Role of hippocampal CA1 atrophy in memory encoding deficits in amnestic Mild Cognitive Impairment

NeuroImage

Volumn 59, Issue 4, 2012, Pages 3309-3315

  Fouquet, Marine ^a,b,c,d   Desgranges, Béatrice ^a,b,c,d   La Joie, Renaud ^a,b,c,d   Rivière, Denis ^e   Mangin, Jean François ^e   Landeau, Brigitte ^a,b,c,d   Mézenge, Florence ^a,b,c,d   Pélerin, Alice ^a,b,c,d   de La Sayette, Vincent ^a,b,c,d   Viader, Fausto ^a,b,c,d   Baron, Jean Claude ^f   Eustache, Francis ^a,b,c,d   Chételat, Gaël ^a,b,c,d  

^a Centre Cyceron   (France)

^b UNIVERSITÉ DE CAEN   (France)

^c PSL RESEARCH UNIVERSITY   (France)

^d CAEN UNIVERSITY HOSPITAL   (France)

^e DIF   (France)

^f INSERM   (France)

Author keywords

Amnestic Mild Cognitive Impairment; CA1; Encoding; Episodic memory; Hippocampus; MRI

Indexed keywords

ADULT; ANATOMICAL VARIATION; ARTICLE; BRAIN ATROPHY; BRAIN FUNCTION; BRAIN MAPPING; CLINICAL ARTICLE; CONTROLLED STUDY; CORRELATION ANALYSIS; FEMALE; FRONTAL CORTEX; GRAY MATTER; HIPPOCAMPAL CA1 REGION; HUMAN; IMAGE ANALYSIS; IMAGE PROCESSING; MALE; MILD COGNITIVE IMPAIRMENT; NEUROIMAGING; NEUROPSYCHOLOGICAL TEST; NUCLEAR MAGNETIC RESONANCE IMAGING; PARIETAL CORTEX; PRIORITY JOURNAL; WHITE MATTER;

AGED; ATROPHY; FEMALE; HIPPOCAMPUS; HUMANS; MALE; MEMORY DISORDERS; MILD COGNITIVE IMPAIRMENT;

EID: 84855170462     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2011.11.036     Document Type: Article

References (71)

