Brain Imaging and Behavior

, Volume 6, Issue 4, pp 551–567

Voxel and surface-based topography of memory and executive deficits in mild cognitive impairment and Alzheimer’s disease

  • Kwangsik Nho
  • Shannon L. Risacher
  • Paul K. Crane
  • Charles DeCarli
  • M. Maria Glymour
  • Christian Habeck
  • Sungeun Kim
  • Grace J. Lee
  • Elizabeth Mormino
  • Shubhabrata Mukherjee
  • Li Shen
  • John D. West
  • Andrew J. Saykin
  • Alzheimer’s Disease Neuroimaging Initiative (ADNI)
ADNI: Friday Harbor 2011 Workshop SPECIAL ISSUE

Abstract

Mild cognitive impairment (MCI) and Alzheimer’s disease (AD) are associated with a progressive loss of cognitive abilities. In the present report, we assessed the relationship of memory and executive function with brain structure in a sample of 810 Alzheimer’s Disease Neuroimaging Initiative (ADNI) participants, including 188 AD, 396 MCI, and 226 healthy older adults (HC). Composite scores of memory (ADNI-Mem) and executive function (ADNI-Exec) were generated by applying modern psychometric theory to item-level data from ADNI’s neuropsychological battery. We performed voxel-based morphometry (VBM) and surface-based association (SurfStat) analyses to evaluate relationships of ADNI-Mem and ADNI-Exec with grey matter (GM) density and cortical thickness across the whole brain in the combined sample and within diagnostic groups. We observed strong associations between ADNI-Mem and medial and lateral temporal lobe atrophy. Lower ADNI-Exec scores were associated with advanced GM and cortical atrophy across broadly distributed regions, most impressively in the bilateral parietal and temporal lobes. We also evaluated ADNI-Exec adjusted for ADNI-Mem, and found associations with GM density and cortical thickness primarily in the bilateral parietal, temporal, and frontal lobes. Within-group analyses suggest these associations are strongest in patients with MCI and AD. The present study provides insight into the spatially unbiased associations between brain atrophy and memory and executive function, and underscores the importance of structural brain changes in early cognitive decline.

Keywords

Voxel-based morphometry (VBM) Surface-based analysis Memory Executive function Alzheimer’s disease Mild cognitive impairment 

References

  1. Albert, M. S., DeKosky, S. T., Dickson, D., Dubois, B., Feldman, H. H., Fox, N. C., et al. (2011). The diagnosis of mild cognitive impairment due to Alzheimer’s disease: recommendations from the National Institute on Aging-Alzheimer’s Association workgroups on diagnostic guidelines for Alzheimer’s disease. Alzheimer’s & Dementia, 7(3), 270–279.CrossRefGoogle Scholar
  2. Amici, S., Ogar, J., Brambati, S. M., Miller, B. L., Neuhaus, J., Dronkers, N. L., et al. (2007). Performance in specific language tasks correlates with regional volume changes in progressive aphasia. Cognitive and Behavioral Neurology, 20(4), 203–211.PubMedCrossRefGoogle Scholar
  3. Apostolova, L. G., Lu, P., Rogers, S., Dutton, R. A., Hayashi, K. M., Toga, A. W., et al. (2008). 3D mapping of language networks in clinical and pre-clinical Alzheimer’s disease. Brain and Language, 104(1), 33–41.PubMedCrossRefGoogle Scholar
  4. Apostolova, L. G., Morra, J. H., Green, A. E., Hwang, K. S., Avedissian, C., Woo, E., et al. (2010). Automated 3D mapping of baseline and 12-month associations between three verbal memory measures and hippocampal atrophy in 490 ADNI subjects. NeuroImage, 51(1), 488–499.PubMedCrossRefGoogle Scholar
  5. Armstrong, R. A. (2009). The molecular biology of senile plaques and neurofibrillary tangles in Alzheimer’s disease. Folia Neuropathologica, 47(4), 289–299.PubMedGoogle Scholar
  6. Ashburner, J., & Friston, K. J. (2000). Voxel-based morphometry—the methods. NeuroImage, 11(6 Pt 1), 805–821.PubMedCrossRefGoogle Scholar
  7. Barbeau, E. J., Ranjeva, J. P., Didic, M., Confort-Gouny, S., Felician, O., Soulier, E., et al. (2008). Profile of memory impairment and gray matter loss in amnestic mild cognitive impairment. Neuropsychologia, 46(4), 1009–1019.PubMedCrossRefGoogle Scholar
  8. Berlingeri, M., Bottini, G., Basilico, S., Silani, G., Zanardi, G., Sberna, M., et al. (2008). Anatomy of the episodic buffer: a voxel-based morphometry study in patients with dementia. Behavioural Neurology, 19(1–2), 29–34.PubMedGoogle Scholar
  9. Braak, H., & Braak, E. (1996). Evolution of the neuropathology of Alzheimer’s disease. Acta Neurologica Scandinavica. Supplementum, 165, 3–12.PubMedCrossRefGoogle Scholar
  10. Braak, H., Braak, E., & Bohl, J. (1993). Staging of Alzheimer-related cortical destruction. European Neurology, 33(6), 403–408.PubMedCrossRefGoogle Scholar
