Hostname: page-component-cd9895bd7-mkpzs Total loading time: 0 Render date: 2024-12-25T05:17:42.939Z Has data issue: false hasContentIssue false
  • English
  • Français

Pre-dementia Memory Impairment is Associated with White Matter Tract Affection

Published online by Cambridge University Press:  24 November 2010

Ramune Grambaite ,
Ivar Reinvang ,
Per Selnes ,
Anders M. Fjell ,
Kristine B. Walhovd ,
Vidar Stenset  and
Tormod Fladby
Ramune Grambaite*
Affiliation:
Department of Neurology, Akershus University Hospital, Lørenskog, Norway Akershus University Hospital Research Center, Lørenskog, Norway
Ivar Reinvang
Affiliation:
Center for the Study of Human Cognition, Department of Psychology, University of Oslo, Oslo, Norway
Per Selnes
Affiliation:
Department of Neurology, Akershus University Hospital, Lørenskog, Norway Faculty Division Akershus University Hospital, University of Oslo, Oslo, Norway
Anders M. Fjell
Affiliation:
Center for the Study of Human Cognition, Department of Psychology, University of Oslo, Oslo, Norway Department of Neuropsychology, Oslo University Hospital Ulleval, Oslo, Norway
Kristine B. Walhovd
Affiliation:
Center for the Study of Human Cognition, Department of Psychology, University of Oslo, Oslo, Norway Department of Neuropsychology, Oslo University Hospital Ulleval, Oslo, Norway
Vidar Stenset
Affiliation:
Department of Neurology, Akershus University Hospital, Lørenskog, Norway Faculty Division Akershus University Hospital, University of Oslo, Oslo, Norway Department of Neurosurgery, Oslo University Hospital Ulleval, Oslo, Norway
Tormod Fladby
Affiliation:
Department of Neurology, Akershus University Hospital, Lørenskog, Norway Faculty Division Akershus University Hospital, University of Oslo, Oslo, Norway
*
Correspondence and reprint requests to: Ramune Grambaite, Department of Neurology, Akershus University Hospital, Sykehusveien 25, NO-1478 Lørenskog, Norway. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Mild cognitive impairment (MCI), especially amnestic, often represents pre-dementia Alzheimer’s disease, characterized by medial temporal lobe atrophy, while white matter (WM) alterations are insufficiently described. We analyze both cortical morphometric and WM diffusivity differences in amnestic versus non-amnestic subtypes and ask if memory and WM tract affection are related independently of cortical atrophy. Forty-nine patients from a university-hospital based memory clinic with a score of 3 on the Global Deterioration Scale aged 43–77 years (45% female) were included. Two neuropsychologists have classified cases as amnestic (aMCI), non-amnestic (naMCI), or less advanced (laMCI), not satisfying criteria for aMCI/naMCI. Diffusion tensor imaging (DTI) WM tract and morphometric data of the temporal-parietal memory network were compared among patient subtypes and related to story, word list, and visual memory. WM radial and mean diffusivity (DR and MD), underlying the entorhinal cortex, were higher in aMCI compared with laMCI. WM DR and MD, underlying the entorhinal, parahippocampal, and middle temporal cortex, explained unique variance in word list and story memory, and this was not due to secondary effects of cortical thinning. DTI may thus potentially aid diagnosis in early disease stages. (JINS, 2011, 17, 000–000)

