Hippocampal dysfunction in patients with mild cognitive impairment: A functional neuroimaging study of a visuospatial paired associates learning task

Neuropsychologia

Volumn 49, Issue 7, 2011, Pages 2060-2070

  De Rover, Mischa ^a,b,e   Pironti, Valentino A ^a   McCabe, Jonathan A ^a   Acosta Cabronero, Julio ^c   Arana, F Sergio ^a   Morein Zamir, Sharon ^a   Hodges, John R ^c,d,f   Robbins, Trevor W ^a,b   Fletcher, Paul C ^a   Nestor, Peter J ^c   Sahakian, Barbara J ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UK   (United Kingdom)

^c ADDENBROOKE S HOSPITAL   (United Kingdom)

^d MRC COGNITION AND BRAIN SCIENCES UNIT   (United Kingdom)

^e LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^f UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

Biomarkers; FMRI; Hippocampus; Humans; MCI; Paired associates learning

Indexed keywords

ADULT; AGED; ALZHEIMER DISEASE; ARTICLE; BOLD SIGNAL; BRAIN DYSFUNCTION; CAMBRIDGE NEUROPSYCHOLOGICAL TEST AUTOMATED BATTERY; CINGULATE GYRUS; CLINICAL ARTICLE; CONTROLLED STUDY; EARLY DIAGNOSIS; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GRAY MATTER; HIPPOCAMPUS DYSFUNCTION; HUMAN; IMAGE ANALYSIS; MALE; MEMORY; MILD COGNITIVE IMPAIRMENT; NERVE CELL NETWORK; NEUROPATHOLOGY; NEUROPSYCHOLOGICAL TEST; PAIRED ASSOCIATE LEARNING; PREFRONTAL CORTEX; TASK PERFORMANCE; TEMPORAL GYRUS;

AGED; ASSOCIATION LEARNING; BRAIN; COGNITION DISORDERS; DATA INTERPRETATION, STATISTICAL; FEMALE; HIPPOCAMPUS; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; MEMORY; MIDDLE AGED; NEUROPSYCHOLOGICAL TESTS; PARAHIPPOCAMPAL GYRUS; PHOTIC STIMULATION; SPACE PERCEPTION; VERBAL BEHAVIOR; VISUAL PERCEPTION;

EID: 79956113931     PISSN: 00283932     EISSN: 18733514     Source Type: Journal    
DOI: 10.1016/j.neuropsychologia.2011.03.037     Document Type: Article

References (87)