  11. Braak, H., Braak, E., Yilmazer, D., de Vos, R. A., Jansen, E. N., & Bohl, J. (1996). Pattern of brain destruction in Parkinson’s and Alzheimer’s diseases. Journal of Neural Transmission, 103(4), 455–490.PubMedCrossRefGoogle Scholar
  12. Brambati, S. M., Myers, D., Wilson, A., Rankin, K. P., Allison, S. C., Rosen, H. J., et al. (2006). The anatomy of category-specific object naming in neurodegenerative diseases. Journal of Cognitive Neuroscience, 18(10), 1644–1653.PubMedCrossRefGoogle Scholar
  13. Braskie, M. N., Small, G. W., & Bookheimer, S. Y. (2009). Entorhinal cortex structure and functional MRI response during an associative verbal memory task. Human Brain Mapping, 30(12), 3981–3992.PubMedCrossRefGoogle Scholar
  14. Cabeza, R. (2008). Role of parietal regions in episodic memory retrieval: the dual attentional processes hypothesis. Neuropsychologia, 46(7), 1813–1827.PubMedCrossRefGoogle Scholar
  15. Cabeza, R., & Nyberg, L. (2000). Imaging cognition II: an empirical review of 275 PET and fMRI studies. Journal of Cognitive Neuroscience, 12(1), 1–47.PubMedCrossRefGoogle Scholar
  16. Cabeza, R., Ciaramelli, E., Olson, I. R., & Moscovitch, M. (2008). The parietal cortex and episodic memory: an attentional account. Nature Reviews Neuroscience, 9(8), 613–625.PubMedCrossRefGoogle Scholar
  17. Cahn-Weiner, D. A., Sullivan, E. V., Shear, P. K., Fama, R., Lim, K. O., Yesavage, J. A., et al. (1999). Brain structural and cognitive correlates of clock drawing performance in Alzheimer’s disease. Journal of International Neuropsychological Society, 5(6), 502–509.CrossRefGoogle Scholar
  18. Chang, Y. L., Bondi, M. W., Fennema-Notestine, C., McEvoy, L. K., Hagler, D. J., Jr., Jacobson, M. W., et al. (2010). Brain substrates of learning and retention in mild cognitive impairment diagnosis and progression to Alzheimer’s disease. Neuropsychologia, 48(5), 1237–1247.PubMedCrossRefGoogle Scholar
  19. Chang, Y. L., Jacobson, M. W., Fennema-Notestine, C., Hagler, D. J., Jr., Jennings, R. G., Dale, A. M., et al. (2010). Level of executive function influences verbal memory in amnestic mild cognitive impairment and predicts prefrontal and posterior cingulate thickness. Cerebral Cortex, 20(6), 1305–1313.PubMedCrossRefGoogle Scholar
  20. Chetelat, G., Desgranges, B., de la Sayette, V., Viader, F., Berkouk, K., Landeau, B., et al. (2003). Dissociating atrophy and hypometabolism impact on episodic memory in mild cognitive impairment. Brain, 126(Pt 9), 1955–1967.PubMedCrossRefGoogle Scholar
  21. Chetelat, G., Villemagne, V. L., Pike, K. E., Ellis, K. A., Bourgeat, P., Jones, G., et al. (2011). Independent contribution of temporal beta-amyloid deposition to memory decline in the pre-dementia phase of Alzheimer’s disease. Brain, 134(Pt 3), 798–807.PubMedCrossRefGoogle Scholar
  22. Chiang, G. C., Insel, P. S., Tosun, D., Schuff, N., Truran-Sacrey, D., Raptentsetsang, S., et al. (2011). Identifying cognitively healthy elderly individuals with subsequent memory decline by using automated MR temporoparietal volumes. Radiology, 259(3), 844–851.PubMedCrossRefGoogle Scholar
  23. Chou, Y. Y., Lepore, N., Avedissian, C., Madsen, S. K., Parikshak, N., Hua, X., et al. (2009). Mapping correlations between ventricular expansion and CSF amyloid and tau biomarkers in 240 subjects with Alzheimer’s disease, mild cognitive impairment and elderly controls. NeuroImage, 46(2), 394–410.PubMedCrossRefGoogle Scholar
  24. Chou, Y. Y., Lepore, N., Saharan, P., Madsen, S. K., Hua, X., Jack, C. R., et al. (2010). Ventricular maps in 804 ADNI subjects: correlations with CSF biomarkers and clinical decline. Neurobiology of Aging, 31(8), 1386–1400.PubMedCrossRefGoogle Scholar
  25. Cockrell, J. R., & Folstein, M. F. (1988). Mini-Mental State Examination (MMSE). Psychopharmacology Bulletin, 24(4), 689–692.PubMedGoogle Scholar
  26. Convit, A., de Asis, J., de Leon, M. J., Tarshish, C. Y., De Santi, S., & Rusinek, H. (2000). Atrophy of the medial occipitotemporal, inferior, and middle temporal gyri in non-demented elderly predict decline to Alzheimer’s disease. Neurobiology of Aging, 21(1), 19–26.PubMedCrossRefGoogle Scholar
  27. Costafreda, S. G., Fu, C. H., Lee, L., Everitt, B., Brammer, M. J., & David, A. S. (2006). A systematic review and quantitative appraisal of fMRI studies of verbal fluency: role of the left inferior frontal gyrus. Human Brain Mapping, 27(10), 799–810.PubMedCrossRefGoogle Scholar
  28. Crane, P. K., Carle, A., Gibbons L. E., et al. (2012). Development and assessment of a composite score for memory in the Alzheimer’s Disease Neuroimaging Initiative (ADNI). Brain Imaging and Behavior. doi:10.1007/s11682-012-9186-z.
