Differential effect of age on hippocampal subfields assessed using a new high-resolution 3T MR sequence

NeuroImage

Volumn 53, Issue 2, 2010, Pages 506-514

  La Joie, Renaud ^a   Fouquet, Marine ^a   Mézenge, Florence ^a   Landeau, Brigitte ^a   Villain, Nicolas ^a   Mevel, Katell ^a   Pélerin, Alice ^a   Eustache, Francis ^a   Desgranges, Béatrice ^a   Chételat, Gaël ^a  

^a UNIVERSITÉ DE CAEN   (France)

Author keywords

Aging; CA1; Developmental hypothesis; High resolution MRI; Hippocampal subfields; Subiculum; VBM

Indexed keywords

ADULT; AGED; AGING; ARTICLE; BRAIN REGION; BRAIN SIZE; CONTROLLED STUDY; DENTATE GYRUS; FEMALE; GRAY MATTER; HIPPOCAMPUS; HUMAN; HUMAN EXPERIMENT; IMAGE ANALYSIS; MALE; NORMAL HUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; RELIABILITY; SUBICULUM; VOXEL BASED MORPHOMETRY;

ADULT; AGED; AGING; CA1 REGION, HIPPOCAMPAL; CA3 REGION, HIPPOCAMPAL; EDUCATION; FEMALE; HIPPOCAMPUS; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; NEUROPSYCHOLOGICAL TESTS; REFERENCE VALUES; REPRODUCIBILITY OF RESULTS; SEX CHARACTERISTICS; SOFTWARE; YOUNG ADULT;

EID: 77956061781     PISSN: 10538119     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2010.06.024     Document Type: Article

References (67)

