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Compensatory Brain Activity during Encoding among Older Adults with Better Recognition Memory for Face-Name Pairs: An Integrative Functional, Structural, and Perfusion Imaging Study

Published online by Cambridge University Press:  20 March 2012

Katherine J. Bangen ,
Allison R. Kaup ,
Heline Mirzakhanian ,
Christina E. Wierenga ,
Dilip V. Jeste  and
Lisa T. Eyler
Katherine J. Bangen*
Affiliation:
Department of Psychiatry, University of California San Diego, La Jolla, California
Allison R. Kaup
Affiliation:
San Diego State University/University of California, San Diego Joint Doctoral Program in Clinical Psychology, San Diego, California
Heline Mirzakhanian
Affiliation:
Department of Psychiatry, University of California San Diego, La Jolla, California
Christina E. Wierenga
Affiliation:
Department of Psychiatry, University of California San Diego, La Jolla, California Research Service, Veterans Affairs San Diego Healthcare System, San Diego, California
Dilip V. Jeste
Affiliation:
Department of Psychiatry, University of California San Diego, La Jolla, California Sam and Rose Stein Institute for Research on Aging, La Jolla, California
Lisa T. Eyler
Affiliation:
Department of Psychiatry, University of California San Diego, La Jolla, California Sam and Rose Stein Institute for Research on Aging, La Jolla, California Desert-Pacific Mental Illness Research, Education, and Clinical Center, Veterans Affairs San Diego Healthcare System, San Diego, California
*
Correspondence and reprint requests to: Katherine J. Bangen, 9500 Gilman Drive # 9151B, La Jolla, CA 92093-9151B, E-mail: kbangen@ucsd.edu
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Abstract

Many neuroimaging studies interpret the commonly reported findings of age-related increases in frontal response and/or increased bilateral activation as suggestive of compensatory neural recruitment. However, it is often unclear whether differences are due to compensation or reflective of other cognitive or physiological processes. This study aimed to determine whether there are compensatory age-related changes in brain systems supporting successful associative encoding while taking into account potentially confounding factors including age-related differences in task performance, atrophy, and resting perfusion. Brain response during encoding of face-name pairs was measured using functional magnetic resonance imaging in 10 older and nine young adults and was correlated with memory performance. During successful encoding, older adults demonstrated increased frontal and decreased occipital activity as well as greater bilateral involvement relative to the young. Findings remained significant after controlling for age-related cortical atrophy and hypoperfusion. Among the older adults, greater response was associated with better memory performance. Cognitive aging may involve recruitment of compensatory mechanisms to improve performance or prevent impairment. Results extend previous findings by suggesting that age-related alterations in activation cannot be attributed to the commonly observed findings of poorer task performance, reduced resting perfusion, or cortical atrophy among older adults. (JINS, 2012, 18, 402–413)

Keywords

Magnetic resonance imagingAgingCognitionFrontal lobeNeuropsychologyPaired associate learning

Information

Type
Research Articles
Information
Journal of the International Neuropsychological Society , Volume 18 , Issue 3 , May 2012 , pp. 402 - 413
Copyright
Copyright © The International Neuropsychological Society 2012