  29. Crane, P. K., Narasimhalu, K., Gibbons, L. E., Pedraza, O., Mehta, K. M., Tang, Y., et al. (2008). Composite scores for executive function items: demographic heterogeneity and relationships with quantitative magnetic resonance imaging. Journal of International Neuropsychological Society, 14(5), 746–759.CrossRefGoogle Scholar
  30. Dale, A., Fischl, B., & Sereno, M. (1999). Cortical surface-based analysis. I. Segmentation and surface reconstruction. NeuroImage, 9(2), 179–194.PubMedCrossRefGoogle Scholar
  31. Deweer, B., Lehericy, S., Pillon, B., Baulac, M., Chiras, J., Marsault, C., et al. (1995). Memory disorders in probable Alzheimer’s disease: the role of hippocampal atrophy as shown with MRI. Journal of Neurology, Neurosurgery, and Psychiatry, 58(5), 590–597.PubMedCrossRefGoogle Scholar
  32. Di Paola, M., Macaluso, E., Carlesimo, G. A., Tomaiuolo, F., Worsley, K. J., Fadda, L., et al. (2007). Episodic memory impairment in patients with Alzheimer’s disease is correlated with entorhinal cortex atrophy. A voxel-based morphometry study. Journal of Neurology, 254(6), 774–781.PubMedCrossRefGoogle Scholar
  33. Dickerson, B. C., & Wolk, D. A. (2011). Dysexecutive versus amnesic phenotypes of very mild Alzheimer’s disease are associated with distinct clinical, genetic and cortical thinning characteristics. Journal of Neurology, Neurosurgery, and Psychiatry, 82(1), 45–51.PubMedCrossRefGoogle Scholar
  34. Epstein, N. U., Saykin, A. J., Risacher, S. L., Gao, S., & Farlow, M. R. (2010). Differences in medication use in the Alzheimer’s disease neuroimaging initiative: analysis of baseline characteristics. Drugs & Aging, 27(8), 677–686.CrossRefGoogle Scholar
  35. Evans, M. C., Barnes, J., Nielsen, C., Kim, L. G., Clegg, S. L., Blair, M., et al. (2010). Volume changes in Alzheimer’s disease and mild cognitive impairment: cognitive associations. European Radiology, 20(3), 674–682.PubMedCrossRefGoogle Scholar
  36. Fischl, B., & Dale, A. M. (2000). Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proceedings of the National Academy of Sciences of the United States of America, 97(20), 11050–11055.PubMedCrossRefGoogle Scholar
  37. Fischl, B., Sereno, M., & Dale, A. (1999). Cortical surface-based analysis. II: inflation, flattening, and a surface-based coordinate system. NeuroImage, 9(2), 195–207.PubMedCrossRefGoogle Scholar
  38. Fischl, B., Salat, D., Busa, E., Albert, M., Dieterich, M., Haselgrove, C., et al. (2002). Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron, 33(3), 341–355.PubMedCrossRefGoogle Scholar
  39. Folstein, M. F., Folstein, S. E., & McHugh, P. R. (1975). Mini-mental state. A practical method for grading the cognitive state of patients for the clinician. Journal of Psychiatric Research, 12(3), 189–198.PubMedCrossRefGoogle Scholar
  40. Fox, N. C., Warrington, E. K., Freeborough, P. A., Hartikainen, P., Kennedy, A. M., Stevens, J. M., et al. (1996). Presymptomatic hippocampal atrophy in Alzheimer’s disease. A longitudinal MRI study. Brain, 119(Pt 6), 2001–2007.PubMedCrossRefGoogle Scholar
  41. Gibbons, L. E., Carle, A. C., Mackin, R. S., Harvey, D., et al. (2012). A composite score for executive functioning, validated in Alzheimer’s Disease Neuroimaging Initiative (ADNI) participants with baseline mild cognitive impairment. Brain Imaging and Behavior. doi:10.1007/s11682-012-9176-1.
  42. Good, C. D., Johnsrude, I. S., Ashburner, J., Henson, R. N., Friston, K. J., & Frackowiak, R. S. (2001). A voxel-based morphometric study of ageing in 465 normal adult human brains. NeuroImage, 14(1 Pt 1), 21–36.PubMedCrossRefGoogle Scholar
  43. Goodglass, H., & Kaplan, E. (1983). The assessment of aphasia and related disorders. Philadelphia: Lea & Febiger.Google Scholar
  44. Goto, M., Abe, O., Miyati, T., Yoshikawa, T., Hayashi, N., Takao, H., et al. (2011). Entorhinal cortex volume measured with 3 T MRI is positively correlated with the Wechsler Memory Scale-Revised logical/verbal memory score for healthy subjects. Neuroradiology, 53(8), 617–622.PubMedCrossRefGoogle Scholar
  45. Grady, C. L., McIntosh, A. R., Beig, S., Keightley, M. L., Burian, H., & Black, S. E. (2003). Evidence from functional neuroimaging of a compensatory prefrontal network in Alzheimer’s disease. Journal of Neuroscience, 23(3), 986–993.PubMedGoogle Scholar
  46. Greene, S. J., & Killiany, R. J. (2010). Subregions of the inferior parietal lobule are affected in the progression to Alzheimer’s disease. Neurobiology of Aging, 31(8), 1304–1311.PubMedCrossRefGoogle Scholar
  47. Greene, S. J., & Killiany, R. J. (2011). Hippocampal subregions are differentially affected in the progression to alzheimer’s disease. Anatomical Record (Hoboken).Google Scholar
  48. Grossman, M., McMillan, C., Moore, P., Ding, L., Glosser, G., Work, M., et al. (2004). What’s in a name: voxel-based morphometric analyses of MRI and naming difficulty in Alzheimer’s disease, frontotemporal dementia and corticobasal degeneration. Brain, 127(Pt 3), 628–649.PubMedGoogle Scholar