1. Allen J.S., Bruss J., Brown C.K., Damasio H. Normal neuroanatomical variation due to age: the major lobes and a parcellation of the temporal region. Neurobiol. Aging 2005, 26:1245-1260.
2. 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, 63:693-699.
3. 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. 2008.
4. Ashburner J. A fast diffeomorphic image registration algorithm. Neuroimage 2007, 38:95-113.
5. Barboriak D.P., Doraiswamy P.M., Krishnan K.R., Vidyarthi S., Sylvester J., Charles H.C. Hippocampal sulcal cavities on MRI: relationship to age and apolipoprotein E genotype. Neurology 2000, 54:2150-2153.
6. Bastos-Leite A.J., van Waesberghe J.H., Oen A.L., van der Flier W.M., Scheltens P., Barkhof F. Hippocampal sulcus width and cavities: comparison between patients with Alzheimer disease and nondemented elderly subjects. AJNR Am. J. Neuroradiol. 2006, 27:2141-2145.
7. Bergouignan L., Chupin M., Czechowska Y., Kinkingnehun S., Lemogne C., Le B.G., Lepage M., Garnero L., Colliot O., Fossati P. Can voxel based morphometry, manual segmentation and automated segmentation equally detect hippocampal volume differences in acute depression?. Neuroimage 2009, 45:29-37.
8. Bird C.M., Burgess N. The hippocampus and memory: insights from spatial processing. Nat. Rev. Neurosci. 2008, 9:182-194.
9. Burgess N., Maguire E.A., O'Keefe J. The human hippocampus and spatial and episodic memory. Neuron 2002, 35:625-641.
10. Carr V.A., Rissman J., Wagner A.D. Imaging the human medial temporal lobe with high-resolution fMRI. Neuron 2010, 65:298-308.
11. Chételat G., Baron J.C. Early diagnosis of Alzheimer's disease: contribution of structural neuroimaging. Neuroimage 2003, 18:525-541.
12. 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, 46:1721-1731.
13. Cho Z.H., Han J.Y., Hwang S.I., Kim D.S., Kim K.N., Kim N.B., Kim S.J., Chi J.G., Park C.W., Kim Y.B. Quantitative analysis of the hippocampus using images obtained from 7.0 T MRI. Neuroimage 2010, 49:2134-2140.
14. Csernansky J.G., Wang L., Swank J., Miller J.P., Gado M., McKeel D., Miller M.I., Morris J.C. Preclinical detection of Alzheimer's disease: hippocampal shape and volume predict dementia onset in the elderly. Neuroimage 2005, 25:783-792.
15. Davis S.W., Dennis N.A., Buchler N.G., White L.E., Madden D.J., Cabeza R. Assessing the effects of age on long white matter tracts using diffusion tensor tractography. Neuroimage 2009, 46:530-541.
16. De Vita E., Thomas D.L., Roberts S., Parkes H.G., Turner R., Kinchesh P., Shmueli K., Yousry T.A., Ordidge R.J. High resolution MRI of the brain at 4.7 Tesla using fast spin echo imaging. Br. J. Radiol. 2003, 76:631-637.
17. Duvernoy H.M. The human hippocampus, functional anatomy, vascularization, and serial sections with MRI 1998, Springer, Berlin. 2nd ed.
18. Ekstrom A.D., Kahana M.J., Caplan J.B., Fields T.A., Isham E.A., Newman E.L., Fried I. Cellular networks underlying human spatial navigation. Nature 2003, 425:184-188.
19. 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, 25:3280-3286.
20. Eriksson S.H., Thom M., Bartlett P.A., Symms M.R., McEvoy A.W., Sisodiya S.M., Duncan J.S. PROPELLER MRI visualizes detailed pathology of hippocampal sclerosis. Epilepsia 2008, 49:33-39.
21. Fjell A.M., Walhovd K.B., Fennema-Notestine C., McEvoy L.K., Hagler D.J., Holland D., Brewer J.B., Dale A.M. One-year brain atrophy evident in healthy aging. J. Neurosci. 2009, 29:15223-15231.
22. Frisoni G.B., Ganzola R., Canu E., Rub U., Pizzini F.B., Alessandrini F., Zoccatelli G., Beltramello A., Caltagirone C., Thompson P.M. Mapping local hippocampal changes in Alzheimer's disease and normal ageing with MRI at 3 Tesla. Brain 2008, 131:3266-3276.
23. Frisoni G.B., Fox N.C., Jack C.R., Scheltens P., Thompson P.M. The clinical use of structural MRI in Alzheimer disease. Nat. Rev. Neurol. 2010, 6:67-77.
