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Table of Contents
Vol. 26, No. 2, 2008
Issue release date: September 2008
Section title: Original Research Article
Free Access
Dement Geriatr Cogn Disord 2008;26:123–137
(DOI:10.1159/000148190)

fMRI Activation Changes during Successful Episodic Memory Encoding and Recognition in Amnestic Mild Cognitive Impairment Relative to Cognitively Healthy Older Adults

Trivedi M.A.a · Murphy C.M.a · Goetz C.a · Shah R.C.b, d · Gabrieli J.D.E.e · Whitfield-Gabrieli S.e · Turner D.A.c · Stebbins G.T.a
Departments of aNeurological Sciences, bFamily Medicine and cNuclear Medicine and Diagnostic Radiology, and dRush Alzheimer’s Disease Research Center, Rush University Medical Center, Chicago, Ill., and eDepartment of Brain and Cognitive Science, Massachusetts Institute of Technology, Cambridge, Mass., USA
email Corresponding Author

Glenn T. Stebbins, PhD

Rush University Medical Center, Department of Neurological Sciences

1725 West Harrison, Suite 309

Chicago, IL 60612 (USA)

Tel. +1 312 563 3854, Fax +1 312 563 4009, E-Mail gstebbin@rush.edu


References

  1. Petersen RC: Mild cognitive impairment as a diagnostic entity. J Intern Med 2004;256:183–194.
  2. Hyman BT, Arriagada PV, van Hoesen GW, Damasio AR: Memory impairment in Alzheimer’s disease: an anatomical perspective; in Parks RW, Zec RF, Wilson RS (eds): Neuropsychology of Alzheimer’s Disease and Other Dementias. New York, Oxford University Press, 1993, pp 138–150.
  3. Desgranges B, Baron JC, de la Sayette V, Petit-Taboue MC, 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;121:611–631.
  4. Buckner RL, Snyder AZ, Shannon BJ, LaRossa G, Sachs R, Fotenos AF, Sheline YI, Klunk WE, Mathis CA, Morris JC, Mintun MA: Molecular, structural, and functional characterization of Alzheimer’s disease: evidence for a relationship between default activity, amyloid, and memory. J Neurosci 2005;25:7709–7717.
  5. Ries ML, Jabbar BM, Schmitz TW, Trivedi MA, Gleason CE, Carlsson CM, Rowley HA, Asthana S, Johnson SC: Anosognosia in mild cognitive impairment: relationship to activation of cortical midline structures involved in self-appraisal. J Int Neuropsychol Soc 2007;13:450–461.
  6. Chetelat G, Baron JC: Early diagnosis of Alzheimer’s disease: contribution of structural neuroimaging. Neuroimage 2003;18:525–541.
  7. Jack CR Jr, Petersen RC, Xu Y, O’Brien PC, Smith GE, Ivnik RJ, Tangalos EG, Kokmen E: Rate of medial temporal lobe atrophy in typical aging and Alzheimer’s disease. Neurology 1998;51:993–999.
  8. Stoub TR, Bulgakova M, Leurgans S, Bennett DA, Fleischman D, Turner DA, deToledo-Morrell L: MRI predictors of risk of incident Alzheimer disease: a longitudinal study. Neurology 2005;64:1520–1524.
  9. Engler H, Forsberg A, Almkvist O, Blomquist G, Larsson E, Savitcheva I, Wall A, Ringheim A, Langstrom B, Nordberg A: Two-year follow-up of amyloid deposition in patients with Alzheimer’s disease. Brain 2006;129:2856–2866.
  10. Forsberg A, Engler H, Almkvist O, Blomquist G, Hagman G, Wall A, Ringheim A, Langstrom B, Nordberg A: PET imaging of amyloid deposition in patients with mild cognitive impairment. Neurobiol Aging, in press.
  11. Klunk WE, Engler H, Nordberg A, Wang Y, Blomqvist G, Holt DP, Bergstrom M, Savitcheva I, Huang GF, Estrada S, Ausen B, Debnath ML, Barletta J, Price JC, Sandell J, Lopresti BJ, Wall A, Koivisto P, Antoni G, Mathis CA, Langstrom B: Imaging brain amyloid in Alzheimer’s disease with Pittsburgh Compound-B. Ann Neurol 2004;55:306–319.
  12. Small GW, Kepe V, Ercoli LM, Siddarth P, Bookheimer SY, Miller KJ, Lavretsky H, Burggren AC, Cole GM, Vinters HV, Thompson PM, Huang SC, Satyamurthy N, Phelps ME, Barrio JR: PET of brain amyloid and tau in mild cognitive impairment. N Engl J Med 2006;355:2652–2663.
