Hostname: page-component-8448b6f56d-c47g7 Total loading time: 0 Render date: 2024-04-16T04:17:17.763Z Has data issue: false hasContentIssue false
  • English
  • Français

Event-Related Functional Magnetic Resonance Imaging Changes during Relational Retrieval in Normal Aging and Amnestic Mild Cognitive Impairment

Published online by Cambridge University Press:  24 May 2012

Kelly S. Giovanello ,
Felipe De Brigard ,
Jaclyn Hennessey Ford ,
Daniel I. Kaufer ,
James R. Burke ,
Jeffrey N. Browndyke  and
Kathleen A. Welsh-Bohmer
Kelly S. Giovanello*
Affiliation:
Department of Psychology, The University of North Carolina, Chapel Hill, North Carolina Biomedical Research Imaging Center, The University of North Carolina, Chapel Hill, North Carolina
Felipe De Brigard
Affiliation:
Department of Psychology, The University of North Carolina, Chapel Hill, North Carolina Department of Philosophy, The University of North Carolina, Chapel Hill, North Carolina
Jaclyn Hennessey Ford
Affiliation:
Department of Psychology, The University of North Carolina, Chapel Hill, North Carolina
Daniel I. Kaufer
Affiliation:
Department of Neurology, The University of North Carolina, Chapel Hill, North Carolina
James R. Burke
Affiliation:
Joseph & Kathleen Bryan Alzheimer's Disease Research Center, Duke University Medical Center, Durham, North Carolina Division of Neurology, Duke University Medical Center, Durham, North Carolina
Jeffrey N. Browndyke
Affiliation:
Joseph & Kathleen Bryan Alzheimer's Disease Research Center, Duke University Medical Center, Durham, North Carolina Department of Psychiatry & Behavioral Sciences, Duke University Medical Center, Durham, North Carolina
Kathleen A. Welsh-Bohmer
Affiliation:
Joseph & Kathleen Bryan Alzheimer's Disease Research Center, Duke University Medical Center, Durham, North Carolina Division of Neurology, Duke University Medical Center, Durham, North Carolina Department of Psychiatry & Behavioral Sciences, Duke University Medical Center, Durham, North Carolina
*
Correspondence and reprint requests to: Kelly S. Giovanello, Department of Psychology, The University of North Carolina, Campus Box 3270, Chapel Hill, NC 27713. E-mail: kgio@unc.edu
Get access Rights & Permissions [Opens in a new window]

Abstract

The earliest cognitive deficits observed in amnestic mild cognitive impairment (aMCI) appear to center on memory tasks that require relational memory (RM), the ability to link or integrate unrelated pieces of information. RM impairments in aMCI likely reflect neural changes in the medial temporal lobe (MTL) and posterior parietal cortex (PPC). We tested the hypothesis that individuals with aMCI, as compared to cognitively normal (CN) controls, would recruit neural regions outside of the MTL and PPC to support relational memory. To this end, we directly compared the neural underpinnings of successful relational retrieval in aMCI and CN groups, using event-related functional magnetic resonance imaging (fMRI), holding constant the stimuli and encoding task. The fMRI data showed that the CN, compared to the aMCI, group activated left precuneus, left angular gyrus, right posterior cingulate, and right parahippocampal cortex during relational retrieval, while the aMCI group, relative to the CN group, activated superior temporal gyrus and supramarginal gyrus for this comparison. Such findings indicate an early shift in the functional neural architecture of relational retrieval in aMCI, and may prove useful in future studies aimed at capitalizing on functionally intact neural regions as targets for treatment and slowing of the disease course. (JINS, 2012, 18, 1–12)