Keywords

Alzheimer’s diseaseMild cognitive impairmentDiffusion tensor imagingRadial and mean diffusivityCortical thicknessTemporal-parietal memory network
Type
Research Articles
Information
Journal of the International Neuropsychological Society , Volume 17 , Issue 1 , January 2011 , pp. 143 - 153
Copyright
Copyright © The International Neuropsychological Society 2010

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Andersson, J.L.R., Jenkinson, M., Smith, S. (2007). Non-linear registration, aka Spatial normalisation. FMRIB Technical Report TR07JA2 from www.fmrib.ox.ac.uk/analysis/techrep.Google Scholar
Auer, S., Reisberg, B. (1997). The GDS/FAST staging system. International Psychogeriatrics/IPA, 9(Suppl 1), 167–171.CrossRefGoogle ScholarPubMed
Bickel, H., Mosch, E., Seigerschmidt, E., Siemen, M., Forstl, H. (2006). Prevalence and persistence of mild cognitive impairment among elderly patients in general hospitals. Dementia and Geriatric Cognitive Disorders, 21, 242–250.CrossRefGoogle ScholarPubMed
Bosch, B., Arenaza-Urquijo, E.M., Rami, L., Sala-Llonch, R., Junque, C., Sole-Padulles, C., Bartrés-Faz, D. (2010). Multiple DTI index analysis in normal aging, amnestic MCI and AD. Relationship with neuropsychological performance. Neurobiology of Aging, [Epub ahead of print].Google Scholar
Braak, H., Braak, E. (1996). Evolution of the neuropathology of Alzheimer’s disease. Acta Neurologica Scandinavica. Supplementum, 165, 3–12.CrossRefGoogle ScholarPubMed
Buckner, R.L., Wheeler, M.E. (2001). The cognitive neuroscience of remembering. Nature Reviews. Neuroscience, 2, 624–634.CrossRefGoogle ScholarPubMed
Charlton, R.A., Barrick, T.R., McIntyre, D.J., Shen, Y., O’Sullivan, M., Howe, F.A., Markus, H.S. (2006). White matter damage on diffusion tensor imaging correlates with age-related cognitive decline. Neurology, 66, 217–222.CrossRefGoogle ScholarPubMed
Chetelat, G., Desgranges, B., de la Sayette, V., Viader, F., Berkouk, K., Landeau, B., Eustache, F. (2003). Dissociating atrophy and hypometabolism impact on episodic memory in mild cognitive impairment. Brain, 126, 1955–1967.CrossRefGoogle ScholarPubMed
Cohen, C.K. (1988). Statistical power analysis for the behavioral sciences. Hillsdale, NJ: Erlbaum.Google Scholar
Concha, L., Livy, D.J., Beaulieu, C., Wheatley, B.M., Gross, D.W. (2010). In vivo diffusion tensor imaging and histopathology of the fimbria-fornix in temporal lobe epilepsy. The Journal of Neuroscience, 30, 996–1002.CrossRefGoogle ScholarPubMed
De Santi, S., de Leon, M.J., Rusinek, H., Convit, A., Tarshish, C.Y., Roche, A., Fowler, J. (2001). Hippocampal formation glucose metabolism and volume losses in MCI and AD. Neurobiology of Aging, 22, 529–539.CrossRefGoogle ScholarPubMed
Delis, D.C., Kaplan, E., Kramer, J.H. (2001). Delis and Kaplan D-KEFS Executive Functions System: Examiner’s manual. San Antonio, TX: The Psychological Corporation.Google Scholar
Desikan, R.S., Ségonne, F., Fischl, B., Quinn, B.T., Dickerson, B.C., Blacker, D., Killiany, R.J. (2006). An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage, 31, 968–980.CrossRefGoogle ScholarPubMed