  13. Cabeza R, Nyberg L: Imaging cognition II: an empirical review of 275 PET and fMRI studies. J Cogn Neurosci 2000;12:1–47.
  14. Wagner AD, Shannon BJ, Kahn I, Buckner RL: Parietal lobe contributions to episodic memory retrieval. Trends Cogn Sci 2005;9:445–453.
  15. Drzezga A, Grimmer T, Henriksen G, Stangier I, Perneczky R, Diehl-Schmid J, Mathis CA, Klunk WE, Price J, Dekosky S, Wester HJ, Schwaiger M, Kurz A: Imaging of amyloid plaques and cerebral glucose metabolism in semantic dementia and Alzheimer’s disease. Neuroimage 2008;39:619–633.
  16. Nordberg A: Amyloid imaging in Alzheimer’s disease. Curr Opin Neurol 2007;20:398–402.
  17. Dickerson BC, Salat DH, Bates JF, Atiya M, Killiany RJ, Greve DN, Dale AM, Stern CE, Blacker D, Albert MS, Sperling RA: Medial temporal lobe function and structure in mild cognitive impairment. Ann Neurol 2004;56:27–35.
  18. Dickerson BC, Salat DH, Greve DN, Chua EF, Rand-Giovannetti E, Rentz DM, Bertram L, Mullin K, Tanzi RE, Blacker D, Albert MS, Sperling RA: Increased hippocampal activation in mild cognitive impairment compared to normal aging and AD. Neurology 2005;65:404–411.
  19. Hamalainen A, Pihlajamaki M, Tanila H, Hanninen T, Niskanen E, Tervo S, Karjalainen PA, Vanninen RL, Soininen H: Increased fMRI responses during encoding in mild cognitive impairment. Neurobiol Aging 2007;28:1889–1903.
  20. Heun R, Freymann K, Erb M, Leube DT, Jessen F, Kircher TT, Grodd W: Mild cognitive impairment (MCI) and actual retrieval performance affect cerebral activation in the elderly. Neurobiol Aging 2007;28:404–413.
  21. Kircher TT, Weis S, Freymann K, Erb M, Jessen F, Grodd W, Heun R, Leube DT: Hippocampal activation in patients with mild cognitive impairment is necessary for successful memory encoding. J Neurol Neurosurg Psychiatry 2007;78:812–818.
  22. Johnson SC, Schmitz TW, Moritz CH, Meyerand ME, Rowley HA, Alexander AL, Hansen KW, Gleason CE, Carlsson CM, Ries ML, Asthana S, Chen K, Reiman EM, Alexander GE: Activation of brain regions vulnerable to Alzheimer’s disease: the effect of mild cognitive impairment. Neurobiol Aging 2006;27:1604–1612.
  23. Mandzia JL, McAndrews MP, Grady CL, Graham SJ, Black SE: Neural correlates of incidental memory in mild cognitive impairment: an fMRI study. Neurobiol Aging, in press.
  24. Xu G, Antuono PG, Jones J, Xu Y, Wu G, Ward D, Li SJ: Perfusion fMRI detects deficits in regional CBF during memory-encoding tasks in MCI subjects. Neurology 2007;69:1650–1656.
  25. Johnson SC, Baxter LC, Susskind-Wilder L, Connor DJ, Sabbagh MN, Caselli RJ: Hippocampal adaptation to face repetition in healthy elderly and mild cognitive impairment. Neuropsychologia 2004;42:980–989.
  26. Machulda MM, Ward HA, Borowski B, Gunter JL, Cha RH, O’Brien PC, Petersen RC, Boeve BF, Knopman D, Tang-Wai DF, Ivnik RJ, Smith GE, Tangalos EG, Jack CR Jr: Comparison of memory fMRI response among normal, MCI, and Alzheimer’s patients. Neurology 2003;61:500–506.
  27. Small SA, Perera GM, DeLaPaz R, Mayeux R, Stern Y: Differential regional dysfunction of the hippocampal formation among elderly with memory decline and Alzheimer’s disease. Ann Neurol 1999;45:466–472.
  28. Petrella JR, Krishnan S, Slavin MJ, Tran TT, Murty L, Doraiswamy PM: Mild cognitive impairment: evaluation with 4-T functional MR imaging. Radiology 2006;240:177–186.
  29. Dickerson BC, Sperling RA: Functional abnormalities of the medial temporal lobe memory system in mild cognitive impairment and Alzheimer’s disease: insights from functional MRI studies. Neuropsychologia 2008;46:1624–1635.
  30. Brewer JB, Zhao Z, Desmond JE, Glover GH, Gabrieli JD: Making memories: brain activity that predicts how well visual experience will be remembered. Science 1998;281:1185–1187.