Keywords

Mild cognitive impairmentAgingMemoryFunctional MRIMedial temporal lobeParietal lobe
Type
Research Articles
Information
Journal of the International Neuropsychological Society , Volume 18 , Issue 5 , September 2012 , pp. 886 - 897
Copyright
Copyright © The International Neuropsychological Society 2012

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

Anderson, N.D., Ebert, P.L., Jennings, J.M., Grady, C.L., Cabeza, R., Graham, S.J. (2008). Recollection- and familiarity-based memory in healthy aging and amnestic mild cognitive impairment. Neuropsychology, 22, 177–187.Google Scholar
Brainerd, C.J., Reyna, V.F. (1990). Gist is the gist: The fuzzy-trace theory and new intuitionism. Developmental Review, 10, 3–47.CrossRefGoogle Scholar
Buckner, R.L., Andrews-Hanna, J.R., Schacter, D.L. (2008). The brain's default network: Anatomy, function, and relevance to disease. Annals of the New York Academy of Sciences, 1124, 1–38.Google Scholar
Buckner, R.L., Snyder, A.Z., Shannon, B.J., LaRossa, G., Sachs, R., Fotenos, A.F., Mintun, M.A. (2005). Molecular, structural, and functional characterization of Alzheimer's disease: Evidence for a relationship between default activity, amyloid, and memory. Journal of Neuroscience, 25, 7709–7717.CrossRefGoogle ScholarPubMed
Burgess, P.W., Simons, J.S., Dumontheil, I., Gilbert, S.J. (2005). The gateway hypothesis of rostral prefrontal cortex (area 10) function. In J Duncan, L Phillips, P McLeod (Eds), Measuring the mind: Speed, control, and age (pp. 217–248). Oxford: Oxford University Press.Google Scholar
Cabeza, R. (2008). Role of parietal regions in episodic memory retrieval: The dual attentional processes hypothesis. Neuropsychologia, 46, 1813–1827.Google Scholar
Cabeza, R., Ciaramelli, E., Olson, I.R., Moscovitch, M. (2008). The parietal cortex and episodic memory: An attentional account. Nature Reviews Neuroscience, 9, 613–625.CrossRefGoogle ScholarPubMed
Cabeza, R., Nyberg, L. (2000). Neural bases of learning and memory: Functional neuroimaging evidence. Current Opinion in Neurology, 13, 415–421.CrossRefGoogle ScholarPubMed
Celone, K., Calhoun, V., Dickerson, B., Atri, A., Chua., E., Miller, S., Sperling, R. (2006). Alterations in memory networks in mild cognitive impairment and Alzheimer's disease: An independent component analysis. The Journal of Neuroscience, 26, 10222–10231.CrossRefGoogle ScholarPubMed
Ciaramelli, E., Grady, C.L., Levine, B., Ween, J., Moscovitch, M. (2010). Top-down and bottom-up attention to memory are dissociated in posterior parietal cortex: Neuroimaging and neuropsychological evidence. Journal of Neuroscience, 30, 4943–4956.CrossRefGoogle Scholar
Convit, A., de Leon, M.J., Tarshishi, C., De Santri, S., Tsui, W., Rusinek, H., George, A.E. (1997). Specific hippocampal volume reductions in individuals at risk for Alzheimer's disease. Neurobiology of Aging, 18, 131–138.Google Scholar
Corbetta, M., Kincade, J.M., Ollinger, J.M., McAvoy, M.P., Shulman, G.L. (2000). Voluntary orienting is dissociated from target detection in human posterior parietal cortex. Nature Neuroscience, 3, 292–297.Google Scholar
Corbetta, M., Shulman, G.L. (2002). Control of goal-directed and stimulus-driven attention in the brain. Nature Reviews Neuroscience, 3, 201–215.Google Scholar