1. Acosta-Cabronero J., Williams G.B., Pereira J.M., Pengas G., Nestor P.J. The impact of skull-stripping and radio-frequency bias correction on grey-matter segmentation for voxel-based morphometry. Neuroimage 2008, 39:1654-1665.
2. Ahmed S., Mitchell J., Arnold R., Nestor P.J., Hodges J.R. Predicting rapid clinical progression in amnestic mild cognitive impairment. Dementia and Geriatric Cognitive Disorders 2008, 25:170-177.
3. Apostolova L.G., Dinov I.D., Dutton R.A., Hayashi K.M., Toga A.W., Cummings J.L., et al. 3D comparison of hippocampal atrophy in amnestic mild cognitive impairment and Alzheimer's disease. Brain 2006, 129:2867-2873.
4. Ashburner J., Friston K.J. Voxel-based morphometry - the methods. Neuroimage 2000, 11:805-821.
5. Ashburner J., Friston K.J. Unified segmentation. Neuroimage 2005, 26:839-851.
6. Bai F., Zhang Z., Watson D.R., Yu H., Shi Y., Yuan Y., et al. Abnormal functional connectivity of hippocampus during episodic memory retrieval processing network in amnestic mild cognitive impairment. Biological Psychiatry 2009, 65:951-958.
7. Beddington J., Cooper C.L., Field J., Goswami U., Huppert F.A., Jenkins R., et al. The mental wealth of nations. Nature 2008, 455:1057-1060.
8. Blackwell A.D., Sahakian B.J., Vesey R., Semple J.M., Robbins T.W., Hodges J.R. Detecting dementia: Novel neuropsychological markers of preclinical Alzheimer's disease. Dementia and Geriatric Cognitive Disorders 2004, 17:42-48.
9. Braak H., Braak E. Neuropathological staging of Alzheimer-related changes. Acta Neuropathologica (Berl) 1991, 82:239-259.
10. Cabeza R., Nyberg L. Imaging cognition II: An empirical review of 275 PET and fMRI studies. Journal of Cognitive Neuroscience 2000, 12:1-47.
11. Celone K.A., Calhoun V.D., Dickerson B.C., Atri A., Chua E.F., Miller S.L., et al. Alterations in memory networks in mild cognitive impairment and Alzheimer's disease: An independent component analysis. Journal of Neuroscience 2006, 26:10222-10231.
12. Chetelat G., Desgranges B., de la Sayette V., Viader F., Berkouk K., Landeau B., et al. Dissociating atrophy and hypometabolism impact on episodic memory in mild cognitive impairment. Brain 2003, 126:1955-1967.
13. Choo I.H., Lee D.Y., Oh J.S., Lee J.S., Lee D.S., Song I.C., et al. Posterior cingulate cortex atrophy and regional cingulum disruption in mild cognitive impairment and Alzheimer's disease. Neurobiology of Aging 2010, 31:772-779.
14. Dannhauser T.M., Shergill S.S., Stevens T., Lee L., Seal M., Walker R.W., et al. An fMRI study of verbal episodic memory encoding in amnestic mild cognitive impairment. Cortex 2008, 44:869-880.
15. de Jager C., Lesk V., Zhi X., Marsico M., Chandler J. Episodic memory test constructs affect discrimination among health elderly and cases with mild cognitive impairment and Alzheimer's disease. International conference on Alzheimer's disease 2008.
16. Dickerson B.C., Salat D.H., Bates J.F., Atiya M., Killiany R.J., Greve D.N., et al. Medial temporal lobe function and structure in mild cognitive impairment. Annals of Neurology 2004, 56:27-35.
17. Dickerson B.C., Salat D.H., Greve D.N., Chua E.F., Rand-Giovannetti E., Rentz D.M., et al. Increased hippocampal activation in mild cognitive impairment compared to normal aging and AD. Neurology 2005, 65:404-411.
18. Dickerson B.C., Sperling R.A. Functional abnormalities of the medial temporal lobe memory system in mild cognitive impairment and Alzheimer's disease: Insights from functional MRI studies. Neuropsychologia 2008, 46:1624-1635.
19. Dubois B., Feldman H.H., Jacova C., Dekosky S.T., Barberger-Gateau P., Cummings J., et al. Research criteria for the diagnosis of Alzheimer's disease: Revising the NINCDS-ADRDA criteria. Lancet Neurology 2007, 6:734-746.
20. Fein G., Landman B., Tran H., Barakos J., Moon K., Di Sclafani V., et al. Statistical parametric mapping of brain morphology: Sensitivity is dramatically increased by using brain-extracted images as inputs. Neuroimage 2006, 30:1187-1195.
21. Fletcher P.C., Henson R.N. Frontal lobes and human memory: Insights from functional neuroimaging. Brain 2001, 124:849-881.
