Hostname: page-component-cd9895bd7-q99xh Total loading time: 0 Render date: 2024-12-25T01:06:40.209Z Has data issue: false hasContentIssue false
  • English
  • Français

Functional magnetic resonance imaging changes in amnestic and nonamnestic mild cognitive impairment during encoding and recognition tasks

Published online by Cambridge University Press:  01 May 2009

MARY M. MACHULDA ,
MATTHEW L. SENJEM ,
STEPHEN D. WEIGAND ,
GLENN E. SMITH ,
ROBERT J. IVNIK ,
BRAD F. BOEVE ,
DAVID S. KNOPMAN ,
RONALD C. PETERSEN  and
CLIFFORD R. JACK JR
MARY M. MACHULDA*
Affiliation:
Department of Psychiatry and Psychology, Mayo Clinic, Rochester, Minnesota
MATTHEW L. SENJEM
Affiliation:
Department of Information Technology, Mayo Clinic, Rochester, Minnesota
STEPHEN D. WEIGAND
Affiliation:
Department of Health Sciences Research, Mayo Clinic, Rochester, Minnesota
GLENN E. SMITH
Affiliation:
Department of Psychiatry and Psychology, Mayo Clinic, Rochester, Minnesota
ROBERT J. IVNIK
Affiliation:
Department of Psychiatry and Psychology, Mayo Clinic, Rochester, Minnesota
BRAD F. BOEVE
Affiliation:
Department of Neurology, Mayo Clinic, Rochester, Minnesota
DAVID S. KNOPMAN
Affiliation:
Department of Neurology, Mayo Clinic, Rochester, Minnesota
RONALD C. PETERSEN
Affiliation:
Department of Neurology, Mayo Clinic, Rochester, Minnesota
CLIFFORD R. JACK JR
Affiliation:
Department of Radiology, Mayo Clinic, Rochester, Minnesota
*
*Correspondence and reprint requests to: Mary M. Machulda, Department of Psychiatry and Psychology, Mayo Clinic, 200 1st Street SW, Rochester, Minnesota 55905. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Functional magnetic resonance imaging (fMRI) shows changes in multiple regions in amnestic mild cognitive impairment (aMCI). The concept of MCI recently evolved to include nonamnestic syndromes, so little is known about fMRI changes in these individuals. This study investigated activation during visual complex scene encoding and recognition in 29 cognitively normal (CN) elderly, 19 individuals with aMCI, and 12 individuals with nonamnestic MCI (naMCI). During encoding, CN activated an extensive network that included bilateral occipital–parietal–temporal cortex; precuneus; posterior cingulate; thalamus; insula; and medial, anterior, and lateral frontal regions. Amnestic MCI activated an anatomic subset of these regions. Non-amnestic MCI activated an even smaller anatomic subset. During recognition, CN activated the same regions observed during encoding except the precuneus. Both MCI groups again activated a subset of the regions activated by CN. During encoding, CN had greater activation than aMCI and naMCI in bilateral temporoparietal and frontal regions. During recognition, CN had greater activation than aMCI in predominantly temporoparietal regions bilaterally, while CN had greater activation than naMCI in larger areas involving bilateral temporoparietal and frontal regions. The diminished parietal and frontal activation in naMCI may reflect compromised ability to perform nonmemory (i.e., attention/executive, visuospatial function) components of the task. (JINS, 2009, 15, 372–382.)

Keywords

Magnetic resonance imagingNeuropsychologyFrontal lobeParietal lobeTemporal lobeDementia
Type
Research Articles
Information
Journal of the International Neuropsychological Society , Volume 15 , Issue 3 , May 2009 , pp. 372 - 382
Copyright
Copyright © The International Neuropsychological Society 2009