Dubois, B., Feldman, H.H., Jacova, C., Dekosky, S.T., Barberger-Gateau, P., Cummings, J., Scheltens, P. (2007). Research criteria for the diagnosis of Alzheimer’s disease: Revising the NINCDS-ADRDA criteria. Lancet Neurology, 6, 734–746.CrossRefGoogle ScholarPubMed
Edman, A., Mahnfeldt, M., Wallin, A. (2001). Inter-rater reliability of the STEP protocol. Journal of Geriatric Psychiatry and Neurology, 14, 140–144.CrossRefGoogle ScholarPubMed
Fellgiebel, A., Muller, M.J., Wille, P., Dellani, P.R., Scheurich, A., Schmidt, L.G., Stoeter, P. (2005). Color-coded diffusion-tensor-imaging of posterior cingulate fiber tracts in mild cognitive impairment. Neurobiology of Aging, 26, 1193–1198.CrossRefGoogle ScholarPubMed
Fischer, P., Jungwirth, S., Zehetmayer, S., Weissgram, S., Hoenigschnabl, S., Gelpi, E., Tragl, K.H. (2007). Conversion from subtypes of mild cognitive impairment to Alzheimer dementia. Neurology, 68, 288–291.CrossRefGoogle ScholarPubMed
Fischl, B., Salat, D.H., Busa, E., Albert, M., Dieterich, M., Haselgrove, C., Dale, A.M. (2002). Whole brain segmentation: Automated labeling of neuroanatomical structures in the human brain. Neuron, 33, 341–355.CrossRefGoogle ScholarPubMed
Fischl, B., van der Kouwe, A., Destrieux, C., Halgren, E., Segonne, F., Salat, D.H., Dale, A.M. (2004). Automatically parcellating the human cerebral cortex. Cerebral Cortex, 14, 11–22.CrossRefGoogle ScholarPubMed
Fjell, A.M., Amlien, I.K., Westlye, L.T., Stenset, V., Fladby, T., Skinningsrud, A., Walhovd, K.B. (2010). CSF biomarker pathology correlates with a medial temporo-parietal network affected by very mild to moderate Alzheimer’s disease but not a fronto-striatal network affected by healthy aging. Neuroimage, 49, 1820–1830.CrossRefGoogle Scholar
Fjell, A.M., Walhovd, K.B., Amlien, I., Bjornerud, A., Reinvang, I., Gjerstad, L., Fladby, T. (2008). Morphometric changes in the episodic memory network and tau pathologic features correlate with memory performance in patients with mild cognitive impairment. AJNR. American Journal of Neuroradiology, 29, 1183–1189.CrossRefGoogle ScholarPubMed
Fjell, A.M., Westlye, L.T., Greve, D.N., Fischl, B., Benner, T., van der Kouwe, A.J., Walhovd, K.B. (2008). The relationship between diffusion tensor imaging and volumetry as measures of white matter properties. Neuroimage, 42, 1654–1668.CrossRefGoogle ScholarPubMed
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, 189–198.CrossRefGoogle ScholarPubMed
Grambaite, R., Stenset, V., Reinvang, I., Walhovd, K.B., Fjell, A.M., Fladby, T. (2010). White matter diffusivity predicts memory in patients with subjective and mild cognitive impairment and normal CSF total tau levels. Journal of the International Neuropsychological Society, 16, 58–69.CrossRefGoogle ScholarPubMed
Huang, J., Friedland, R.P., Auchus, A.P. (2007). Diffusion tensor imaging of normal-appearing white matter in mild cognitive impairment and early Alzheimer disease: Preliminary evidence of axonal degeneration in the temporal lobe. AJNR. American journal of neuroradiology, 28, 1943–1948.CrossRefGoogle ScholarPubMed
Jack, C.R.J., Lowe, V.J., Senjem, M.L., Weigand, S.D., Kemp, B.J., Shiung, M.M., Petersen, R.C. (2008). 11C PiB and structural MRI provide complementary information in imaging of Alzheimer’s disease and amnestic mild cognitive impairment. Brain, 131, 665–680.CrossRefGoogle ScholarPubMed