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References

Bangen, K. J., Restom, K., Liu, T. T., Jak, A. J., Wierenga, C. E., Salmon, D. P., Bondi, M. W. (2009). Differential age effects on cerebral blood flow and BOLD response to encoding: Associations with cognition and stroke risk. Neurobiology of Aging, 30, 1276–1287.CrossRefGoogle ScholarPubMed
Beck, A. T., Steer, R. A. (1993). Beck anxiety inventory manual. San Antonio, TX: Psychological Corporation.Google Scholar
Buckner, R. L., Head, D., Parker, J., Fotenos, A. F., Marcus, D., Morris, J. C., Snyder, A. Z. (2004). A unified approach for morphometric and functional data analysis in young, old, and demented adults using automated atlas-based head size normalization: Reliability and validation against manual measurement of total intracranial volume. Neuroimage, 23, 724–738.CrossRefGoogle ScholarPubMed
Cabeza, R. (2002). Hemispheric asymmetry reduction in older adults: The HAROLD model. Psychology and Aging, 17, 85–100.CrossRefGoogle ScholarPubMed
Cabeza, R., Grady, C. L., Nyberg, L., McIntosh, A. R., Tulving, E., Kapur, S., Craik, F. I. M. (1997). Age-related differences in neural activity during memory encoding and retrieval: A positron emission tomography study. The Journal of Neuroscience, 17, 391–400.CrossRefGoogle ScholarPubMed
Chalela, J. A., Alsop, D. C., Gonzalex-Atavales, J. B., Maldjian, J. A., Kasner, S. E., Detre, J. A. (2000). Magnetic resonance perfusion imaging in acute ischemic stroke using continuous arterial spin labeling. Stroke, 31, 680–687.CrossRefGoogle ScholarPubMed
Cox, R. W. (1996). AFNI: Software for analysis and visualization of functional magnetic resonance neuroimages. Computers and Biomedical Research, 29, 162–173.CrossRefGoogle ScholarPubMed
Dale, A. M., Fischl, B., Sereno, M. I. (1999). Cortical surface-based analysis. I. Segmentation and surface reconstruction. Neuroimage, 9, 179–194.CrossRefGoogle ScholarPubMed
Davis, S. W., Dennis, N. A., Daselaar, S. M., Fleck, M. S., Cabeza, R. (2008). Que PASA? The posterior-anterior shift in aging. Cerebral Cortex, 18, 1201–1209.CrossRefGoogle ScholarPubMed
Delis, D. C., Kramer, J. H., Kaplan, E., Ober, B. A. (2000). The California Verbal Learning Test—Second Edition. New York: Psychological Corporation.Google Scholar
Depp, C., Vahia, I. V., Jeste, D. (2010). Successful aging: Focus on cognitive and emotional health. Annual Review of Clinical Psychology, 6, 527–550.CrossRefGoogle ScholarPubMed
D'Esposito, M., Deouell, L. Y., Gazzaley, A. (2003). Alterations in the BOLD FMRI signal with ageing and disease: A challenge for neuroimaging. Nature Reviews Neuroscience, 4, 863–872.CrossRefGoogle ScholarPubMed
Duverne, S., Motamedinia, S., Rugg, M. D. (2009). The relationship between aging, performance, and the neural correlates of successful memory encoding. Cerebral Cortex, 19, 733–744.CrossRefGoogle ScholarPubMed
Eyler, L. T., Sherzai, A., Kaup, A. R., Jeste, D. V. (2011). A review of functional brain imaging correlates of successful cognitive aging. Biological Psychiatry, 70, 115–122.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Grady, C. L., McIntosh, A. R., Horwtiz, B., Maisog, J. A., Ungerleider, L. G., Mentis, M. J., Haxby, J. V. (1995). Age-related reductions in human recognition memory due to impaired encoding. Science, 269, 218–221.CrossRefGoogle ScholarPubMed
Han, S. D., Bangen, K. J., Bondi, M. W. (2009). Functional magnetic resonance imaging of compensatory neural recruitment in adding and risk for Alzheimer's disease: Review and recommendations. Dementia and Geriatric Cognitive Disorders, 27, 1–10.CrossRefGoogle Scholar
Han, S. D., Houston, W. S., Jak, A. J., Eyler, L. T., Nagel, B. J., Fleisher, A. S., Bondi, M. W. (2007). Verbal paired-associate learning by APOE genotype in non-demented older adults: FMRI evidence of a right hemispheric compensatory response. Neurobiology of Aging, 28, 238–247.CrossRefGoogle ScholarPubMed
Hedden, T., Gabrieli, J. D. E. (2004). Insights into the aging mind: A view from cognitive neuroscience. Nature Reviews Neuroscience, 5, 87–96.CrossRefGoogle ScholarPubMed
Johnson, S. C., Saykin, A. J., Flashman, L. A., McAllister, T. W., Sparling, M. B. (2001). Brain activation on fMRI and verbal memory ability: Functional neuroanatomic correlates of CVLT performance. Journal of the International Neuropsychological Society, 7, 55–62.CrossRefGoogle ScholarPubMed