  49. Hackert, V. H., den Heijer, T., Oudkerk, M., Koudstaal, P. J., Hofman, A., & Breteler, M. M. (2002). Hippocampal head size associated with verbal memory performance in nondemented elderly. NeuroImage, 17(3), 1365–1372.PubMedCrossRefGoogle Scholar
  50. Hamalainen, A., Pihlajamaki, M., Tanila, H., Hanninen, T., Niskanen, E., Tervo, S., et al. (2007). Increased fMRI responses during encoding in mild cognitive impairment. Neurobiology of Aging, 28(12), 1889–1903.PubMedCrossRefGoogle Scholar
  51. Hardy, J., & Selkoe, D. J. (2002). The amyloid hypothesis of Alzheimer’s disease: progress and problems on the road to therapeutics. Science, 297(5580), 353–356.PubMedCrossRefGoogle Scholar
  52. Hart, J., Jr., Anand, R., Zoccoli, S., Maguire, M., Gamino, J., Tillman, G., et al. (2007). Neural substrates of semantic memory. Journal of International Neuropsychological Society, 13(5), 865–880.CrossRefGoogle Scholar
  53. Hirono, N., Mori, E., Ishii, K., Imamura, T., Tanimukai, S., Kazui, H., et al. (2001). Neuronal substrates for semantic memory: a positron emission tomography study in Alzheimer’s disease. Dementia and Geriatric Cognitive Disorders, 12(1), 15–21.PubMedCrossRefGoogle Scholar
  54. Holtzman, D. M., Morris, J. C., & Goate, A. M. (2011). Alzheimer’s disease: the challenge of the second century. Science Translational Medicine, 3(77), 77sr71.CrossRefGoogle Scholar
  55. Hua, X., Leow, A. D., Parikshak, N., Lee, S., Chiang, M. C., Toga, A. W., et al. (2008). Tensor-based morphometry as a neuroimaging biomarker for Alzheimer’s disease: an MRI study of 676 AD, MCI, and normal subjects. NeuroImage, 43(3), 458–469.PubMedCrossRefGoogle Scholar
  56. Huey, E. D., Goveia, E. N., Paviol, S., Pardini, M., Krueger, F., Zamboni, G., et al. (2009). Executive dysfunction in frontotemporal dementia and corticobasal syndrome. Neurology, 72(5), 453–459.PubMedCrossRefGoogle Scholar
  57. Ino, T., Asada, T., Ito, J., Kimura, T., & Fukuyama, H. (2003). Parieto-frontal networks for clock drawing revealed with fMRI. Neurosciences Research, 45(1), 71–77.CrossRefGoogle Scholar
  58. Jack, C. R., Jr., Lowe, V. J., Weigand, S. D., Wiste, H. J., Senjem, M. L., Knopman, D. S., et al. (2009). Serial PIB and MRI in normal, mild cognitive impairment and Alzheimer’s disease: implications for sequence of pathological events in Alzheimer’s disease. Brain, 132(Pt 5), 1355–1365.PubMedCrossRefGoogle Scholar
  59. Jagust, W., Gitcho, A., Sun, F., Kuczynski, B., Mungas, D., & Haan, M. (2006). Brain imaging evidence of preclinical Alzheimer’s disease in normal aging. Annals of Neurology, 59(4), 673–681.PubMedCrossRefGoogle Scholar
  60. Juottonen, K., Laakso, M. P., Insausti, R., Lehtovirta, M., Pitkanen, A., Partanen, K., et al. (1998). Volumes of the entorhinal and perirhinal cortices in Alzheimer’s disease. Neurobiology of Aging, 19(1), 15–22.PubMedCrossRefGoogle Scholar
  61. Kato, T., Knopman, D., & Liu, H. (2001). Dissociation of regional activation in mild AD during visual encoding: a functional MRI study. Neurology, 57, 812–816.PubMedCrossRefGoogle Scholar
  62. King, R. D., Brown, B., Hwang, M., Jeon, T., & George, A. T. (2010). Fractal dimension analysis of the cortical ribbon in mild Alzheimer’s disease. NeuroImage, 53(2), 471–479.PubMedCrossRefGoogle Scholar
  63. Knopman, D. S., DeKosky, S. T., Cummings, J. L., Chui, H., Corey-Bloom, J., Relkin, N., et al. (2001). Practice parameter: diagnosis of dementia (an evidence-based review). Report of the Quality Standards Subcommittee of the American Academy of Neurology. Neurology, 56(9), 1143–1153.PubMedCrossRefGoogle Scholar
  64. Kovacevic, S., Rafii, M. S., & Brewer, J. B. (2009). High-throughput, fully automated volumetry for prediction of MMSE and CDR decline in mild cognitive impairment. Alzheimer Disease and Associated Disorders, 23(2), 139–145.PubMedCrossRefGoogle Scholar
  65. Kramer, J. H., Quitania, L., Dean, D., Neuhaus, J., Rosen, H. J., Halabi, C., et al. (2007). Magnetic resonance imaging correlates of set shifting. Journal of International Neuropsychological Society, 13(3), 386–392.CrossRefGoogle Scholar
  66. Laakso, M. P., Soininen, H., Partanen, K., Helkala, E. L., Hartikainen, P., Vainio, P., et al. (1995). Volumes of hippocampus, amygdala and frontal lobes in the MRI-based diagnosis of early Alzheimer’s disease: correlation with memory functions. Journal of Neural Transmission. Parkinson’s Disease and Dementia Section, 9(1), 73–86.PubMedCrossRefGoogle Scholar
  67. Leow, A. D., Yanovsky, I., Parikshak, N., Hua, X., Lee, S., Toga, A. W., et al. (2009). Alzheimer’s disease neuroimaging initiative: a one-year follow up study using tensor-based morphometry correlating degenerative rates, biomarkers and cognition. NeuroImage, 45(3), 645–655.PubMedCrossRefGoogle Scholar
