal of Psychiatry 1996, 153:1261-1268.
86. Raz N., Gunning-Dixon F., Head D., Rodrigue K.M., Williamson A., Acker J.D. Aging, sexual dimorphism, and hemispheric asymmetry of the cerebral cortex: replicability of regional differences in volume. Neurobiology of Aging 2004, 25:377-396.
87. Raz N., Rodrigue K.M., Kennedy K.M., Head D., Gunning-Dixon F., Acker J.D. Differential aging of the human striatum: longitudinal evidence. AJNR: American Journal of Neuroradiology 2003, 24:1849-1856.
88. Reiman E.M., Chen K., Alexander G.E., Caselli R.J., Bandy D., Osborne D., Saunders A.M., Hardy J. Functional brain abnormalities in young adults at genetic risk for late-onset Alzheimer's dementia. Proceedings of the National Academy of Sciences of the United States of America 2004, 101:284-289.
89. Reiserer R.S., Harrison F.E., Syverud D.C., McDonald M.P. Impaired spatial learning in the APPSwe+PSEN1DeltaE9 bigenic mouse model of Alzheimer's disease. Genes, Brain, and Behavior 2007, 6:54-65.
90. Salthouse T.A. General and specific speed mediation of adult age differences in memory. The Journal of Gerontology 1996, 51:30-42.
91. Sanders A.E., Holtzer R., Lipton R.B., Hall C., Verghese J. Egocentric and exocentric navigation skills in older adults. Journals of Gerontology. Series A, Biological Sciences and Medical Sciences 2008, 63:1356-1363.
92. Scoville W.B., Milner B. Loss of recent memory after bilateral hippocampal lesions. Journal of Neurology, Neurosurgery, and Psychiatry 1957, 20:11-21.
93. Shelton A.L., Gabrieli J.D. Neural correlates of encoding space from route and survey perspectives. Journal of Neuroscience 2002, 22:2711-2717.
94. Suzuki W.A., Amaral D.G. Topographic organization of the reciprocal connections between the monkey entorhinal cortex and the perirhinal and parahippocampal cortices. Journal of Neuroscience 1994, 14:1856-1877.
95. Tang-Wai D.F., Graff-Radford N.R., Boeve B.F., Dickson D.W., Parisi J.E., Crook R., Caselli R.J., Knopman D.S., Petersen R.C. Clinical, genetic, and neuropathologic characteristics of posterior cortical atrophy. Neurology 2004, 63:1168-1174.
96. Tetewsky S.J., Duffy C.J. Visual loss and getting lost in Alzheimer's disease. Neurology 1999, 52:958-965.
97. Tolman E.C. Cognitive maps in rats and men. Psychological Review 1948, 55:189-208.
98. Vallar G., Bottini G., Paulesu E. Neglect syndromes: the role of the parietal cortex. Advances in Neurology 2003, 93:293-319.
99. Walker J.M., Fowler S.W., Miller D.K., Sun A.Y., Weisman G.A., Wood W.G., Sun G.Y., Simonyi A., Schachtman T.R. Spatial learning and memory impairment and increased locomotion in a transgenic amyloid precursor protein mouse model of Alzheimer's disease. Behavioural Brain Research 2011, 222:169-175.
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. Whitehouse P.J., Price D.L., Struble R.G., Clark A.W., Coyle J.T., Delon M.R. Alzheimer's disease and senile dementia: loss of neurons in the basal forebrain. Science (New York, N.Y.) 1982, 215:1237-1239.
102. Whitwell J.L. Progression of atrophy in Alzheimer's disease and related disorders. Neurotoxicity Research 2010, 18:339-346.
103. Whitwell J.L., Przybelski S.A., Weigand S.D., Knopman D.S., Boeve B.F., Petersen R.C., Jack C.R. 3D maps from multiple MRI illustrate changing atrophy patterns as subjects progress from mild cognitive impairment to Alzheimer's disease. Brain 2007, 130:1777-1786.
104. Wilkniss S.M., Jones M.G., Korol D.L., Gold P.E., Manning C.A. Age-related differences in an ecologically based study of route learning. Psychology and Aging 1997, 12:372-375.
105. Wolbers T., Buchel C. Dissociable retrosplenial and hippocampal contributions to successful formation of survey representations. Journal of Neuroscience 2005, 25:3333-3340.
106. Wolbers T., Weiller C., Buchel C. Neural foundations of emerging route knowledge in complex spatial environments. Brain Research 2004, 21:401-411.
107. Wolbers T., Wiener J.M., Mallot H.A., Buchel C. Differential recruitment of the hippocampus, medial prefrontal cortex, and the human motion complex during path integration in humans. Journal of Neuroscience 2007, 27:9408-9416.
108. Yaffe K., Petersen R.C., Lindquist K., Kramer J., Miller B. Subtype of mild cognitive impairment and progression to dementia and death. Dementia and Geriatric Cognitive Disorders 2006, 22:312-319.
109. Yassa M.A., Lacy J.W., Stark S.M., Albert M.S., Gallagher M., Stark C.E. Pattern separation deficits associated with increased hippocampal CA3 and dentate gyrus activity in nondemented older adults. Hippocampus 2010, 21:968-979.
110. Yassa M.A., Mattfeld A.T., Stark S.M., Stark C.E. Age-related memory deficits linked to circuit-specific disruptions in the hippocampus. Proceedings of the National Academy of Sciences of the United States of America 2011, 108:8873-8878.