Jack, C.R.J., Petersen, R.C., Xu, Y.C., O’Brien, P.C., Smith, G.E., Ivnik, R.J., Kokmen, E. (1999). Prediction of AD with MRI-based hippocampal volume in mild cognitive impairment. Neurology, 52, 1397–1403.CrossRefGoogle ScholarPubMed
Jack, C.R.J., Shiung, M.M., Gunter, J.L., O’Brien, P.C., Weigand, S.D., Knopman, D.S., Petersen, R.C. (2004). Comparison of different MRI brain atrophy rate measures with clinical disease progression in AD. Neurology, 62, 591–600.CrossRefGoogle ScholarPubMed
Jak, A.J., Bangen, K.J., Wierenga, C.E., Delano-Wood, L., Corey-Bloom, J., Bondi, M.W. (2009). Contributions of neuropsychology and neuroimaging to understanding clinical subtypes of mild cognitive impairment. International Review of Neurobiology, 84, 81–103.CrossRefGoogle ScholarPubMed
Jak, A.J., Bondi, M.W., Delano-Wood, L., Wierenga, C., Corey-Bloom, J., Salmon, D.P., Delis, D.C. (2009). Quantification of five neuropsychological approaches to defining mild cognitive impairment. The American Journal of Geriatric Psychiatry, 17, 368–375.CrossRefGoogle ScholarPubMed
Jenkinson, M., Smith, S. (2001). A global optimisation method for robust affine registration of brain images. Medical Image Analysis, 5, 143–156.CrossRefGoogle ScholarPubMed
Kaplan, E.F., Goodglass, H., Weintraub, S. (1983). The Boston Naming Test (2nd ed.). Philadelphia: Lea & Febiger.Google Scholar
Karas, G., Sluimer, J., Goekoop, R., van der Flier, W., Rombouts, S.A., Vrenken, H., Barkhof, F. (2008). Amnestic mild cognitive impairment: Structural MR imaging findings predictive of conversion to Alzheimer disease. AJNR. American Journal of Neuroradiology, 29, 944–949.CrossRefGoogle ScholarPubMed
Kiernan, R.J., Mueller, J., Langston, J.W., Van Dyke, C. (1987). The Neurobehavioral Cognitive Status Examination: A brief but quantitative approach to cognitive assessment. Annals of Internal Medicine, 107, 481–485.CrossRefGoogle ScholarPubMed
Le Bihan, D., Mangin, J.F., Poupon, C., Clark, C.A., Pappata, S., Molko, N., Chabriat, H. (2001). Diffusion tensor imaging: Concepts and applications. Journal of Magnetic Resonance Imaging, 13, 534–546.CrossRefGoogle ScholarPubMed
Liu, Y., Spulber, G., Lehtimaki, K.K., Kononen, M., Hallikainen, I., Grohn, H., Soininen, H. (2009). Diffusion tensor imaging and Tract-Based Spatial Statistics in Alzheimer’s disease and mild cognitive impairment. Neurobiology of Aging, [Epub ahead of print].Google ScholarPubMed
Medina, D., DeToledo-Morrell, L., Urresta, F., Gabrieli, J.D., Moseley, M., Fleischman, D., Stebbins, G.T. (2006). White matter changes in mild cognitive impairment and AD: A diffusion tensor imaging study. Neurobiology of Aging, 27, 663–672.CrossRefGoogle Scholar
Meyers, J.E., Meyers, K.R. (1995). Rey complex figure test and recognition trial. Lutz, FL: Psychological Assessment Resources.Google Scholar
Morris, J.C. (1993). The Clinical Dementia Rating (CDR): Current version and scoring rules. Neurology, 43, 2412–2414.CrossRefGoogle ScholarPubMed
Nordlund, A., Rolstad, S., Klang, O., Edman, A., Hansen, S., Wallin, A. (2010). Two year outcome of MCI subtypes and aetiologies in the Goteborg MCI study. Journal of Neurology, Neurosurgery, and Psychiatry, 81, 541–546.CrossRefGoogle ScholarPubMed
Paus, T. (2009). Growth of white matter in the adolescent brain: Myelin or axon? Brain and Cognition, 72, 26–35.CrossRefGoogle ScholarPubMed