  31. Dickerson BC, Miller SL, Greve DN, Dale AM, Albert MS, Schacter DL, Sperling RA: Prefrontal-hippocampal-fusiform activity during encoding predicts intraindividual differences in free recall ability: an event-related functional-anatomic MRI study. Hippocampus 2007;17:1060–1070.
  32. Buckner RL, Wheeler ME, Sheridan MA: Encoding processes during retrieval tasks. J Cogn Neurosci 2001;13:406–415.
  33. Petersen RC, Morris JC: Mild cognitive impairment as a clinical entity and treatment target. Arch Neurol 2005;62:1160–1163; discussion 1167.
  34. Winblad B, Palmer K, Kivipelto M, Jelic V, Fratiglioni L, Wahlund LO, Nordberg A, Backman L, Albert M, Almkvist O, Arai H, Basun H, Blennow K, de Leon M, DeCarli C, Erkinjuntti T, Giacobini E, Graff C, Hardy J, Jack C, Jorm A, Ritchie K, van Duijn C, Visser P, Petersen RC: Mild cognitive impairment – beyond controversies, towards a consensus: report of the international working group on mild cognitive impairment. J Intern Med 2004;256:240–246.
  35. Oldfield RC: The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 1971;9:97–113.
  36. Bennett DA, Schneider JA, Buchman AS, Mendes de Leon C, Bienias JL, Wilson RS: The Rush Memory and Aging Project: study design and baseline characteristics of the study cohort. Neuroepidemiology 2005;25:163–175.
  37. Bennett DA, Wilson RS, Schneider JA, Evans DA, Beckett LA, Aggarwal NT, Barnes LL, Fox JH, Bach J: Natural history of mild cognitive impairment in older persons. Neurology 2002;59:198–205.
  38. Dickerson BC, Goncharova I, Sullivan MP, Forchetti C, Wilson RS, Bennett DA, Beckett LA, deToledo-Morrell L: MRI-derived entorhinal and hippocampal atrophy in incipient and very mild Alzheimer’s disease. Neurobiol Aging 2001;22:747–754.
  39. Morris JC, Heyman A, Mohs RC, Hughes JP, van Belle G, Fillenbaum G, Mellits ED, Clark C: The Consortium to Establish a Registry for Alzheimer’s disease (CERAD). I. Clinical and neuropsychological assessment of Alzheimer’s disease. Neurology 1989;39:1159–1165.
  40. Albert M, Smith LA, Scherr PA, Taylor JO, Evans DA, Funkenstein HH: Use of brief cognitive tests to identify individuals in the community with clinically diagnosed Alzheimer’s disease. Int J Neurosci 1991;57:167–178.
  41. Wechsler D: Wechsler Memory Scale-Revised. San Antonio, Psychological Corporation, Harcourt Brace Jovanovich, 1987.
  42. Folstein MF, Folstein SE, McHugh PR: ‘Mini-Mental State’: a practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 1975;12:189–198.
  43. Glover GH, Lai S: Self-navigated spiral fMRI: Interleaved versus single-shot. Magn Reson Med 1998;39:361–368.
  44. Glover GH, Lee AT: Motion artifacts in fMRI: comparison of 2DFT with PR and spiral scan methods. Magn Reson Med 1995;33:624–635.
  45. Snodgrass JG, Vanderwart M: A standardized set of 260 pictures: norms for name agreement, image agreement, familiarity, and visual complexity. J Exp Psychol Hum Learn 1980;6:174–215.
  46. Cohen JD, MacWhinney B, Flatt MR, Provost J: Psyscope: a new graphic interactive environment for designing psychology experiments. Behav Res Methods Instrum Comput 1993;25:257–271.
    External Resources
  47. Ofen N, Kao YC, Sokol-Hessner P, Kim H, Whitfield-Gabrieli S, Gabrieli JD: Development of the declarative memory system in the human brain. Nat Neurosci 2007;10:1198–1205.
  48. Ashburner J, Friston KJ: Nonlinear spatial normalization using basis functions. Hum Brain Mapp 1999;7:254–266.
  49. Friston KJ, Tononi G, Reeke GN Jr, Sporns O, Edelman GM: Value-dependent selection in the brain: simulation in a synthetic neural model. Neuroscience 1994;59:229–243.
  50. Friston KJ, Frith CD, Turner R, Frackowiak RS: Characterizing evoked hemodynamics with fMRI. Neuroimage 1995;2:157–165.