  68. Leube, D. T., Weis, S., Freymann, K., Erb, M., Jessen, F., Heun, R., et al. (2008). Neural correlates of verbal episodic memory in patients with MCI and Alzheimer’s disease—a VBM study. International Journal of Geriatric Psychiatry, 23(11), 1114–1118.PubMedCrossRefGoogle Scholar
  69. Lo, R. Y., Hubbard, A. E., Shaw, L. M., Trojanowski, J. Q., Petersen, R. C., Aisen, P. S., et al. (2011). Longitudinal change of biomarkers in cognitive decline. Archives of Neurology, 68(10), 1257–1266.PubMedCrossRefGoogle Scholar
  70. Madsen, S. K., Ho, A. J., Hua, X., Saharan, P. S., Toga, A. W., Jack, C. R., Jr., et al. (2010). 3D maps localize caudate nucleus atrophy in 400 Alzheimer’s disease, mild cognitive impairment, and healthy elderly subjects. Neurobiology of Aging, 31(8), 1312–1325.PubMedCrossRefGoogle Scholar
  71. McDonald, C. R., Gharapetian, L., McEvoy, L. K., Fennema-Notestine, C., Hagler, D. J., Jr., Holland, D., et al. (2012). Relationship between regional atrophy rates and cognitive decline in mild cognitive impairment. Neurobiology of Aging, 33(2), 242–253.PubMedCrossRefGoogle Scholar
  72. McKhann, G., Drachman, D., Folstein, M., Katzman, R., Price, D., & Stadlan, E. M. (1984). Clinical diagnosis of Alzheimer’s disease: report of the NINCDS-ADRDA work group under the auspices of Health and Human Services Task Force on Alzheimer’s Disease. Neurology, 34, 939–944.PubMedCrossRefGoogle Scholar
  73. McKhann, G. M., Knopman, D. S., Chertkow, H., Hyman, B. T., Jack, C. R., Jr., Kawas, C. H., et al. (2011). The diagnosis of dementia due to Alzheimer’s disease: recommendations from the National Institute on Aging-Alzheimer’s Association workgroups on diagnostic guidelines for Alzheimer’s disease. Alzheimer’s & Dementia, 7(3), 263–269.CrossRefGoogle Scholar
  74. Mechelli, A. P., Price, C. J., Friston, K. J., & Ashburner, J. (2005). Voxel-based morphometry of the human brain: methods and applications. Current Medical Imaging Reviews, 1(1), 1–9.CrossRefGoogle Scholar
  75. Minati, L., Edginton, T., Bruzzone, M. G., & Giaccone, G. (2009). Current concepts in Alzheimer’s disease: a multidisciplinary review. American Journal of Alzheimer’s Disease and Other Dementias, 24(2), 95–121.PubMedCrossRefGoogle Scholar
  76. Mohs, R. C. (1994). Administration and scoring manual for the Alzheimer’s Disease Assessment Scale, 1994 revised edition.Google Scholar
  77. Moll, J., de Oliveira-Souza, R., Moll, F. T., Bramati, I. E., & Andreiuolo, P. A. (2002). The cerebral correlates of set-shifting: an fMRI study of the trail making test. Arquivos de Neuro-Psiquiatria, 60(4), 900–905.PubMedCrossRefGoogle Scholar
  78. Monchi, O., Petrides, M., Petre, V., Worsley, K., & Dagher, A. (2001). Wisconsin Card Sorting revisited: distinct neural circuits participating in different stages of the task identified by event-related functional magnetic resonance imaging. Journal of Neuroscience, 21(19), 7733–7741.PubMedGoogle Scholar
  79. Mormino, E. C., Kluth, J. T., Madison, C. M., Rabinovici, G. D., Baker, S. L., Miller, B. L., et al. (2009). Episodic memory loss is related to hippocampal-mediated beta-amyloid deposition in elderly subjects. Brain, 132(Pt 5), 1310–1323.PubMedCrossRefGoogle Scholar
  80. Morra, J. H., Tu, Z., Apostolova, L. G., Green, A. E., Avedissian, C., Madsen, S. K., et al. (2009a). Automated 3D mapping of hippocampal atrophy and its clinical correlates in 400 subjects with Alzheimer’s disease, mild cognitive impairment, and elderly controls. Human Brain Mapping, 30(9), 2766–2788.PubMedCrossRefGoogle Scholar
  81. Morra, J. H., Tu, Z., Apostolova, L. G., Green, A. E., Avedissian, C., Madsen, S. K., et al. (2009b). Automated mapping of hippocampal atrophy in 1-year repeat MRI data from 490 subjects with Alzheimer’s disease, mild cognitive impairment, and elderly controls. NeuroImage, 45(1 Suppl), S3–S15.PubMedCrossRefGoogle Scholar
  82. Morris, J. C. (1993). The Clinical Dementia Rating (CDR): current version and scoring rules. Neurology, 43(11), 2412–2414.PubMedCrossRefGoogle Scholar
  83. Morris, J., Heyman, A., Mohs, R., Hughes, J., van Belle, G., Fillenbaum, G., et al. (1989). The Consortium to Establish a Registry for Alzheimer’s Disease (CERAD). Part I. Clinical and neuropsychological assessment of Alzheimer’s disease. Neurology, 39(9), 1159–1165.PubMedCrossRefGoogle Scholar
  84. Mueller, S. G., Weiner, M. W., Thal, L. J., Petersen, R. C., Jack, C., Jagust, W., et al. (2005a). The Alzheimer’s disease neuroimaging initiative. Neuroimaging Clinics of North America, 15(4), 869–877.PubMedCrossRefGoogle Scholar
  85. Mueller, S. G., Weiner, M. W., Thal, L. J., Petersen, R. C., Jack, C. R., Jagust, W., et al. (2005b). Ways toward an early diagnosis in Alzheimer’s disease: the Alzheimer’s Disease Neuroimaging Initiative (ADNI). Alzheimer’s & Dementia, 1(1), 55–66.CrossRefGoogle Scholar