24. Geuze E., Vermetten E., Bremner J.D. MR-based in vivo hippocampal volumetrics: 2. Findings in neuropsychiatric disorders. Mol. Psychiatry 2005, 10:160-184.
25. Good C.D., Johnsrude I.S., Ashburner J., Henson R.N., Friston K.J., Frackowiak R.S. A voxel-based morphometric study of ageing in 465 normal adult human brains. Neuroimage 2001, 14:21-36.
26. Grieve S.M., Clark C.R., Williams L.M., Peduto A.J., Gordon E. Preservation of limbic and paralimbic structures in aging. Hum. Brain Mapp. 2005, 25:391-401.
27. Harding A.J., Halliday G.M., Kril J.J. Variation in hippocampal neuron number with age and brain volume. Cereb. Cortex 1998, 8:710-718.
28. Hayman L.A., Fuller G.N., Cavazos J.E., Pfleger M.J., Meyers C.A., Jackson E.F. The hippocampus: normal anatomy and pathology. AJR Am. J. Roentgenol. 1998, 171:1139-1146.
29. Jack C.R., Petersen R.C., O'Brien P.C., Tangalos E.G. MR-based hippocampal volumetry in the diagnosis of Alzheimer's disease. Neurology 1992, 42:183-188.
30. Jack C.R., Petersen R.C., Xu Y.C., Waring S.C., O'Brien P.C., Tangalos E.G., Smith G.E., Ivnik R.J., Kokmen E. Medial temporal atrophy on MRI in normal aging and very mild Alzheimer's disease. Neurology 1997, 49:786-794.
31. Kalpouzos G., Chételat G., Baron J.C., Landeau B., Mevel K., Godeau C., Barré L., Constans J.M., Viader F., Eustache F., Desgranges B. Voxel-based mapping of brain gray matter volume and glucose metabolism profiles in normal aging. Neurobiol. Aging 2009, 30:112-124.
32. Kennedy K.M., Raz N. Pattern of normal age-related regional differences in white matter microstructure is modified by vascular risk. Brain Res. 2009, 1297:41-56.
33. Lemaitre H., Crivello F., Grassiot B., Alperovitch A., Tzourio C., Mazoyer B. Age- and sex-related effects on the neuroanatomy of healthy elderly. Neuroimage 2005, 26:900-911.
34. Lepage M., Habib R., Tulving E. Hippocampal PET activations of memory encoding and retrieval: the HIPER model. Hippocampus 1998, 8:313-322.
35. Li Y., Li J., Segal S., Wegiel J., De S.S., Zhan J., de Leon M.J. Hippocampal cerebrospinal fluid spaces on MR imaging: relationship to aging and Alzheimer disease. AJNR Am. J. Neuroradiol. 2006, 27:912-918.
36. 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 1998, 280:921-924.
37. Malykhin N.V., Bouchard T.P., Camicioli R., Coupland N.J. Aging hippocampus and amygdala. NeuroReport 2008, 19:543-547.
38. Malykhin N.V., Lebel R.M., Coupland N.J., Wilman A.H., Carter R. In vivo quantification of hippocampal subfields using 4.7 T fast spin echo imaging. Neuroimage 2010, 49:1224-1230.
39. Mattis S. Mental status examination for organic mental syndrome in the elderly patient. Mental status examination for organic mental syndrome in the elderly patients 1976, 77-101. Grune & Stratton, New York. L. Bellack, T.B. Karasu (Eds.).
40. Mueller S.G., Weiner M.W. Selective effect of age, Apo e4, and Alzheimer's disease on hippocampal subfields. Hippocampus 2009, 19:558-564.
41. Mueller S.G., Stables L., Du A.T., Schuff N., Truran D., Cashdollar N., Weiner M.W. Measurement of hippocampal subfields and age-related changes with high resolution MRI at 4T. Neurobiol. Aging 2007, 28:719-726.
42. Mueller S.G., Schuff N., Raptentsetsang S., Elman J., Weiner M.W. Selective effect of Apo e4 on CA3 and dentate in normal aging and Alzheimer's disease using high resolution MRI at 4 T. Neuroimage 2008, 42:42-48.
43. Nakada T., Kwee I.L., Fujii Y., Knight R.T. High-field, T2 reversed MRI of the hippocampus in transient global amnesia. Neurology 2005, 64:1170-1174.
44. Pan J.W., Vaughan J.T., Kuzniecky R.I., Pohost G.M., Hetherington H.P. High resolution neuroimaging at 4.1T. Magn. Reson. Imaging 1995, 13:915-921.
45. Price J.L., Ko A.I., Wade M.J., Tsou S.K., McKeel D.W., Morris J.C. Neuron number in the entorhinal cortex and CA1 in preclinical Alzheimer disease. Arch. Neurol. 2001, 58:1395-1402.
46. Raji C.A., Lopez O.L., Kuller L.H., Carmichael O.T., Becker J.T. Age, Alzheimer disease, and brain structure. Neurology 2009, 73:1899-1905.