1. Amaral D.G. Emerging principles of intrinsic hippocampal organization. Curr. Opin. Neurobiol. 1993, 3(2):225-229.
2. Amaral D.G., Witter M.P. The three-dimensional organization of the hippocampal formation: a review of anatomical data. Neuroscience 1989, 31(3):571-591.
3. Apostolova L.G., Dinov I.D., Dutton R.A., Hayashi K.M., Toga A.W., Cummings J.L., Thompson P.M. 3D comparison of hippocampal atrophy in amnestic mild cognitive impairment and Alzheimer's disease. Brain 2006, 129(Pt 11):2867-2873.
4. Apostolova L.G., Dutton R.A., Dinov I.D., Hayashi K.M., Toga A.W., Cummings J.L., Thompson P.M. Conversion of mild cognitive impairment to Alzheimer disease predicted by hippocampal atrophy maps. Arch. Neurol. 2006, 63(5):693-699.
5. Apostolova L.G., Mosconi L., Thompson P.M., Green A.E., Hwang K.S., Ramirez A., Mistur R., Tsui W.H., de Leon M.J. Subregional hippocampal atrophy predicts Alzheimer's dementia in the cognitively normal. Neurobiol. Aging 2010, 31(7):1077-1088.
6. Apostolova L.G., Thompson P.M., Green A.E., Hwang K.S., Zoumalan C., Jack C.R., Harvey D.J., Petersen R.C., Thal L.J., Aisen P.S., Toga A.W., Cummings J.L., Decarli C.S. 3D comparison of low, intermediate, and advanced hippocampal atrophy in MCI. Hum. Brain Mapp. 2010, 31(5):786-797.
7. 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 2011, NeuroImage.
8. Bartsch T., Schönfeld R., Müller F.J., Alfke K., Leplow B., Aldenhoff J., Deuschl G., Koch J.M. Focal lesions of human hippocampal CA1 neurons in transient global amnesia impair place memory. Science 2010, 328(5984):1412-1415.
9. Bartsch T., Deuschl G. Transient global amnesia: functional anatomy and clinical implications. Lancet Neurol. 2010, 9(2):205-214.
10. Becker J.T., Davis S.W., Hayashi K.M., Meltzer C.C., Toga A.W., Lopez O.L., Thompson P.M. Three-dimensional patterns of hippocampal atrophy in mild cognitive impairment. Arch. Neurol. 2006, 63(1):97-101.
11. Belleville S., Sylvain-Roy S., de Boysson C., Ménard M.-C. Characterizing the memory changes in persons with mild cognitive impairment. Prog. Brain Res. 2008, 169:365-375.
12. Braak E., Braak H. Alzheimer's disease: transiently developing dendritic changes in pyramidal cells of sector CA1 of the Ammon's horn. Acta Neuropathol. 1997, 93(4):323-325.
13. Braak H., Braak E. Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol. 1991, 82(4):239-259.
14. Buckner R.L., Wheeler M.E. The cognitive neuroscience of remembering. Nat. Rev. Neurosci. 2001, 2(9):624-634.
15. Carr V.A., Rissman J., Wagner A.D. Imaging the human medial temporal lobe with high-resolution fMRI. Neuron 2010, 65(3):298-308.
16. Carr V.A., Viskontas I.V., Engel S.A., Knowlton B.J. Neural activity in the hippocampus and perirhinal cortex during encoding is associated with the durability of episodic memory. J. Cogn. Neurosci. 2010, 22(11):2652-2662.
17. Chua T.C., Wen W., Slavin M.J., Sachdev P.S. Diffusion tensor imaging in mild cognitive impairment and Alzheimer's disease: a review. Curr. Opin. Neurol. 2008, 21(1):83-92.
18. Chételat G., Desgranges B., de la Sayette V., Viader F., Berkouk K., Landeau B., Lalevée C., Le Doze F., Dupuy B., Hannequin D., Baron J.-C., Eustache F. Dissociating atrophy and hypometabolism impact on episodic memory in mild cognitive impairment. Brain 2003, 126(Pt 9):1955-1967.
19. Chételat G., Eustache F., Viader F., De La Sayette V., Pélerin A., Mézenge F., Hannequin D., Dupuy B., Baron J.-C., Desgranges B. FDG-PET measurement is more accurate than neuropsychological assessments to predict global cognitive deterioration in patients with mild cognitive impairment. Neurocase 2005, 11(1):14-25.