  51. Heun R, Jessen F, Klose U, Erb M, Granath DO, Grodd W: Response-related fMRI analysis during encoding and retrieval revealed differences in cerebral activation by retrieval success. Psychiatry Res 2000;99:137–150.
  52. Heun R, Jessen F, Klose U, Erb M, Granath DO, Grodd W: Response-related fMRI of veridical and false recognition of words. Eur Psychiatry 2004;19:42–52.
  53. Maldjian JA, Laurienti PJ, Kraft RA, Burdette JH: An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. Neuroimage 2003;19:1233–1239.
  54. Greicius MD, Flores BH, Menon V, Glover GH, Solvason HB, Kenna H, Reiss AL, Schatzberg AF: Resting-state functional connectivity in major depression: abnormally increased contributions from subgenual cingulate cortex and thalamus. Biol Psychiatry 2007;62:429–437.
  55. Petrella JR, Wang L, Krishnan S, Slavin MJ, Prince SE, Tran TT, Doraiswamy PM: Cortical deactivation in mild cognitive impairment: high-field-strength functional MR imaging. Radiology 2007;245:224–235.
  56. Bondi MW, Houston WS, Eyler LT, Brown GG: fMRI evidence of compensatory mechanisms in older adults at genetic risk for Alzheimer disease. Neurology 2005;64:501–508.
  57. Sperling RA, Bates JF, Chua EF, Cocchiarella AJ, Rentz DM, Rosen BR, Schacter DL, Albert MS: fMRI studies of associative encoding in young and elderly controls and mild Alzheimer’s disease. J Neurol Neurosurg Psychiatry 2003;74:44–50.
  58. Chetelat G, Desgranges B, Landeau B, Mezenge F, Poline JB, de la Sayette V, Viader F, Eustache F, Baron JC: Direct voxel-based comparison between grey matter hypometabolism and atrophy in Alzheimer’s disease. Brain 2008;131:60–71.
  59. DeToledo-Morrell L, Stoub TR, Bulgakova M, Wilson RS, Bennett DA, Leurgans S, Wuu J, Turner DA: MRI-derived entorhinal volume is a good predictor of conversion from MCI to AD. Neurobiol Aging 2004;25:1197–1203.
  60. Kircher T, Weis S, Freymann K, Erb M, Jessen F, Grodd W, Heun R, Leube DT: Hippocampal activation in MCI patients is necessary for successful memory encoding. J Neurol Neurosurg Psychiatry 2007;78:812–818.
  61. Hamalainen A, Pihlajamaki M, Tanila H, Hanninen T, Niskanen E, Tervo S, Karjalainen PA, Vanninen RL, Soininen H: Increased fMRI responses during encoding in mild cognitive impairment. Neurobiol Aging 2007;28:1889–1903.
  62. Wierenga CE, Bondi MW: Use of functional magnetic resonance imaging in the early identification of Alzheimer’s disease. Neuropsychol Rev 2007;17:127–143.
  63. Stark CE, Squire LR: When zero is not zero: the problem of ambiguous baseline conditions in fMRI. Proc Natl Acad Sci USA 2001;98:12760–12766.
  64. Craik FIM, Tulving E: Depth of processing and the retention of words in episodic memory. J Exp Psychol Gen 1975;104:168–294.
  65. Celone KA, Calhoun VD, Dickerson BC, Atri A, Chua EF, Miller SL, DePeau K, Rentz DM, Selkoe DJ, Blacker D, Albert MS, Sperling RA: Alterations in memory networks in mild cognitive impairment and Alzheimer’s disease: an independent component analysis. J Neurosci 2006;26:10222–10231.
  66. Miller SL, Fenstermacher E, Bates J, Blacker D, Sperling RA, Dickerson BC: Hippocampal activation in adults with mild cognitive impairment predicts subsequent cognitive decline. J Neurol Neurosurg Psychiatry 2008;79:630–635.
  67. Raichle ME, Gusnard DA: Intrinsic brain activity sets the stage for expression of motivated behavior. J Comp Neurol 2005;493:167–176.
  68. Krishnan S, Slavin MJ, Tran TT, Doraiswamy PM, Petrella JR: Accuracy of spatial normalization of the hippocampus: implications for fMRI research in memory disorders. Neuroimage 2006;31:560–571.
  69. Sandstrom CK, Krishnan S, Slavin MJ, Tran TT, Doraiswamy PM, Petrella JR: Hippocampal atrophy confounds template-based functional MR imaging measures of hippocampal activation in patients with mild cognitive impairment. AJNR Am J Neuroradiol 2006;27:1622–1627.