  86. Murphy, E. A., Holland, D., Donohue, M., McEvoy, L. K., Hagler, D. J., Jr., Dale, A. M., et al. (2010). Six-month atrophy in MTL structures is associated with subsequent memory decline in elderly controls. NeuroImage, 53(4), 1310–1317.PubMedCrossRefGoogle Scholar
  87. Nestor, S. M., Rupsingh, R., Borrie, M., Smith, M., Accomazzi, V., Wells, J. L., et al. (2008). Ventricular enlargement as a possible measure of Alzheimer’s disease progression validated using the Alzheimer’s disease neuroimaging initiative database. Brain, 131(Pt 9), 2443–2454.PubMedCrossRefGoogle Scholar
  88. Nettiksimmons, J., Harvey, D., Brewer, J., Carmichael, O., DeCarli, C., Jack, C. R., Jr., et al. (2010). Subtypes based on cerebrospinal fluid and magnetic resonance imaging markers in normal elderly predict cognitive decline. Neurobiology of Aging, 31(8), 1419–1428.PubMedCrossRefGoogle Scholar
  89. Newman, L. M., Trivedi, M. A., Bendlin, B. B., Ries, M. L., & Johnson, S. C. (2007). The relationship between gray matter morphometry and neuropsychological performance in a large sample of cognitively healthy adults. Brain Imaging and Behavior, 1(1–2), 3–10.PubMedCrossRefGoogle Scholar
  90. Oh, H., Mormino, E. C., Madison, C., Hayenga, A., Smiljic, A., & Jagust, W. J. (2011). Beta-amyloid affects frontal and posterior brain networks in normal aging. NeuroImage, 54(3), 1887–1895.PubMedCrossRefGoogle Scholar
  91. Pa, J., Boxer, A., Chao, L. L., Gazzaley, A., Freeman, K., Kramer, J., et al. (2009). Clinical-neuroimaging characteristics of dysexecutive mild cognitive impairment. Annals of Neurology, 65(4), 414–423.PubMedCrossRefGoogle Scholar
  92. Pa, J., Possin, K. L., Wilson, S. M., Quitania, L. C., Kramer, J. H., Boxer, A. L., et al. (2010). Gray matter correlates of set-shifting among neurodegenerative disease, mild cognitive impairment, and healthy older adults. Journal of International Neuropsychological Society, 16(4), 640–650.CrossRefGoogle Scholar
  93. Pantel, J., Schonknecht, P., Essig, M., & Schroder, J. (2004). Distribution of cerebral atrophy assessed by magnetic resonance imaging reflects patterns of neuropsychological deficits in Alzheimer’s dementia. Neuroscience Letters, 361(1–3), 17–20.PubMedCrossRefGoogle Scholar
  94. Park, H., & Seo, J. (2011). Application of multidimensional scaling to quantify shape in Alzheimer’s disease and its correlation with Mini Mental State Examination: a feasibility study. Journal of Neuroscience Methods, 194(2), 380–385.PubMedCrossRefGoogle Scholar
  95. Petersen, R. C. (2000). Mild cognitive impairment: transition between aging and Alzheimer’s disease. Neurologia, 15(3), 93–101.PubMedGoogle Scholar
  96. Petersen, R. C., Smith, G. E., Waring, S. C., Ivnik, R. J., Tangalos, E. G., & Kokmen, E. (1999). Mild cognitive impairment: clinical characterization and outcome. Archives of Neurology, 56(3), 303–308.PubMedCrossRefGoogle Scholar
  97. Petersen, R. C., Jack, C. R., Jr., Xu, Y. C., Waring, S. C., O’Brien, P. C., Smith, G. E., et al. (2000). Memory and MRI-based hippocampal volumes in aging and AD. Neurology, 54(3), 581–587.PubMedCrossRefGoogle Scholar
  98. Poulin, S. P., Dautoff, R., Morris, J. C., Barrett, L. F., & Dickerson, B. C. (2011). Amygdala atrophy is prominent in early Alzheimer’s disease and relates to symptom severity. Psychiatry Research, 194(1), 7–13.PubMedCrossRefGoogle Scholar
  99. Rabin, L. A., Saykin, A. J., West, J. D., Borgos, M. J., Wishart, H. A., Nutter-Upham, K. E., et al. (2009). Judgement in older adults with normal cognition, cognitive complaints, MCI, and mild AD: relation to regional frontal grey matter. Brain Imaging and Behavior, 3(2), 212–219.CrossRefGoogle Scholar
  100. Reitan, R., & Wolfson, D. (1985). The Halstead-Reitan Neuropsychological Test Battery. Tucson: Neuropsychology Press.Google Scholar
  101. Remy, F., Mirrashed, F., Campbell, B., & Richter, W. (2005). Verbal episodic memory impairment in Alzheimer’s disease: a combined structural and functional MRI study. NeuroImage, 25(1), 253–266.PubMedCrossRefGoogle Scholar
  102. Rey, A. (1964). L’examen clinique en psychologie. Paris: Presses Universitaires de France.Google Scholar
  103. Risacher, S. L., Saykin, A. J., West, J. D., Shen, L., Firpi, H. A., & McDonald, B. C. (2009). Baseline MRI predictors of conversion from MCI to probable AD in the ADNI cohort. Current Alzheimer Research, 6(4), 347–361.PubMedCrossRefGoogle Scholar
  104. Risacher, S. L., Shen, L., West, J. D., Kim, S., McDonald, B. C., Beckett, L. A., et al. (2010). Longitudinal MRI atrophy biomarkers: relationship to conversion in the ADNI cohort. Neurobiology of Aging, 31(8), 1401–1418.PubMedCrossRefGoogle Scholar
  105. Risacher, S. L., Wishart, H. A., & Saykin, A. J. (2011). Functional MRI studies of memory in aging, mild cognitive impairment, and Alzheimer’s disease. In S. H. Faro & F. B. Mohamed (Eds.), Functional neuroradiology (2nd ed.). New York: Springer.Google Scholar