22. Folstein M.F., Folstein S.E., McHugh P.R. Mini-mental state. A practical method for grading the cognitive state of patients for the clinician. Journal of Psychiatric Research 1975, 12:189-198.
23. Fowler K.S., Saling M.M., Conway E.L., Semple J.M., Louis W.J. Computerized delayed matching to sample and paired associate performance in the early detection of dementia. Applied Neuropsychology 1995, 2:72-78.
24. Fowler K.S., Saling M.M., Conway E.L., Semple J.M., Louis W.J. Computerized neuropsychological tests in the early detection of dementia: Prospective findings. Journal of the International Neuropsychological Society 1997, 3:139-146.
25. 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 the International Neuropsychological Society 2002, 8:58-71.
26. Fox N.C., Warrington E.K., Rossor M.N. Serial magnetic resonance imaging of cerebral atrophy in preclinical Alzheimer's disease. Lancet 1999, 353:2125.
27. Friston K.J., Holmes A.P., Worsley K.J., Poline J.B., Frackowiak R.S. Statistical parametric maps in functional imaging: A general linear approach. Human Brain Mapping 1995, 2:189-210.
28. Geerts H. Drug evaluation: (R)-flurbiprofen - an enantiomer of flurbiprofen for the treatment of Alzheimer's disease. IDrugs 2007, 10:121-133.
29. Genovese C.R., Lazar N.A., Nichols T. Thresholding of statistical maps in functional neuroimaging using the false discovery rate. Neuroimage 2002, 15:870-878.
30. Gould R.L., Arroyo B., Brown R.G., Owen A.M., Bullmore E.T., Howard R.J. Brain mechanisms of successful compensation during learning in Alzheimer disease. Neurology 2006, 67:1011-1017.
31. Gould R.L., Brown R.G., Owen A.M., Bullmore E.T., Howard R.J. Task-induced deactivations during successful paired associates learning: An effect of age but not Alzheimer's disease. Neuroimage 2006, 31:818-831.
32. Gould R.L., Brown R.G., Owen A.M., Bullmore E.T., Williams S.C., Howard R.J. Functional neuroanatomy of successful paired associate learning in Alzheimer's disease. American Journal of Psychiatry 2005, 162:2049-2060.
33. Gould R.L., Brown R.G., Owen A.M., Ffytche D.H., Howard R.J. fMRI BOLD response to increasing task difficulty during successful paired associates learning. Neuroimage 2003, 20:1006-1019.
34. Greicius M.D., Krasnow B., Reiss A.L., Menon V. Functional connectivity in the resting brain: A network analysis of the default mode hypothesis. Proceedings of the National Academy of Sciences of the United States of America 2003, 100:253-258.
35. Greig N.H., Sambamurti K., Yu Q.-S., Brossi A., Bruinsma G.B., Lahiri D.K. An overview of phenserine tartrate, a novel acetylcholinesterase inhibitor for the treatment of Alzheimer's disease. Current Alzheimer Research 2005, 2:281-290.
36. Gusnard D.A., Raichle M.E., Raichle M.E. Searching for a baseline: Functional imaging and the resting human brain. Nature Reviews Neuroscience 2001, 2:685-694.
37. Hamalainen A., Pihlajamaki M., Tanila H., Hanninen T., Niskanen E., Tervo S., et al. Increased fMRI responses during encoding in mild cognitive impairment. Neurobiology of Aging 2006, 28(12):1889-1903.
38. Hayasaka S., Nichols T.E. Validating cluster size inference: Random field and permutation methods. Neuroimage 2003, 20:2343-2356.
39. Jack C.R., Lowe V.J., Senjem M.L., Weigand S.D., Kemp B.J., Shiung M.M., et al. 11C PiB and structural MRI provide complementary information in imaging of Alzheimer's disease and amnestic mild cognitive impairment. Brain 2008, 131:665-680.
40. Jack C.R., Lowe V.J., Weigand S.D., Wiste H.J., Senjem M.L., Knopman D.S., et al. Serial PIB and MRI in normal, mild cognitive impairment and Alzheimer's disease: Implications for sequence of pathological events in Alzheimer's disease. Brain 2009, 132:1355-1365.
41. Johnson S.C., Baxter L.C., Susskind-Wilder L., Connor D.J., Sabbagh M.N., Caselli R.J. Hippocampal adaptation to face repetition in healthy elderly and mild cognitive impairment. Neuropsychologia 2004, 42:980-989.
42. Jones E.G., Powell T.P. An anatomical study of converging sensory pathways within the cerebral cortex of the monkey. Brain 1970, 93:793-820.
43. Lee A.C., Robbins T.W., Owen A.M. Episodic memory meets working memory in the frontal lobe: Functional neuroimaging studies of encoding and retrieval. Critical Reviews in Neurobiology 2000, 14:165-197.