Kongs, S. K., Thompson, L. L., Iverson, G. L., Heaton, R. K. (2000). Wisconsin Card Sorting Test—64-card version: Professional manual. Odessa, FL: Psychological Assessment Resources.Google Scholar
Li, S. C., Lindenberger, U. (1999). Cross-level unification: A computational exploration of the link between deterioration of cognitive abilities in old age. In: L. G. Nilsson & H. J., Markowitsch (Eds.), Cognitive neuroscience of memory (pp. 103–146). Seattle, WA: Hogrefe & Huber Publishers.Google Scholar
Logan, J. M., Sanders, A. L., Snyder, A. Z., Morris, J. C., Buckner, R. L. (2002). Underrecruitment and nonselective recruitment: Dissociable neural mechanisms associated with aging. Neuron, 33, 827–840.CrossRefGoogle ScholarPubMed
Miller, S. L., Celone, K., Depeau, K., Diamond, E., Dickerson, B. C., Rentz, D. M., Sperling, R. A. (2008). Age-related memory impairment associated with loss of parietal deactivation but preserved hippocampal activation. Proceedings of the National Academy of Sciences of the United States of America, 105, 2181–2186.CrossRefGoogle ScholarPubMed
Minati, L., Grisoli, M., Bruzzone, M. G. (2007). MR spectroscopy, functional MRI, and diffusion-tensor imaging in the aging brain: A conceptual review. Journal of Geriatric Psychiatry and Neurology, 20, 3–21.CrossRefGoogle ScholarPubMed
Papp, K. V., Walsh, S. J., Snyder, P. J. (2009). Immediate and delayed effects of cognitive interventions in healthy elderly: A review of current literature and future directions. Alzheimers & Dementia, 5, 50–60.CrossRefGoogle ScholarPubMed
Phillips, P. J., Moon, H., Rizvi, S. A., Rauss, P. (2000). The FERET evaluation methodology for face-recognition algorithms. IEEE Transactions on Pattern Analysis and Machine Intelligence, 22, 1090–1104.CrossRefGoogle Scholar
Phillips, P. J., Wechsler, H., Huang, J., Rauss, P. (1998). The FERET database and evaluation procedure for face recognition algorithms. Image and Vision Computing, 16, 295–306.CrossRefGoogle Scholar
Reuter-Lorenz, P. A. (2002). New visions of the aging mind and brain. Trends in Cognitive Sciences, 6, 394–400.Google Scholar
Rowe, J. W., Kahn, R. L. (1997). Successful aging. The Gerontologist, 37, 433–440.CrossRefGoogle ScholarPubMed
Seghier, M. L. (2008). Laterality index in functional MRI: Methodological issues. Magnetic Resonance Imaging, 26, 594–601.CrossRefGoogle ScholarPubMed
Smith, S. M., Jenkinson, M., Woolrich, M. W., Beckmann, C. E., 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
Sperling, R. (2007). Functional MRI studies of associative encoding in normal aging, mild cognitive impairment, and Alzheimer's disease. Annals of the New York Academy of Sciences, 1097, 146–155.CrossRefGoogle ScholarPubMed
Sperling, R. A., Bates, J. F., Chua, E. F., Cocchiarella, A. J., Rentz, D. M., Rosen, B. R., Albert, M. S. (2003). fMRI studies of associative encoding in young and elderly controls and mild AD patients. Journal of Neurology, Neurosurgery, and Psychiatry, 74, 44–50.CrossRefGoogle Scholar
Talairach, J., Tournoux, P. (1988). Co-Planar stereotaxic atlas of the human brain. New York: Thiem Medical Publishers.Google Scholar
Wechsler, D. (1997a). Wechsler Adult Intelligence Scale—Third Edition. San Antonio, TX: Psychological Corporation.Google Scholar
Wechsler, D. (1997b). Wechsler Memory Scale—Third Edition. San Antonio, TX: Harcourt Assessment.Google Scholar
Welford, A. T. (1965). Performance, biological mechanisms and age: A theoretical sketch. In A. T. Welford & J. E. Birren (Eds.), Behavior, aging, and the nervous system (pp. 3–20). Springfield, IL: Thomas.Google Scholar
Wierenga, C. E., Bondi, M. W. (2007). Use of functional magnetic resonance imaging in the early identification of Alzheimer's disease. Neuropsychology Review, 17, 127–143.CrossRefGoogle ScholarPubMed
Wilson, R. S., Beckett, L. A., Barnes, L. L., Schneider, J. A., Bach, J., Evans, D. A., Bennett, D. A. (2002). Individual differences in rates of change in cognitive abilities of older persons. Psychology and Aging, 17, 179–193.CrossRefGoogle ScholarPubMed
Wong, E. C. (2005). Quantifying CBF with pulsed ASL: Technical and pulse sequence factors. Journal of Magnetic Resonance Imaging, 22, 727–731.CrossRefGoogle ScholarPubMed
Yesavage, J. A., Brink, T. L., Rose, T. L., Lum, O., Huang, V., Adey, M. B., Leirer, V. O. (1983). Development and validation of a geriatric depression screening scale: A preliminary report. Journal of Psychiatric Research, 17, 37–49.CrossRefGoogle Scholar