  106. Rombouts, S. A., Barkhof, F., Veltman, D. J., Machielsen, W. C., Witter, M. P., Bierlaagh, M. A., et al. (2000). Functional MR imaging in Alzheimer’s disease during memory encoding. AJNR. American Journal of Neuroradiology, 21(10), 1869–1875.PubMedGoogle Scholar
  107. Rushworth, M. F., Hadland, K. A., Paus, T., & Sipila, P. K. (2002). Role of the human medial frontal cortex in task switching: a combined fMRI and TMS study. Journal of Neurophysiology, 87(5), 2577–2592.PubMedGoogle Scholar
  108. Rusinek, H., De Santi, S., Frid, D., Tsui, W. H., Tarshish, C. Y., Convit, A., et al. (2003). Regional brain atrophy rate predicts future cognitive decline: 6-year longitudinal MR imaging study of normal aging. [Research Support, U.S. Gov’t, P.H.S.]. Radiology, 229(3), 691–696.PubMedCrossRefGoogle Scholar
  109. Sabuncu, M. R., Desikan, R. S., Sepulcre, J., Yeo, B. T., Liu, H., Schmansky, N. J., et al. (2011). The dynamics of cortical and hippocampal atrophy in Alzheimer disease. Archives of Neurology, 68(8), 1040–1048.PubMedCrossRefGoogle Scholar
  110. Saykin, A. J., Flashman, L. A., Frutiger, S. A., Johnson, S. C., Mamourian, A. C., Moritz, C. H., et al. (1999). Neuroanatomic substrates of semantic memory impairment in Alzheimer’s disease: patterns of functional MRI activation. Journal of International Neuropsychological Society, 5(5), 377–392.CrossRefGoogle Scholar
  111. Schmidt-Wilcke, T., Poljansky, S., Hierlmeier, S., Hausner, J., & Ibach, B. (2009). 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, 47(4), 1914–1920.PubMedCrossRefGoogle Scholar
  112. Shen, K. K., Fripp, J., Meriaudeau, F., Chetelat, G., Salvado, O., & Bourgeat, P. (2011). Detecting global and local hippocampal shape changes in Alzheimer’s disease using statistical shape models. Neuroimage.Google Scholar
  113. Shimamura, A. P. (1995). Memory and the prefrontal cortex. Annals of the New York Academy of Sciences, 769, 151–159.PubMedCrossRefGoogle Scholar
  114. Small, S. A., Perera, G. M., DeLaPaz, R., Mayeux, R., & Stern, Y. (1999). Differential regional dysfunction of the hippocampal formation among elderly with memory decline and Alzheimer’s disease. Annals of Neurology, 45(4), 466–472.PubMedCrossRefGoogle Scholar
  115. Smith, C. D., Malcein, M., Meurer, K., Schmitt, F. A., Markesbery, W. R., & Pettigrew, L. C. (1999). MRI temporal lobe volume measures and neuropsychologic function in Alzheimer’s disease. Journal of Neuroimaging, 9(1), 2–9.PubMedGoogle Scholar
  116. Smith, A. B., Taylor, E., Brammer, M., & Rubia, K. (2004). Neural correlates of switching set as measured in fast, event-related functional magnetic resonance imaging. Human Brain Mapping, 21(4), 247–256.PubMedCrossRefGoogle Scholar
  117. Sperling, R. A., Bates, J. F., Chua, E. F., Cocchiarella, A. J., Rentz, D. M., Rosen, B. R., et al. (2003). FMRI studies of associative encoding in young and elderly controls and mild Alzheimer’s disease. Journal of Neurology, Neurosurgery, and Psychiatry, 74(1), 44–50.PubMedCrossRefGoogle Scholar
  118. Sperling, R. A., Dickerson, B. C., Pihlajamaki, M., Vannini, P., LaViolette, P. S., Vitolo, O. V., et al. (2010). Functional alterations in memory networks in early Alzheimer’s disease. Neuromolecular Medicine, 12(1), 27–43.PubMedCrossRefGoogle Scholar
  119. Spreen, O., & Strauss, E. (1998). A compendium of neuropsychological tests. New York: Oxford University Press.Google Scholar
  120. Stonnington, C. M., Chu, C., Kloppel, S., Jack, C. R., Jr., Ashburner, J., & Frackowiak, R. S. (2010). Predicting clinical scores from magnetic resonance scans in Alzheimer’s disease. NeuroImage, 51(4), 1405–1413.PubMedCrossRefGoogle Scholar
  121. Taylor, S. F., Welsh, R. C., Wager, T. D., Phan, K. L., Fitzgerald, K. D., & Gehring, W. J. (2004). A functional neuroimaging study of motivation and executive function. NeuroImage, 21(3), 1045–1054.PubMedCrossRefGoogle Scholar
  122. Thomann, P. A., Toro, P., Dos Santos, V., Essig, M., & Schroder, J. (2008). Clock drawing performance and brain morphology in mild cognitive impairment and Alzheimer’s disease. Brain and Cognition, 67(1), 88–93.PubMedCrossRefGoogle Scholar
  123. Vemuri, P., Wiste, H. J., Weigand, S. D., Shaw, L. M., Trojanowski, J. Q., Weiner, M. W., et al. (2009a). MRI and CSF biomarkers in normal, MCI, and AD subjects: diagnostic discrimination and cognitive correlations. Neurology, 73(4), 287–293.PubMedCrossRefGoogle Scholar
  124. Vemuri, P., Wiste, H. J., Weigand, S. D., Shaw, L. M., Trojanowski, J. Q., Weiner, M. W., et al. (2009b). MRI and CSF biomarkers in normal, MCI, and AD subjects: predicting future clinical change. Neurology, 73(4), 294–301.PubMedCrossRefGoogle Scholar
  125. Vemuri, P., Wiste, H. J., Weigand, S. D., Knopman, D. S., Shaw, L. M., Trojanowski, J. Q., et al. (2010). Effect of apolipoprotein E on biomarkers of amyloid load and neuronal pathology in Alzheimer disease. Annals of Neurology, 67(3), 308–316.PubMedGoogle Scholar