44. Machulda M.M., Ward H.A., Borowski B., Gunter J.L., Cha R.H., O'Brien P.C., et al. Comparison of memory fMRI response among normal, MCI, and Alzheimer's patients. Neurology 2003, 61:500-506.
45. Maguire E.A., Frith C.D., Burgess N., Donnett J.G., O'Keefe J. Knowing where things are parahippocampal involvement in encoding object locations in virtual large-scale space. Journal of Cognitive Neuroscience 1998, 10:61-76.
46. Maldjian J.A., Laurienti P.J., Kraft R.A., Burdette J.H. An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. Neuroimage 2003, 19:1233-1239.
47. Masters C.L., Beyreuther K. Alzheimer's centennial legacy: Prospects for rational therapeutic intervention targeting the Abeta amyloid pathway. Brain 2006, 129:2823-2839.
48. Mazoyer B., Zago L., Mellet E., Bricogne S., Etard O., Houde O., et al. Cortical networks for working memory and executive functions sustain the conscious resting state in man. Brain Research Bulletin 2001, 54:287-298.
49. McKiernan K.A., Kaufman J.N., Kucera-Thompson J., Binder J.R. A parametric manipulation of factors affecting task-induced deactivation in functional neuroimaging. Journal of Cognitive Neuroscience 2003, 15:394-408.
50. Minoshima S., Giordani B., Berent S., Frey K.A., Foster N.L., Kuhl D.E. Metabolic reduction in the posterior cingulate cortex in very early Alzheimer's disease. Annals of Neurology 1997, 42:85-94.
51. Mioshi E., Dawson K., Mitchell J., Arnold R., Hodges J.R. The Addenbrooke's Cognitive Examination Revised (ACE-R): A brief cognitive test battery for dementia screening. International Journal of Geriatric Psychiatry 2006, 21:1078-1085.
52. Morris J.C. The Clinical Dementia Rating (CDR): Current version and scoring rules. Neurology 1993, 43:2412-2414.
53. Nagahama Y., Okina T., Suzuki N., Matsuda M. The Cambridge Behavioral Inventory: Validation and application in a memory clinic. Journal of Geriatric Psychiatry and Neurology 2006, 19:220-225.
54. Nestor P.J., Fryer T.D., Smielewski P., Hodges J.R. Limbic hypometabolism in Alzheimer's disease and mild cognitive impairment. Annals of Neurology 2003, 54:343-351.
55. O'Brien J.L., O'Keefe K.M., LaViolette P.S., DeLuca A.N., Blacker D., Dickerson B.C., et al. Longitudinal fMRI in elderly reveals loss of hippocampal activation with clinical decline. Neurology 2010, 74:1969-1976.
56. O'Keefe J., Nadel L. The hippocampus as a cognitive map 1978, The Claredon Press, Oxford, (chapter 2).
57. Owen A.M., Miller B., Petrides M., Evans A.C. A specific role for the right parahippocampal gyrus in the retrieval of object-location: A positron emission tomography study. Journal of Cognitive Neuroscience 1996, 12:163-173.
58. Owen A.M., Sahakian B.J., Semple J., Polkey C.E., Robbins T.W. Visuo-spatial short-term recognition memory and learning after temporal lobe excisions, frontal lobe excisions or amygdalo-hippocampectomy in man. Neuropsychologia 1995, 33:1-24.
59. Parkinson J.K., Murray E.A., Mishkin M. A selective mnemonic role for the hippocampus in monkeys: Memory for the location of objects. Journal of Neuroscience 1988, 8:4159-4167.
60. Pengas G., Hodges J.R., Watson P., Nestor P.J. Focal posterior cingulate atrophy in incipient Alzheimer's disease. Neurobiology of Aging 2010, 31:25-33.
61. Pengas G., Pereira J.M., Williams G.B., Nestor P.J. Comparative reliability of total intracranial volume estimation methods and the influence of atrophy in a longitudinal semantic dementia cohort. Journal of Neuroimaging 2009, 19:37-46.
62. Pennanen C., Testa C., Laakso M.P., Hallikainen M., Helkala E.L., Hanninen T., et al. A voxel based morphometry study on mild cognitive impairment. Journal of Neurology, Neurosurgery and Psychiatry 2005, 76:11-14.
63. Pereira J.M., Xiong L., Acosta-Cabronero J., Pengas G., Williams G.B., Nestor P.J. Registration accuracy for VBM studies varies according to region and degenerative disease grouping. Neuroimage 2010, 49:2205-2215.
64. Petersen R.C. Mild cognitive impairment as a diagnostic entity. Journal of Internal Medicine 2004, 256:183-194.
65. 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.