47. Ramani A., Jensen J.H., Helpern J.A. Quantitative MR imaging in Alzheimer disease. Radiology 2006, 241:26-44.
48. Raz N., Rodrigue K.M., Head D., Kennedy K.M., Acker J.D. Differential aging of the medial temporal lobe: a study of a five-year change. Neurology 2004, 62:433-438.
49. Seab J.P., Jagust W.J., Wong S.T., Roos M.S., Reed B.R., Budinger T.F. Quantitative NMR measurements of hippocampal atrophy in Alzheimer's disease. Magn. Reson. Med. 1988, 8:200-208.
50. Sicotte N.L., Kern K.C., Giesser B.S., Arshanapalli A., Schultz A., Montag M., Wang H., Bookheimer S.Y. Regional hippocampal atrophy in multiple sclerosis. Brain 2008, 131:1134-1141.
51. Simic G., Kostovic I., Winblad B., Bogdanovic N. Volume and number of neurons of the human hippocampal formation in normal aging and Alzheimer's disease. J. Comp. Neurol. 1997, 379:482-494.
52. Spaniol J., Davidson P.S., Kim A.S., Han H., Moscovitch M., Grady C.L. Event-related fMRI studies of episodic encoding and retrieval: meta-analyses using activation likelihood estimation. Neuropsychologia 2009, 47:1765-1779.
53. Squire L.R., Ojemann J.G., Miezin F.M., Petersen S.E., Videen T.O., Raichle M.E. Activation of the hippocampus in normal humans: a functional anatomical study of memory. Proc. Natl Acad. Sci. USA 1992, 89:1837-1841.
54. Sullivan E.V., Marsh L., Pfefferbaum A. Preservation of hippocampal volume throughout adulthood in healthy men and women. Neurobiol. Aging 2005, 26:1093-1098.
55. Suthana N.A., Ekstrom A.D., Moshirvaziri S., Knowlton B., Bookheimer S.Y. Human hippocampal CA1 involvement during allocentric encoding of spatial information. J. Neurosci. 2009, 29:10512-10519.
56. Theysohn J.M., Kraff O., Maderwald S., Schlamann M.U., de, G.A., Forsting M., Ladd S.C., Ladd M.E., Gizewski E.R. The human hippocampus at 7 T-in vivo MRI. Hippocampus 2009, 19:1-7.
57. Thomas B.P., Welch E.B., Niederhauser B.D., Whetsell W.O., Anderson A.W., Gore J.C., Avison M.J., Creasy J.L. High-resolution 7T MRI of the human hippocampus in vivo. J. Magn. Reson. Imaging 2008, 28:1266-1272.
58. Thompson P.M., Hayashi K.M., De Zubicaray G.I., Janke A.L., Rose S.E., Semple J., Hong M.S., Herman D.H., Gravano D., Doddrell D.M., Toga A.W. Mapping hippocampal and ventricular change in Alzheimer disease. Neuroimage 2004, 22:1754-1766.
59. Tulving E., Markowitsch H.J. Episodic and declarative memory: role of the hippocampus. Hippocampus 1998, 8:198-204.
60. Van Leemput K., Bakkour A., Benner T., Wiggins G., Wald L.L., Augustinack J., Dickerson B.C., Golland P., Fischl B. Automated segmentation of hippocampal subfields from ultra-high resolution in vivo MRI. Hippocampus 2009, 19:549-557.
61. Wang L., Swank J.S., Glick I.E., Gado M.H., Miller M.I., Morris J.C., Csernansky J.G. Changes in hippocampal volume and shape across time distinguish dementia of the Alzheimer type from healthy aging. Neuroimage 2003, 20:667-682.
62. 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, 30:52-60.
63. West M.J., Coleman P.D., Flood D.G., Troncoso J.C. Differences in the pattern of hippocampal neuronal loss in normal ageing and Alzheimer's disease. Lancet 1994, 344:769-772.
64. Yassa M.A., Stark C.E. A quantitative evaluation of cross-participant registration techniques for MRI studies of the medial temporal lobe. Neuroimage 2009, 44:319-327.
65. Yoneoka Y., Kwee I.L., Fujii Y., Nakada T. Criteria for normalcy of cavities observed within the adult hippocampus: high-resolution magnetic resonance imaging study on a 3.0-T system. J. Neuroimaging 2002, 12:231-235.
66. Yushkevich P.A., Avants B.B., Pluta J., Das S., Minkoff D., Mechanic-Hamilton D., Glynn S., Pickup S., Liu W., Gee J.C., Grossman M., Detre J.A. A high-resolution computational atlas of the human hippocampus from postmortem magnetic resonance imaging at 9.4 T. Neuroimage 2009, 44:385-398.
67. 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, 299:577-580.