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

Boeve, B., Ferman, T., Smith, G., Knopman, D., Jicha, G., Geda, Y., Silber, M., Edland, S., Parisi, J., Dickson, D., Ivnik, R., & Petersen, R. (2004). Mild cognitive impairment preceding dementia with Lewy bodies. Neurology, 62(Suppl 5), A86.Google Scholar
Cabeza, R. (2001). Cognitive neuroscience of aging: Contributions of functional neuroimaging. Scandinavian Journal of Psychology, 42, 277–286.Google Scholar
Celone, K., Calhoun, V., Dickerson, B., Atri, A., Chua, E., Miller, S., DePeau, K., Rentz, D., Selkoe, D., Blacker, D., Albert, M., & Sperling, R. (2006). Alterations in memory networks in mild cognitive impairment and Alzheimer’s disease: An independent component analysis. The Journal of Neuroscience, 26(40), 10222–10231.Google Scholar
Dickerson, B., Salat, D., Bates, J., Atiya, M., Killiany, R., Greve, D., Dale, A., Stern, C., Blacker, D., Albert, M., & Sperling, R. (2004). Medial temporal lobe function and structure in mild cognitive impairment. Annals of Neurology, 56, 27–35.CrossRefGoogle Scholar
Dickerson, B., Salat, D., Greve, D., Chua, E., Rand-Giovanetti, E., Rentz, D., Bertram, L., Mullin, K., Tanzi, R., Blacker, D., Albert, M., & Sperling, R. (2005). Increased hippocampal activation in mild cognitive impairment compared to normal aging and AD. Neurology, 65, 404–411.Google Scholar
Fletcher, P. & Henson, R. (2001). Frontal lobes and human memory: Insights from functional neuroimaging. Brain, 124, 849–881.CrossRefGoogle Scholar
Friston, K., Holmes, A., Worsley, K., Poline, J., Frith, C., & Frackowiak, R. (1995). Statistical parametric maps in functional imaging: A general linear approach. Human Brain Mapping, 2, 189–210.Google Scholar
Goekoop, R., Rombouts, S., Jonker, C., Hibbel, A., Knol, D., Truyen, L., Barkhof, F., & Scheltens, P. (2004). Challenging the cholinergic system in mild cognitive impairment: A pharmacological fMRI study. NeuroImage, 23, 1450–1459.Google Scholar
Gutchess, A., Welsh, R., Hedden, T., Bangert, A., Minear, M., Liu, L., & Park, D. (2005). Aging and the neural correlates of successful picture encoding: Frontal activations compensate for decreased medial-temporal activity. Journal of Cognitive Neuroscience, 17(1), 84–96.CrossRefGoogle Scholar
Heun, R., Freymann, K., Erb, M., Leube, D., Jessen, F., Kircher, T., & Grodd, W. (2007). Mild cognitive impairment (MCI) and actual retrieval performance affect cerebral activation in the elderly. Neurobiology of Aging, 28(3), 404–413.Google Scholar
Ivnik, R., Malec, J., Smith, G., Tangalos, E., & Petersen, R. (1996). Neuropsychological tests’ norms above age 55: COWAT, BNT, MAE Token, WRAT-R reading, AMNART, Stroop, TMT, and JLO. The Clinical Neuropsychologist, 10, 262–278.Google Scholar
Ivnik, R., Malec, J., Smith, G., Tangalos, E., Petersen, R., Kokmen, E., & Kurland, L. (1992). Mayo’s Older Americans Normative Studies: WAIS-R, WMS-R and AVLT norms for ages 56 through 97. The Clinical Neuropsychologist, 6(Suppl), 1–104.Google Scholar
Johnson, S., Baxter, L., Sussking-Wilder, L., Connor, D., Sabbagh, M., & Caselli, R. (2004). Hippocampal adaptation to face repetition in healthy elderly and mild cognitive impairment. Neuropsychologia, 42, 980–989.CrossRefGoogle Scholar
Johnson, S., Schmitz, T., Asthana, S., Gluck, M., & Myers, C. (2008). Associative learning over trial activates the hippocampus in healthy elderly but not mild cognitive impairment. Aging, Neuropsychology, and Cognition, 15, 129–145.Google Scholar
Johnson, S., Schmitz, T., Moritz, C., Meyerand, M., Rowley, H., Alexander, A., Hansen, K., Gleason, C., Carlsson, C., Ries, M., Asthana, S., Chen, K., Reiman, E., & Alexander, G. (2006). Activation of brain regions vulnerable to Alzheimer’s disease: The effect of mild cognitive impairment. Neurobiology of Aging, 27, 1604–1612.Google Scholar
Kaplan, E., Goodglass, H., & Weintraub, S. (1983). Boston Naming Test. Philadelphia, PA: Lea & Febiger.Google Scholar
Kokmen, E., Smith, G., Petersen, R., Tangalos, E., & Ivnik, R. (1991). The Short Test of Mental Status. Archives of Neurology, 48, 725–728.Google Scholar
Lucas, J.A., Ivnik, R.J., Smith, G.E., Bohac, D.L., Tangalos, E.G., Graff-Radford, N.R., & Petersen, R.C. (1998). Mayo’s Older Americans Normative Studies: Category fluency norms. Journal of Clinical and Experimental Neuropsychology, 20, 1–7.Google Scholar
Machielsen, W., Rombouts, S., Barkhof, F., Scheltens, P., & Witter, M. (2000). fMRI of visual encoding: Reproducibility of activation. Human Brain Mapping, 9, 156–164.Google Scholar