Petersen, R.C. (2003). Conceptual overview. In R.C. Petersen (Ed.), Mild cognitive impairment: Aging to Alzheimer’s disease pp. (1–14). New York: Oxford University Press.CrossRefGoogle Scholar
Petersen, R.C. (2004). Mild cognitive impairment as a diagnostic entity. Journal of Internal Medicine, 256, 183–194.CrossRefGoogle ScholarPubMed
Petersen, R.C., Parisi, J.E., Dickson, D.W., Johnson, K.A., Knopman, D.S., Boeve, B.F., Kokmen, E. (2006). Neuropathologic features of amnestic mild cognitive impairment. Archives of Neurology, 63, 665–672.CrossRefGoogle ScholarPubMed
Petersen, R.C., Roberts, R.O., Knopman, D.S., Boeve, B.F., Geda, Y.E., Ivnik, R.J., Jack, C.R. Jr. (2009). Mild cognitive impairment: Ten years later. Archives of Neurology, 66, 1447–1455.CrossRefGoogle ScholarPubMed
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, 303–308.CrossRefGoogle ScholarPubMed
Pievani, M., Agosta, F., Pagani, E., Canu, E., Sala, S., Absinta, M., Filippi, M. (2010). Assessment of white matter tract damage in mild cognitive impairment and Alzheimer’s disease. Human Brain Mapping, [Epub ahead of print].CrossRefGoogle ScholarPubMed
Reisberg, B., Ferris, S.H., de Leon, M.J., Crook, T. (1988). Global Deterioration Scale (GDS). Psychopharmacology Bulletin, 24, 661–663.Google ScholarPubMed
Rogalski, E.J., Murphy, C.M., deToledo-Morrell, L., Shah, R.C., Moseley, M.E., Bammer, R., Stebbins, G.T. (2009). Changes in parahippocampal white matter integrity in amnestic mild cognitive impairment: A diffusion tensor imaging study. Behavioural Neurology, 21, 51–61.CrossRefGoogle ScholarPubMed
Rose, S.E., McMahon, K.L., Janke, A.L., O’Dowd, B., de Zubicaray, G., Strudwick, M.W., Chalk, J.B. (2006). Diffusion indices on magnetic resonance imaging and neuropsychological performance in amnestic mild cognitive impairment. Journal of Neurology, Neurosurgery, and Psychiatry, 77, 1122–1128.CrossRefGoogle ScholarPubMed
Rountree, S.D., Waring, S.C., Chan, W.C., Lupo, P.J., Darby, E.J., Doody, R.S. (2007). Importance of subtle amnestic and nonamnestic deficits in mild cognitive impairment: Prognosis and conversion to dementia. Dementia and Geriatric Cognitive Disorders, 24, 476–482.CrossRefGoogle ScholarPubMed
Royall, D.R., Mahurin, R.K., Gray, K.F. (1992). Bedside assessment of executive cognitive impairment: The executive interview. Journal of the American Geriatrics Society, 40, 1221–1226.CrossRefGoogle ScholarPubMed
Rueckert, D., Sonoda, L.I., Hayes, C., Hill, D.L., Leach, M.O., Hawkes, D.J. (1999). Nonrigid registration using free-form deformations: Application to breast MR images. IEEE Transactions on Medical Imaging, 18, 712–721.CrossRefGoogle ScholarPubMed
Salat, D.H., Tuch, D.S., van der Kouwe, A.J., Greve, D.N., Pappu, V., Lee, S.Y., Rosas, H.D. (2010). White matter pathology isolates the hippocampal formation in Alzheimer’s disease. Neurobiology of Aging, 31, 244–256.CrossRefGoogle ScholarPubMed
Schmidt, M. (1996). Rey auditory and verbal learning test. A handbook. Los Angeles, CA: Western Psychological Services.Google Scholar
Schneider, J.A., Arvanitakis, Z., Leurgans, S.E., Bennett, D.A. (2009). The neuropathology of probable Alzheimer disease and mild cognitive impairment. Annals of Neurology, 66, 200–208.CrossRefGoogle ScholarPubMed