66. Petrella J.R., Krishnan S., Slavin M.J., Tran T.T., Murty L., Doraiswamy P.M. Mild cognitive impairment: Evaluation with 4-T functional MR imaging. Radiology 2006, 240:177-186.
67. Raichle M.E., MacLeod A.M., Snyder A.Z., Powers W.J., Gusnard D.A., Shulman G.L. A default mode of brain function. Proceedings of the National Academy of Sciences of the United States of America 2001, 98:676-682.
68. Rowe C.C., Ng S., Ackermann U., Gong S.J., Pike K., Savage G., et al. Imaging beta-amyloid burden in aging and dementia. Neurology 2007, 68:1718-1725.
69. Sahakian B.J., Morris R.G., Evenden J.L., Heald A., Levy R., Philpot M., et al. A comparative study of visuospatial memory and learning in Alzheimer-type dementia and Parkinson's disease. Brain 1988, 111(Pt 3):695-718.
70. Schmand B., Huizenga H.M., van Gool W.A. Meta-analysis of CSF and MRI biomarkers for detecting preclinical Alzheimer's disease. Psychological Medicine 2010, 40:135-145.
71. Segonne F., Dale A.M., Busa E., Glessner M., Salat D., Hahn H.K., et al. A hybrid approach to the skull stripping problem in MRI. Neuroimage 2004, 22:1060-1075.
72. Sled J.G., Zijdenbos A.P., Evans A.C. A nonparametric method for automatic correction of intensity nonuniformity in MRI data. IEEE Transactions of Medical Imaging 1998, 17:87-97.
73. Small S.A., Perera G.M., DeLaPaz R., Mayeux R., Stern Y. Differential regional dysfunction of the hippocampal formation among elderly with memory decline and Alzheimer's disease. Annals of Neurology 1999, 45:466-472.
74. Smith M.L., Milner B. The role of the right hippocampus in the recall of spatial location. Neuropsychologia 1981, 19:781-793.
75. Smith S.M. Fast robust automated brain extraction. Human Brain Mapping 2002, 17:143-155.
76. Stark C. Functinal role of the human hippocampus. The hippocampus book 2007, 549-579. Oxford Univerity Press, New York. P. Andersen, R. Morris, D. Amaral, T. Bliss, J. O'Keefe (Eds.).
77. Svoboda E., McKinnon M.C., Levine B. The functional neuroanatomy of autobiographical memory: A meta-analysis. Neuropsychologia 2006, 44:2189-2208.
78. 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.
79. Taffe M.A., Weed M.R., Gutierrez T., Davis S.A., Gold L.H. Differential muscarinic and NMDA contributions to visuo-spatial paired-associate learning in rhesus monkeys. Psychopharmacology (Berl) 2002, 160:253-262.
80. Talpos J.C., Winters B.D., Dias R., Saksida L.M., Bussey T.J. A novel touchscreen-automated paired-associate learning (PAL) task sensitive to pharmacological manipulation of the hippocampus: A translational rodent model of cognitive impairments in neurodegenerative disease. Psychopharmacology (Berl) 2009, 205:157-168.
81. Trivedi M.A., Murphy C.M., Goetz C., Shah R.C., Gabrieli J.D., Whitfield-Gabrieli S., et al. fMRI activation changes during successful episodic memory encoding and recognition in amnestic mild cognitive impairment relative to cognitively healthy older adults. Dementia and Geriatric Cognitive Disorders 2008, 26:123-137.
82. Tulving E., Kapur S., Markowitsch H.J., Craik F.I., Habib R., Houle S. Neuroanatomical correlates of retrieval in episodic memory: Auditory sentence recognition. Proceedings of the National Academy of Sciences of the United States of America 1994, 91:2012-2015.
83. Vellas B., Andrieu S., Sampaio C., Wilcock G. Disease-modifying trials in Alzheimer's disease: A European task force consensus. Lancet Neurology 2007, 6:56-62.
84. Weed M.R., Taffe M.A., Polis I., Roberts A.C., Robbins T.W., Koob G.F., et al. Performance norms for a rhesus monkey neuropsychological testing battery: Acquisition and long-term performance. Cognitive Brain Research 1999, 8:185-201.
85. Whitwell J.L., Przybelski S.A., Weigand S.D., Knopman D.S., Boeve B.F., Petersen R.C., et al. 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.
86. Worsley K.J., Marrett S., Neelin P., Vandal A.C., Friston K.J., Evans A.C. A unified statistical approach for determining significant signals in images of cerebral activation. Human Brain Mapping 1996, 4:58-73.
87. Ziolko S.K., Weissfeld L.A., Klunk W.E., Mathis C.A., Hoge J.A., Lopresti B.J., et al. Evaluation of voxel-based methods for the statistical analysis of PIB PET amyloid imaging studies in Alzheimer's disease. Neuroimage 2006, 33:94-102.