Dalla Barba, G., Parlato, V., Jobert, A., Samson, Y., Pappata, S. (1998). Cortical networks implicated in semantic and episodic memory: Common or unique? Cortex, 34, 547–561.CrossRefGoogle ScholarPubMed
Davis, S.W., Dennis, N.A., Daselaar, S.M., Fleck, M.S., Cabeza, R. (2008). Qué PASA? The posterior-anterior shift in aging. Cerebral Cortex, 18, 1201–1209.Google Scholar
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.Google Scholar
Dennis, N.A., Kim, H., Cabeza, R. (2008). Age-related differences in brain activity during true and false memory retrieval. Journal of Cognitive Neuroscience, 20, 1390–1402.Google Scholar
Dickerson, B.C., Goncharova, I., Sullivan, M.P., Forchetti, C., Wilson, R.S., Bennett, D.A., deToledo-Morrell, L. (2001). MRI-derived entorhinal and hippocampal atrophy in incipient and very mild Alzheimer's disease. Neurobiology of Aging, 22, 747–754.CrossRefGoogle ScholarPubMed
Dickerson, B.C., Salat, D.H., Greve, D.N., Chua, E.F., Rand-Giovannetti, E., Rentz, D.M., Sperling, R.A. (2005). Increased hippocampal activation in mild cognitive impairment compared to normal aging and AD. Neurology, 65, 404–411.Google Scholar
Dickerson, B.C., Sperling, R.A. (2009). Large-scale functional brain network abnormalities in Alzheimer's disease: Insights from functional neuroimaging. Behavioral Neurology, 21, 63–75.Google Scholar
Dobbins, I.G., Wagner, A.D. (2005). Domain-general and domain-sensitive prefrontal mechanisms for recollecting events and detecting novelty. Cerebral Cortex, 15, 1768–1778.Google Scholar
Du, A.T., Schuff, N., Amend, D., Laakso, M.P., Hsu, Y.Y., Jagust, W.J., Weiner, M.W. (2001). Magnetic resonance imaging of the entorhinal cortex and hippocampus in mild cognitive impairment and Alzheimer's disease. Journal of Neurology, Neurosurgery, and Psychiatry, 71, 441–447.CrossRefGoogle ScholarPubMed
Düzel, E., Cabeza, R., Picton, T.W., Yonelinas, A.P., Scheich, H., Heinze, H.J., Tulving, E. (1999). Task-related and item-related brain processes of memory retrieval. Proceedings of the National Academy of Sciences of the United States of America, 96, 1794–1799.Google Scholar
Eichenbaum, H., Yonelinas, A.P., Ranganath, C. (2007). The medial temporal lobe and recognition memory. Annual Review of Neuroscience, 30, 123–152.Google Scholar
Fisher, R.A. (1950). Statistical methods for research workers. London: Oliver and Boyd.Google Scholar
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 Psychiatry Research, 12, 189–198.Google Scholar
Fowler, K.S., Saling, M.M., Conway, E.L., Semple, J.M., Louis, W.J. (2002). Paired associate performance in the early detection of DAT. Journal of the International Neuropsychological Society, 8, 58–71.Google Scholar
Friederici, A.D., Makuuchi, M., Bahlmann, J. (2009). The role of the posterior superior temporal cortex in sentence comprehension. Neuroreport, 20, 563–568.Google Scholar
Giovanello, K.S., Schacter, D.L. (2012). Reduced specificity of hippocampal and posterior ventrolateral prefrontal activity during relational retrieval in normal aging. Journal of Cognitive Neuroscience, 24, 159–170.Google Scholar
Glisky, E.L., Rubin, S.R., Davidson, P.S. (2001). Source memory in older adults: An encoding or retrieval problem? Journal of Experimental Psychology: Learning, Memory, and Cognition, 27, 1131–1146.Google ScholarPubMed
Golde, T.E. (2006). Disease modifying therapy for AD? Journal of Neurochemistry, 99, 689–707.CrossRefGoogle Scholar
Grundman, M., Sencakova, D., Jack, C.R. Jr., Petersen, R.C., Kim, H.T., Schultz, A., Thal, L.J. (2002). Brain MRI hippocampal volume and prediction of clinical status in a mild cognitive impairment trial. Journal of Molecular Neuroscience, 19, 23–27.Google Scholar