Smith, S.M. (2002). Fast robust automated brain extraction. Human Brain Mapping, 17, 143–155.CrossRefGoogle ScholarPubMed
Smith, S.M., Jenkinson, M., Johansen-Berg, H., Rueckert, D., Nichols, T.E., Mackay, C.E., Behrens, T.E. (2006). Tract-based spatial statistics: Voxelwise analysis of multi-subject diffusion data. Neuroimage, 31, 1487–1505.CrossRefGoogle ScholarPubMed
Smith, S.M., Jenkinson, M., Woolrich, M.W., Beckmann, C.F., Behrens, T.E., Johansen-Berg, H., Matthews, P.M. (2004). Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage, 23(Suppl 1), S208–S219.CrossRefGoogle ScholarPubMed
Snowdon, D.A., Greiner, L.H., Mortimer, J.A., Riley, K.P., Greiner, P.A., Markesbery, W.R. (1997). Brain infarction and the clinical expression of Alzheimer disease. The Nun Study. JAMA, 277, 813–817.CrossRefGoogle ScholarPubMed
Song, S.K., Sun, S.W., Ju, W.K., Lin, S.J., Cross, A.H., Neufeld, A.H. (2003). Diffusion tensor imaging detects and differentiates axon and myelin degeneration in mouse optic nerve after retinal ischemia. Neuroimage, 20, 1714–1722.CrossRefGoogle ScholarPubMed
Song, S.K., Yoshino, J., Le, T.Q., Lin, S.J., Sun, S.W., Cross, A.H., Armstrong, R.C. (2005). Demyelination increases radial diffusivity in corpus callosum of mouse brain. Neuroimage, 26, 132–140.CrossRefGoogle ScholarPubMed
Spreen, O., Strauss, E.A. (1998). A compendium of neuropsychological tests, second edition: Administration, norms and commentary. New York: Oxford University Press.Google Scholar
Stebbins, G.T., Murphy, C.M. (2009). Diffusion tensor imaging in Alzheimer’s disease and mild cognitive impairment. Behavioural Neurology, 21, 39–49.CrossRefGoogle ScholarPubMed
Stenset, V., Bjornerud, A., Fjell, A.M., Walhovd, K.B., Hofoss, D., Due-Tonnessen, P., Fladby, T. (2009). Cingulum fiber diffusivity and CSF T-tau in patients with subjective and mild cognitive impairment. Neurobiology of Aging, [Epub ahead of print].Google ScholarPubMed
Stenset, V., Grambaite, R., Reinvang, I., Hessen, E., Cappelen, T., Bjornerud, A., Fladby, T. (2007). Diaschisis after thalamic stroke: A comparison of metabolic and structural changes in a patient with amnesic syndrome. Acta Neurologica Scandinavica. Supplementum, 187, 68–71.CrossRefGoogle Scholar
Stenset, V., Hofoss, D., Johnsen, L., Skinningsrud, A., Berstad, A.E., Negaard, A., Fladby, T. (2008). White matter lesion severity is associated with reduced cognitive performances in patients with normal CSF Abeta42 levels. Acta Neurologica Scandinavica, 118, 373–378.CrossRefGoogle ScholarPubMed
Stenset, V., Johnsen, L., Kocot, D., Negaard, A., Skinningsrud, A., Gulbrandsen, P., Fladby, T. (2006). Associations between white matter lesions, cerebrovascular risk factors, and low CSF Abeta42. Neurology, 67, 830–833.CrossRefGoogle ScholarPubMed
Wagner, A.D., Shannon, B.J., Kahn, I., Buckner, R.L. (2005). Parietal lobe contributions to episodic memory retrieval. Trends in Cognitive Sciences, 9, 445–453.CrossRefGoogle ScholarPubMed
Walhovd, K.B., Fjell, A.M., Amlien, I., Grambaite, R., Stenset, V., Bjornerud, A., Fladby, T. (2009). Multimodal imaging in mild cognitive impairment: Metabolism, morphometry and diffusion of the temporal-parietal memory network. Neuroimage, 45, 215–223.CrossRefGoogle ScholarPubMed