20. Chételat G., Fouquet M., Kalpouzos G., Denghien I., De la Sayette V., Viader F., Mézenge F., Landeau B., Baron J.C., Eustache F., Desgranges B. Three-dimensional surface mapping of hippocampal atrophy progression from MCI to AD and over normal aging as assessed using voxel-based morphometry. Neuropsychologia 2008, 46(6):1721-1731.
21. Convit A., De Leon M.J., Tarshish C., De Santi S., Tsui W., Rusinek H., George A. Specific hippocampal volume reductions in individuals at risk for Alzheimer's disease. Neurobiol. Aging 1997, 18(2):131-138.
22. Desgranges B., Baron J.C., de la Sayette V., Petit-Taboué M.C., Benali K., Landeau B., Lechevalier B., Eustache F. The neural substrates of memory systems impairment in Alzheimer's disease. A PET study of resting brain glucose utilization. Brain 1998, 121(Pt 4):611-631.
23. Duvernoy H.M. The Human Hippocampus, Functional Anatomy, Vascularization, and Serial Sections with MRI 1998, Springer, Berlin. 2e ed.
24. Eldridge L.L., Engel S.A., Zeineh M.M., Bookheimer S.Y., Knowlton B.J. A dissociation of encoding and retrieval processes in the human hippocampus. J. Neurosci. 2005, 25(13):3280-3286.
25. Eustache F., Desgranges B., Lalevée C. Clinical evaluation of memory. Rev. Neurol. (Paris) 1998, 154(Suppl 2):S18-S32.
26. Eustache F., Desgranges B., Laville P., Guillery B., Lalevée C., Schaeffer S., de la Sayette V., Iglesias S., Baron J.C., Viader F. Episodic memory in transient global amnesia: encoding, storage, or retrieval deficit?. J. Neurol. Neurosurg. Psychiatry 1999, 66(2):148-154.
27. Eustache F., Piolino P., Giffard B., Viader F., De La Sayette V., Baron J.-C., Desgranges B. « In the course of time »: a PET study of the cerebral substrates of autobiographical amnesia in Alzheimer's disease. Brain 2004, 127(Pt 7):1549-1560.
28. Fellgiebel A., Müller M.J., Wille P., Dellani P.R., Scheurich A., Schmidt L.G., Stoeter P. Color-coded diffusion-tensor-imaging of posterior cingulate fiber tracts in mild cognitive impairment. Neurobiol. Aging 2005, 26(8):1193-1198.
29. Fjell A.M., Walhovd K.B., Amlien I., Bjørnerud A., Reinvang I., Gjerstad L., Cappelen T., Willoch F., Due-Tønnessen P., Grambaite R., Skinningsrud A., Stenset V., Fladby T. Morphometric changes in the episodic memory network and tau pathologic features correlate with memory performance in patients with mild cognitive impairment. AJNR Am. J. Neuroradiol. 2008, 29(6):1183-1189.
30. 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. J. Psychiatr. Res. 1975, 12(3):189-198.
31. Gabrieli J.D., Brewer J.B., Desmond J.E., Glover G.H. Separate neural bases of two fundamental memory processes in the human medial temporal lobe. Science 1997, 276(5310):264-266.
32. Gazzaniga M.S. Cerebral specialization and interhemispheric communication: does the corpus callosum enable the human condition?. Brain 2000, 123(Pt 7):1293-1326.
33. Gouw A.A., Seewann A., Vrenken H., van der Flier W.M., Rozemuller J.M., Barkhof F., Scheltens P., Geurts J.J.G. Heterogeneity of white matter hyperintensities in Alzheimer's disease: post-mortem quantitative MRI and neuropathology. Brain 2008, 131(Pt 12):3286-3298.
34. Hanseeuw B., Dricot L., Kavec M., Grandin C., Seron X., Ivanoiu A. Associative encoding deficits in amnestic mild cognitive impairment: a volumetric and functional MRI study. Neuroimage 2011, 56(3):1743-1748.
35. Jeong S.-H., Lee J.H., Lee A.Y. Reversible visual memory in transient splenial lesion. Neurology 2009, 73(8):647.
36. Jhoo J.H., Lee D.Y., Choo I.H., Seo E.H., Oh J.S., Lee J.S., Lee D.S., Kim S.G., Youn J.C., Kim K.W., Woo J.I. Discrimination of normal aging, MCI and AD with multimodal imaging measures on the medial temporal lobe. Psychiatry Res. 2010, 183(3):237-243.