  126. Vemuri, P., Wiste, H. J., Weigand, S. D., Knopman, D. S., Trojanowski, J. Q., Shaw, L. M., et al. (2010). Serial MRI and CSF biomarkers in normal aging, MCI, and AD. Neurology, 75(2), 143–151.PubMedCrossRefGoogle Scholar
  127. Vemuri, P., Weigand, S. D., Przybelski, S. A., Knopman, D. S., Smith, G. E., Trojanowski, J. Q., et al. (2011). Cognitive reserve and Alzheimer’s disease biomarkers are independent determinants of cognition. Brain, 134(Pt 5), 1479–1492.PubMedCrossRefGoogle Scholar
  128. Venneri, A., McGeown, W. J., Hietanen, H. M., Guerrini, C., Ellis, A. W., & Shanks, M. F. (2008). The anatomical bases of semantic retrieval deficits in early Alzheimer’s disease. Neuropsychologia, 46(2), 497–510.PubMedCrossRefGoogle Scholar
  129. Wager, T. D., Jonides, J., & Reading, S. (2004). Neuroimaging studies of shifting attention: a meta-analysis. NeuroImage, 22(4), 1679–1693.PubMedCrossRefGoogle Scholar
  130. Walhovd, K. B., Fjell, A. M., Brewer, J., McEvoy, L. K., Fennema-Notestine, C., Hagler, D. J., Jr., et al. (2010). Combining MR imaging, positron-emission tomography, and CSF biomarkers in the diagnosis and prognosis of Alzheimer disease. AJNR. American Journal of Neuroradiology, 31(2), 347–354.PubMedCrossRefGoogle Scholar
  131. Walhovd, K. B., Fjell, A. M., Dale, A. M., McEvoy, L. K., Brewer, J., Karow, D. S., et al. (2010). Multi-modal imaging predicts memory performance in normal aging and cognitive decline. Neurobiology of Aging, 31(7), 1107–1121.PubMedCrossRefGoogle Scholar
  132. Wechsler, D. (1981). Wechsler Adult Intelligence Scale-Revised. The Psychological Corporation.Google Scholar
  133. Wechsler, D. (1987). Wechsler Memory Scale—revised. New York: Psychological Association.Google Scholar
  134. Weiner, M. W., Aisen, P. S., Jack, C. R., Jr., Jagust, W. J., Trojanowski, J. Q., Shaw, L., et al. (2010). The Alzheimer’s disease neuroimaging initiative: progress report and future plans. Alzheimers Dement, 6(3), 202–211 e207.Google Scholar
  135. Weiner, M. W., Veitch, D. P., Aisen, P. S., Beckett, L. A., Cairns, N. J., Green, R. C., et al. (2011). The Alzheimer’s Disease Neuroimaging Initiative: a review of papers published since its inception. Alzheimers Dement.Google Scholar
  136. Wolk, D. A., & Dickerson, B. C. (2010). Apolipoprotein E (APOE) genotype has dissociable effects on memory and attentional-executive network function in Alzheimer’s disease. Proceedings of the National Academy of Sciences of the United States of America, 107(22), 10256–10261.PubMedCrossRefGoogle Scholar
  137. Wolk, D. A., & Dickerson, B. C. (2011). Fractionating verbal episodic memory in Alzheimer’s disease. NeuroImage, 54(2), 1530–1539.PubMedCrossRefGoogle Scholar
  138. Wolz, R., Heckemann, R. A., Aljabar, P., Hajnal, J. V., Hammers, A., Lotjonen, J., et al. (2010). Measurement of hippocampal atrophy using 4D graph-cut segmentation: application to ADNI. NeuroImage, 52(1), 109–118.PubMedCrossRefGoogle Scholar
  139. Zakzanis, K. K., Graham, S. J., & Campbell, Z. (2003). A meta-analysis of structural and functional brain imaging in dementia of the Alzheimer’s type: a neuroimaging profile. Neuropsychology Review, 13(1), 1–18.PubMedCrossRefGoogle Scholar
  140. Zakzanis, K. K., Mraz, R., & Graham, S. J. (2005). An fMRI study of the Trail Making Test. Neuropsychologia, 43(13), 1878–1886.PubMedCrossRefGoogle Scholar
  141. Zhang, N., Song, X., Zhang, Y., Chen, W., D’Arcy, R. C., Darvesh, S., et al. (2011). An MRI brain atrophy and lesion index to assess the progression of structural changes in Alzheimer’s disease, mild cognitive impairment, and normal aging: a follow-up study. Journal of Alzheimer’s Disease, 26(Suppl 3), 359–367.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2012

Authors and Affiliations

  • Kwangsik Nho
    • 1
  • Shannon L. Risacher
    • 1
  • Paul K. Crane
    • 2
  • Charles DeCarli
    • 3
  • M. Maria Glymour
    • 4
  • Christian Habeck
    • 5
  • Sungeun Kim
    • 1
  • Grace J. Lee
    • 6
  • Elizabeth Mormino
    • 7
  • Shubhabrata Mukherjee
    • 2
  • Li Shen
    • 1
  • John D. West
    • 1
  • Andrew J. Saykin
    • 1
  • Alzheimer’s Disease Neuroimaging Initiative (ADNI)
  1. 1.Center for Neuroimaging, Department of Radiology and Imaging SciencesIndiana University School of MedicineIndianapolisUSA
  2. 2.Department of MedicineUniversity of WashingtonSeattleUSA
  3. 3.Department of Neurology and the Center for Neuroscience, School of MedicineUniversity of California DavisDavisUSA
  4. 4.Department of Society, Human Development and HealthHarvard School of Public HealthBostonUSA
  5. 5.Cognitive Neuroscience Division of Taub Institute for the Study of Alzheimer’s Disease and Aging BrainColumbia University College of Physicians and SurgeonsNew YorkUSA
  6. 6.Department of NeurologyDavid Geffen School of Medicine at UCLALos AngelesUSA
  7. 7.Helen Wills Neuroscience InstituteUniversity of California BerkeleyBerkeleyUSA

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