Hachinski, V.C., Iliff, L.D., Zilhka, E., Du Boulay, G.H., McAllister, V.L., Marshall, J., Symon, L. (1975). Cerebral blood flow in dementia. Archives of Neurology, 32, 632–637.Google Scholar
Hayden, K.M., Jones, R.N., Zimmer, C., Plassman, B., Browndyke, J.N., Pieper, C., Welsh-Bohmer, K.A. (2011). Factor structure of the National Alzheimer's Coordinating Centers Uniform Dataset Neuropsychological Battery: An evaluation of invariance between and within diagnostic groups over time. Alzheimer's and Association Disorders, 25, 128–137.Google Scholar
Herholz, K., Salmon, E., Perani, D., Baron, J.C., Holthoff, V., Frölich, L., Heiss, W.D. (2002). Discrimination between Alzheimer dementia and controls by automated analysis of multicenter FDG PET. Neuroimage, 17, 302–316.CrossRefGoogle ScholarPubMed
Hockley, W.A., Consoli, C. (1999). Familiarity and recollection in item and associative recognition. Memory and Cognition, 27, 657–664.Google Scholar
Iidaka, T., Anderson, N.D., Kapur, S., Cabeza, R., Craik, F.I. (2000). The effect of divided attention on encoding and retrieval in episodic memory revealed by positron emission tomography. Journal of Cognitive Neuroscience, 12, 267–280.Google Scholar
Ivanoiu, A., Adam, S., Van der Linden, M., Salmon, E., Juillerat, A.C., Mulligan, R., Seron, X. (2005). Memory evaluation with a new cued recall test in patients with mild cognitive impairment and Alzheimer's disease. Journal of Neurology, 252, 47–55.CrossRefGoogle ScholarPubMed
Jack, C.R. Jr., 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.Google Scholar
Kaplan, E., Goodglass, H., Weintraub, S. (1983). Boston Naming Test. Philadelphia, PA: Lea and Febiger.Google Scholar
Kaye, J.A., Moore, M.M., Dame, A., Quinn, J., Camicioli, R., Howieson, D., Sexton, G. (2005). Asynchronous regional brain volume losses in presymptomatic to moderate AD. Journal of Alzheimer's Disease, 8, 51–56.CrossRefGoogle ScholarPubMed
Kelley, W.M., Macrae, C.N., Wyland, C.L., Caglar, S., Inati, S., Heatherton, T.F. (2002). Finding the self? An event-related fMRI study. Journal of Cognitive Neuroscience, 14, 785–794.Google Scholar
Killiany, R.J., Gomez-Isla, T., Moss, M., Kikinis, R., Sandor, T., Jolesz, F., Albert, M.S. (2000). Use of structural magnetic resonance imaging to predict who will get Alzheimer's disease. Annals of Neurology, 47, 430–439.Google Scholar
Kramer, J.H., Nelson, A., Johnson, J.K., Yaffe, K., Glenn, S., Rosen, H.J., Miller, B.L. (2006). Multiple cognitive deficits in amnestic mild cognitive impairment. Dementia and Geriatric Cognitive Disorders, 22, 306–311.Google Scholar
Lazar, N.A., Luna, B., Sweeney, J.A., Eddy, W.F. (2002). Combining brains: a survey of methods for statistical pooling of information. Neuroimage, 16, 538–550.Google Scholar
Lenzi, D., Serra, L., Perri, R., Pantano, P., Lenzi, G.L., Paulesu, E., Macaluso, E. (2011). Single domain amnestic MCI: A multiple cognitive domains fMRI investigation. Neurobiology of Aging, 32, 1542–1557.Google Scholar
Lepage, M., Ghaffar, O., Nyberg, L., Tulving, E. (2000). Prefrontal cortex and episodic memory retrieval mode. Proceedings of the National Academy of Sciences of the United States of America, 97, 506–511.CrossRefGoogle ScholarPubMed
Lieberman, M.D., Cunningham, W.A. (2009). Type I and Type II error concerns in fMRI research: re-balancing the scale. Social Cognitive and Affective Neuroscience, 4, 423–428.CrossRefGoogle ScholarPubMed