37. La Joie R., Fouquet M., Mézenge F., Landeau B., Villain N., Mevel K., Pélerin A., Eustache F., Desgranges B., Chételat G. Differential effect of age on hippocampal subfields assessed using a new high-resolution 3T MR sequence. Neuroimage 2010, 53(2):506-514.
38. Lepage M., Habib R., Tulving E. Hippocampal PET activations of memory encoding and retrieval: the HIPER model. Hippocampus 1998, 8(4):313-322.
39. Leube D.T., Weis S., Freymann K., Erb M., Jessen F., Heun R., Grodd W., Kircher T.T. Neural correlates of verbal episodic memory in patients with MCI and Alzheimer's disease-a VBM study. Int. J. Geriatr. Psychiatry 2008, 23(11):1114-1118.
40. Markesbery W.R., Schmitt F.A., Kryscio R.J., Davis D.G., Smith C.D., Wekstein D.R. Neuropathologic substrate of mild cognitive impairment. Arch. Neurol. 2006, 63(1):38-46.
41. 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(7):939-944.
42. Mitchell T.W., Mufson E.J., Schneider J.A., Cochran E.J., Nissanov J., Han L.-Y., Bienias J.L., Lee V.M.-Y., Trojanowski J.Q., Bennett D.A., Arnold S.E. Parahippocampal tau pathology in healthy aging, mild cognitive impairment, and early Alzheimer's disease. Ann. Neurol. 2002, 51(2):182-189.
43. Mueller S.G., Schuff N., Yaffe K., Madison C., Miller B., Weiner M.W. Hippocampal atrophy patterns in mild cognitive impairment and Alzheimer's disease. Hum. Brain Mapp. 2010, 31(9):1339-1347.
44. Nestor P.J., Fryer T.D., Hodges J.R. Declarative memory impairments in Alzheimer's disease and semantic dementia. Neuroimage 2006, 30(3):1010-1020.
45. Di Paola M., Spalletta G., Caltagirone C. In vivo structural neuroanatomy of corpus callosum in Alzheimer's disease and mild cognitive impairment using different MRI techniques: a review. J. Alzheimers Dis. 2010, 20(1):67-95.
46. Petersen R.C. Mild cognitive impairment: useful or not?. Alzheimers Dement. 2005, 1(1):5-10.
47. Pike K.E., Savage G. Memory profiling in mild cognitive impairment: can we determine risk for Alzheimer's disease?. J. Neuropsychol. 2008, 2(Pt 2):361-372.
48. Preston A.R., Bornstein A.M., Hutchinson J.B., Gaare M.E., Glover G.H., Wagner A.D. High-resolution fMRI of content-sensitive subsequent memory responses in human medial temporal lobe. J. Cogn. Neurosci. 2010, 22(1):156-173.
49. Quinette P., Guillery-Girard B., Noël A., de la Sayette V., Viader F., Desgranges B., Eustache F. The relationship between working memory and episodic memory disorders in transient global amnesia. Neuropsychologia 2006, 44(12):2508-2519.
50. Rolls E.T. A theory of hippocampal function in memory. Hippocampus 1996, 6(6):601-620.
51. Rolls E.T. An attractor network in the hippocampus: theory and neurophysiology. Learn. Mem. 2007, 14(11):714-731.
52. Salmon E., Lekeu F., Bastin C., Garraux G., Collette F. Functional imaging of cognition in Alzheimer's disease using positron emission tomography. Neuropsychologia 2008, 46(6):1613-1623.
53. Sarazin M., Chauviré V., Gerardin E., Colliot O., Kinkingnéhun S., de Souza L.C., Hugonot-Diener L., Garnero L., Lehéricy S., Chupin M., Dubois B. The amnestic syndrome of hippocampal type in Alzheimer's disease: an MRI study. J. Alzheimers Dis. 2010, 22(1):285-294.
54. Schacter D.L., Wagner A.D. Medial temporal lobe activations in fMRI and PET studies of episodic encoding and retrieval. Hippocampus 1999, 9(1):7-24.
55. Scheff S.W., Price D.A., Schmitt F.A., DeKosky S.T., Mufson E.J. Synaptic alterations in CA1 in mild Alzheimer disease and mild cognitive impairment. Neurology 2007, 68(18):1501-1508.