Machulda, M., Ward, H., Borowski, B., Gunter, J., Cha, R., O’Brien, P., Petersen, R., Boeve, B., Knopman, D., Tang-Wai, D., Ivnik, R., Smith, G., Tangalos, E., & Jack, C. (2003). Comparison of memory fMRI response among normal, MCI, and Alzheimer patients. Neurology, 61, 500–506.Google Scholar
Machulda, M., Ward, H., Cha, R., O’Brien, P., & Jack, C. Jr. (2001). Functional inferences vary with the method of analysis in fMRI. NeuroImage, 14, 1122–1127.Google Scholar
Morris, J. (1993). The Clinical Dementia Rating (CDR): Current version and scoring rules. Neurology, 43, 2412–2414.Google Scholar
Petersen, R. (2004). Mild cognitive impairment as a diagnostic entity. Journal of Internal Medicine, 256, 183–194.Google Scholar
Petersen, R., Doody, R., Kurz, A., Mohs, R., Morris, J., Rabins, P., Ritchie, K., Rossor, M., Thal, L., & Winblad, B. (2001). Current concepts in mild cognitive impairment. Archives of Neurology, 58, 1985–1992.Google Scholar
Petersen, R., Ivnik, R., Boeve, B., Knopman, D., Smith, G., & Tangalos, E. (2004). Outcome of clinical subtypes of mild cognitive impairment. Neurology, 62(Suppl 5), A295.Google Scholar
Petersen, R., Kokmen, E., Tangalos, E., Ivnik, R.K., & Kurland, L.T. (1990). Mayo Clinic Alzheimer’s Disease Patient Registry. Aging Clinical & Experimental Research, 2(4), 408–415.Google Scholar
Petersen, R., Smith, G., Waring, S., Ivnik, R., Tangalos, E., & Kokmen, E. (1999). Mild cognitive impairment clinical characterization and outcome. Archives of Neurology, 56, 303–308.Google Scholar
Petrella, J., Krishnan, S., Slavin, M., Tran, T.-T.T., Murty, L., & Doraiswamy, P. (2006). Mild cognitive impairment: Evaluation with 4-T functional MR imaging. Radiology, 240(1), 177–186.Google Scholar
Rey, A. (1964). L’examen Clinique en Psychologie. (The clinical examination in psychology). Paris, France: Presses Universitaires de France.Google Scholar
Rombouts, S., Scheltens, P., Machielsen, W., Barkhof, F., Hoogenraad, F., Veltman, D., Valk, J., & Witter, M. (1999). Parametric fMRI analysis of visual encoding in the human medial temporal lobe. Hippocampus, 9, 637–643.Google Scholar
Saykin, A., Wishart, H., Rabin, L., Flashman, L., McHugh, T.L., Mamourian, A., & Santulli, R. (2004). Cholinergic enhancement of frontal lobe activity in mild cognitive impairment. Brain, 127, 1574–1583.Google Scholar
Senjem, M., Gunter, J., Shiung, M., Petersen, R., & Jack, C.J. (2005). Comparison of different methodological implementations of voxel-based morphometry in neurodegenerative disease. NeuroImage, 26, 600–608.Google Scholar
Spreen, O. & Strauss, E. (1991). A compendium of neuropsychological tests: Administration, norms, and commentary. New York: Oxford University Press.Google Scholar
Wagner, A., Shannon, B., Kahn, I., & Buckner, R. (2005). Parietal lobe contributions to episodic memory retrieval. Trends in Cognitive Sciences, 9(9), 445–453.Google Scholar
Wechsler, D. (1981). Wechsler Adult Intelligence Scale—Revised. San Antonio, TX: The Psychological Corporation.Google Scholar
Wechsler, D. (1987). Wechsler Memory Scale—Revised. San Antonio, TX: The Psychological Corporation.Google Scholar
Whitwell, J., Petersen, R., Negash, S., Weigand, S., Ivnik, R., Knopman, D., Boeve, B., Smith, G., & Jack, C. Jr. (2007). Patterns of atrophy differ among specific subtypes of mild cognitive impairment. Archives of Neurology, 64(8), 1130–1138.Google Scholar
Whitwell, J., Shiung, M., Przybelski, S., Weigand, S., Knopman, D., Boeve, B., Petersen, R., & Jack, C. Jr. (2008). MRI patterns of atrophy associated with progression to AD in amnestic mild cognitive impairment. Neurology, 70, 512–520.Google Scholar
Winblad, B., Palmer, K., Kivipelto, M., Jelic, V., Fratiglioni, L., Wahlund, L.-O., Nordberg, A., Backman, L., Albert, M., Almkvist, O., Arai, H., Basun, H., Blennow, K., de Leon, C., Decarli, C., Erkinjuntti, T., Giacobini, E., Graff, C., Hardy, J., Jack, C.J., Jorm, A., Ritchie, K., Van Duijn, C., Visser, P., & Petersen, R. (2004). Mild cognitive impairment—Beyond controversies, towards a consensus: Report of the International Working Group on Mild Cognitive Impairment. Journal of Internal Medicine, 256, 240–246.Google Scholar
Yoshita, M., Fletcher, E., Harvey, D., Ortega, M., Martinez, O., Mungas, D.M., Reed, B.R., & DeCarli, C.S. (2006). Extent and distribution of white matter hyperintensities in normal aging, MCI, and AD. Neurology, 67(12), 2192–2198.Google Scholar
Zanetti, M., Ballabio, C., Abbate, C., Cutaia, C., Vergani, C., & Bergamaschini, L. (2006). Mild cognitive impairment subtypes and vascular dementia in community-dwelling elderly people: A 3-year follow-up study. Journal of the American Geriatrics Society, 54(4), 580–586.Google Scholar