Machulda, M.M., Senjem, M.L., Weigand, S.D., Smith, G.E., Ivnik, R.J., Boeve, B.F., Jackie, C.R. (2009). Functional magnetic resonance imaging changes in amnestic and nonamnestic mild cognitive impairment during encoding and recognition tasks. Journal of the International Neuropsychological Society, 15, 372–382.CrossRefGoogle ScholarPubMed
Minoshima, S., Giordani, B., Berent, S., Frey, K.A., Foster, N.L., Kuhl, D.E. (1997). Metabolic reduction in the posterior cingulate cortex in very early Alzheimer's disease. Annals of Neurology, 42, 85–94.Google Scholar
Mitchell, J.P., Macrae, C.N., Banaji, M.R. (2004). Encoding-specific effects of social cognition on the neural correlates of subsequent memory. Journal of Neuroscience, 24, 4912–4917.Google Scholar
Morris, J.C., Heyman, A., Mohs, R.C., Hughes, J.P., van Belle, G., Fillenbaum, G., Clark, C. (1989). The Consortium to Establish a Registry for Alzheimer's Disease (CERAD). Part I. Clinical and neuropsychological assessment of Alzheimer's disease. Neurology, 39, 1159–1165.Google Scholar
Nyberg, L., Tulving, E., Habib, R., Nilsson, L.G., Kapur, S., Houle, S., McIntosh, A.R. (1995). Functional brain maps of retrieval mode and recovery of episodic information. Neuroreport, 7, 249–252.CrossRefGoogle ScholarPubMed
Petrella, J.R., Prince, S.E., Wang, L., Hellegers, C., Doraiswamy, P.M. (2007). Prognostic value of posteromedial cortex deactivation in mild cognitive impairment. PLoS One, 2, e1104.Google Scholar
Pennanen, C., Kivipelto, M., Tuomainen, S., Hartikainen, P., Hänninen, T., Laakso, M.P., Soininen, H. (2004). Hippocampus and entorhinal cortex in mild cognitive impairment and early AD. Neurobiology of Aging, 25, 303–310.Google Scholar
Petersen, R.C. (2004). Mild cognitive impairment as a diagnostic entity. Journal of Internal Medicine, 256, 183–194.CrossRefGoogle ScholarPubMed
Petersen, R.C., Smith, G.E., Waring, S.C., Ivnik, R.J., Tangalos, E., Kokmen, E. (1999). Mild cognitive impairment: Clinical characterization and outcome. Archives of Neurology, 56, 303–308.Google Scholar
Raichle, M.E., Snyder, A.Z. (2007). A default mode of brain function: A brief history of an evolving idea. Neuroimage, 37, 1083–1090.Google Scholar
Rajah, M.N., Kromas, M., Han, J.E., Pruessner, J.C. (2010). Group differences in anterior hippocampal volume and in the retrieval of spatial and temporal context memory in healthy young versus older adults. Neuropsychologia, 48, 4020–4030.Google Scholar
Reiman, E.M., Caselli, R.J., Yun, L.S., Chen, K., Bandy, D., Minoshima, S., Osborne, D. (1996). Preclinical evidence of Alzheimer's disease in persons homozygous for the epsilon 4 allele for apolipoprotein E. New England Journal of Medicine, 334, 752–758.Google Scholar
Rodrigue, K.M., Raz, N. (2004). Shrinkage of the entorhinal cortex over five years predicts memory performance in healthy adults. Journal of Neuroscience, 24, 956–963.Google Scholar
Rombouts, S.A., Goekoop, R., Stam, C.J., Barkhof, F., Scheltens, P. (2005). Delayed rather than decreased BOLD response as a marker for early Alzheimer's disease. Neuroimage, 26, 1078–1085.Google Scholar
Rosen, A.C., Prull, M.W., Gabrieli, J.D., Stoub, T., O'Hara, R., Friedman, L., deToledo-Morrell, L. (2003). Differential associations between entorhinal and hippocampal volumes and memory performance in older adults. Behavioral Neuroscience, 117, 1150–1160.CrossRefGoogle ScholarPubMed