56. Schmidt-Wilcke T., Poljansky S., Hierlmeier S., Hausner J., Ibach B. Memory performance correlates with gray matter density in the ento-/perirhinal cortex and posterior hippocampus in patients with mild cognitive impairment and healthy controls-a voxel based morphometry study. Neuroimage 2009, 47(4):1914-1920.
57. Schwindt G.C., Black S.E. Functional imaging studies of episodic memory in Alzheimer's disease: a quantitative meta-analysis. Neuroimage 2009, 45(1):181-190.
58. Serra L., Cercignani M., Lenzi D., Perri R., Fadda L., Caltagirone C., Macaluso E., Bozzali M. Grey and white matter changes at different stages of Alzheimer's disease. J. Alzheimers Dis. 2010, 19(1):147-159.
59. Sexton C.E., Mackay C.E., Lonie J.A., Bastin M.E., Terrière E., O'Carroll R.E., Ebmeier K.P. MRI correlates of episodic memory in Alzheimer's disease, mild cognitive impairment, and healthy aging. Psychiatry Res. 2010, 184(1):57-62.
60. Suthana N., Ekstrom A., Moshirvaziri S., Knowlton B., Bookheimer S. Dissociations within human hippocampal subregions during encoding and retrieval of spatial information. Hippocampus 2010, 21(7):694-701.
61. Teyler T.J., DiScenna P. The topological anatomy of the hippocampus: a clue to its function. Brain Res. Bull. 1984, 12(6):711-719.
62. Vemuri P., Whitwell J.L., Kantarci K., Josephs K.A., Parisi J.E., Shiung M.S., Knopman D.S., Boeve B.F., Petersen R.C., Dickson D.W., Jack C.R. Antemortem MRI based STructural Abnormality iNDex (STAND)-scores correlate with postmortem Braak neurofibrillary tangle stage. Neuroimage 2008, 42(2):559-567.
63. Villain N., Desgranges B., Viader F., de la Sayette V., Mézenge F., Landeau B., Baron J.-C., Eustache F., Chételat G. Relationships between hippocampal atrophy, white matter disruption, and gray matter hypometabolism in Alzheimer's disease. J. Neurosci. 2008, 28(24):6174-6181.
64. Villain N., Fouquet M., Baron J.-C., Mézenge F., Landeau B., de La Sayette V., Viader F., Eustache F., Desgranges B., Chételat G. Sequential relationships between grey matter and white matter atrophy and brain metabolic abnormalities in early Alzheimer's disease. Brain 2010, 133(11):3301-3314.
65. Wang L., Miller J.P., Gado M.H., McKeel D.W., Rothermich M., Miller M.I., Morris J.C., Csernansky J.G. Abnormalities of hippocampal surface structure in very mild dementia of the Alzheimer type. Neuroimage 2006, 30(1):52-60.
66. Wang Q.S., Zhou J.N. Retrieval and encoding of episodic memory in normal aging and patients with mild cognitive impairment. Brain Res. 2002, 924(1):113-115.
67. Whitwell J.L., Josephs K.A., Murray M.E., Kantarci K., Przybelski S.A., Weigand S.D., Vemuri P., Senjem M.L., Parisi J.E., Knopman D.S., Boeve B.F., Petersen R.C., Dickson D.W., Jack C.R. MRI correlates of neurofibrillary tangle pathology at autopsy: a voxel-based morphometry study. Neurology 2008, 71(10):743-749.
68. Yassa M.A., Stark S.M., Bakker A., Albert M.S., Gallagher M., Stark C.E.L. High-resolution structural and functional MRI of hippocampal CA3 and dentate gyrus in patients with amnestic Mild Cognitive Impairment. Neuroimage 2010, 51(3):1242-1252.
69. Zarow C., Vinters H.V., Ellis W.G., Weiner M.W., Mungas D., White L., Chui H.C. Correlates of hippocampal neuron number in Alzheimer's disease and ischemic vascular dementia. Ann. Neurol. 2005, 57(6):896-903.
70. Zeineh M.M., Engel S.A., Thompson P.M., Bookheimer S.Y. Dynamics of the hippocampus during encoding and retrieval of face-name pairs. Science 2003, 299(5606):577-580.
71. Zola-Morgan S., Squire L.R., Amaral D.G. Human amnesia and the medial temporal region: enduring memory impairment following a bilateral lesion limited to field CA1 of the hippocampus. J. Neurosci. 1986, 6(10):2950-2967.