Wallin, A., Edman, A., Blennow, K., Gottfries, C.G., Karlsson, I., Regland, B., Sjögren, M. (1996). Stepwise comparative status analysis (STEP): A tool for identification of regional brain syndromes in dementia. Journal of Geriatric Psychiatry and Neurology, 9, 185–199.CrossRefGoogle ScholarPubMed
Wang, L., Goldstein, F.C., Veledar, E., Levey, A.I., Lah, J.J., Meltzer, C.C., Mao, H. (2009). Alterations in cortical thickness and white matter integrity in mild cognitive impairment measured by whole-brain cortical thickness mapping and diffusion tensor imaging. AJNR. American Journal of Neuroradiology, 30, 893–899.CrossRefGoogle ScholarPubMed
Wechsler, D. (1987). Wechsler memory scale-revised. New York: Psychological Corporation.Google Scholar
Wechsler, D. (1999). Wechsler Abbreviated scale of intelligence (WASI). San Antonio, TX: The Psychological Corporation.Google Scholar
Wechsler, D. (2003). Wechsler adult intelligence scale—third edition: manual. San Antonio, TX: The Psychological Corporation.Google Scholar
Whitwell, J.L., Jack, C.R. Jr., Przybelski, S.A., Parisi, J.E., Senjem, M.L., Boeve, B.F., Josephs, K.A. (2009). Temporoparietal atrophy: A marker of AD pathology independent of clinical diagnosis. Neurobiology of Aging, [Epub ahead of print].Google ScholarPubMed
Whitwell, J.L., Petersen, R.C., Negash, S., Weigand, S.D., Kantarci, K., Ivnik, R.J., Jack, C.R. Jr. (2007). Patterns of atrophy differ among specific subtypes of mild cognitive impairment. Archives of Neurology, 64, 1130–1138.CrossRefGoogle ScholarPubMed
Whitwell, J.L., Przybelski, S.A., Weigand, S.D., Knopman, D.S., Boeve, B.F., Petersen, R.C., Jack, C.R. Jr. (2007). 3D maps from multiple MRI illustrate changing atrophy patterns as subjects progress from mild cognitive impairment to Alzheimer’s disease. Brain, 130, 1777–1786.CrossRefGoogle ScholarPubMed
Whitwell, J.L., Shiung, M.M., Przybelski, S.A., Weigand, S.D., Knopman, D.S., Boeve, B.F., Jack, C.R. Jr. (2008). MRI patterns of atrophy associated with progression to AD in amnestic mild cognitive impairment. Neurology, 70, 512–520.CrossRefGoogle ScholarPubMed
Wisdom, N.M., Callahan, J.L., Hawkins, K.A. (2009). The effects of apolipoprotein E on non-impaired cognitive functioning: A meta-analysis. Neurobiology of Aging, [Epub ahead of print].Google ScholarPubMed
Woolrich, M.W., Jbabdi, S., Patenaude, B., Chappell, M., Makni, S., Behrens, T., Smith, S.M. (2009). Bayesian analysis of neuroimaging data in FSL. Neuroimage, 45, S173–S186.CrossRefGoogle ScholarPubMed
World Medical Association. Declaration of Helsinki (1991). Law, Medicine & Health Care, 19, 264–265.CrossRefGoogle Scholar
Yaffe, K., Petersen, R.C., Lindquist, K., Kramer, J., Miller, B. (2006). Subtype of mild cognitive impairment and progression to dementia and death. Dementia and Geriatric Cognitive Disorders, 22, 312–319.CrossRefGoogle ScholarPubMed
Zhang, Y., Schuff, N., Jahng, G.H., Bayne, W., Mori, S., Schad, L., Weiner, M.W. (2007). Diffusion tensor imaging of cingulum fibers in mild cognitive impairment and Alzheimer disease. Neurology, 68, 13–19.CrossRefGoogle ScholarPubMed
Supplementary material: PDF

Grambaite supplementary material

Table.pdf

Download Grambaite supplementary material(PDF)
PDF 73.1 KB