Schacter, D.L., Gallo, D.A., Kensinger, E.A. (2007). The cognitive neuroscience of implicit and false memories: Perspectives on processing specificity. In J.S. Nairne (Ed.),, The foundations of remembering: Essays in honor of Henry L. Roediger III (pp. 353–378). New York: Psychology Press.Google Scholar
Shipley, W.S. (1967). Shipley Institute of Living Scale. Los Angeles, CA: Western Psychological Services.Google Scholar
Simons, J.S., Gilbert, S.J., Owen, A.M., Fletcher, P.C., Burgess, P.W. (2005). Distinct roles for lateral and medial anterior prefrontal cortex in contextual recollection. Journal of Neurophysiology, 94, 813–820.Google Scholar
Simons, J.S., Owen, A.M., Fletcher, P.C., Burgess, P.W. (2005). Anterior prefrontal cortex and the recollection of contextual information. Neuropsychologia, 43, 1774–1783.Google Scholar
Spreen, O., Strauss, E. (1991). A compendium of neuropsychological tests: Administration, norms, and commentary. New York: Oxford University Press.Google Scholar
Trivedi, M.A., Murphy, C.M., Goetz, C., Shah, R.C., Gabrieli, J.D., Whitfield-Gabrieli, S., Stebbins, G.T. (2008). fMRI activation changes during successful episodic memory encoding and recognition in amnestic mild cognitive impairment relative to cognitively healthy older adults. Dementia and Geriatric Cognitive Disorders, 26, 123–137.Google Scholar
Troyer, A.K., Murphy, K.J., Anderson, N.D., Hayman-Abello, B.A., Craik, F.I., Moscovitch, M. (2008). Item and associative memory in amnestic mild cognitive impairment: performance on standardized memory tests. Neuropsychology, 22, 10–16.CrossRefGoogle ScholarPubMed
Tschanz, J.T., Welsh-Bohmer, K.A., Lykestos, C.G., Corcoran, C., Green, R.C., Norton, M.C., Breitner, J.C.S.and the Cache County Investigators (2006). Conversion to dementia from mild cognitive disorder: The Cache County Study. Neurology, 67, 229–234.Google Scholar
Tulving, E. (1983). Elements of episodic memory. Oxford: Clarendon Press.Google Scholar
Velanova, K., Jacoby, L.L., Wheeler, M.E., McAvoy, M.P., Peterson, S.E., Buckner, R.L. (2003). Functional-anatomic correlates of sustained and transient processing components engaged during controlled retrieval. The Journal of Neuroscience, 23, 8460–8470.Google Scholar
Wagner, A., Shannon, B., Kahn, I., Buckner, R.L. (2005). Parietal lobe contributions to episodic memory retrieval. Trends in Cognitive Sciences, 9, 445–453.Google Scholar
Wang, K., Liang, M., Wang, L., Tian, L., Zhang, X., Li, K., Jiang, T. (2007). Altered functional connectivity in early Alzheimer's disease: a resting-state fMRI study. Human Brain Mapping, 28, 967–978.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
Wheeler, M.E., Buckner, R.L. (2004). Functional-anatomic correlates of remembering and knowing. Neuroimage, 21, 1337–1349.Google Scholar
Winblad, B., Palmer, K., Kivipelto, M., Jelic, V., Fratiglioni, L., Wahlund, L.O., 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
Xu, Y.C., Jack, C.R., O'Brien, P.C., Kokmen, E., Smith, G.E., Ivnik, R.J., Petersen, R.C. (2000). Usefulness of MRI measures of entorhinal cortex versus hippocampus in AD. Neurology, 54, 1760–1767.Google Scholar
Yonelinas, A.P. (2001). Components of episodic memory: the contribution of recollection and familiarity. Philosophical Transactions Royal Society London B Biological Science, 356, 1363–1374.Google Scholar
Yonelinas, A.P., Otten, L.J., Shaw, K.N., Rugg, M.D. (2005). Separating the brain regions involved in recollection and familiarity in recognition memory. Journal of Neuroscience, 25, 3002–3008.Google Scholar