Hostname: page-component-cd9895bd7-dk4vv Total loading time: 0 Render date: 2024-12-27T10:37:21.379Z Has data issue: false hasContentIssue false

Subjective Cognitive Decline Modifies the Relationship Between Cerebral Blood Flow and Memory Function in Cognitively Normal Older Adults

Published online by Cambridge University Press:  04 October 2017

Chelsea C. Hays
Affiliation:
VA San Diego Healthcare System, San Diego, California SDSU/UC San Diego Joint Doctoral Program in Clinical Psychology, San Diego, California
Zvinka Z. Zlatar
Affiliation:
VA San Diego Healthcare System, San Diego, California Department of Psychiatry, University of California, San Diego, California
Laura Campbell
Affiliation:
VA San Diego Healthcare System, San Diego, California
M.J. Meloy
Affiliation:
VA San Diego Healthcare System, San Diego, California Department of Psychiatry, University of California, San Diego, California
Christina E. Wierenga*
Affiliation:
VA San Diego Healthcare System, San Diego, California Department of Psychiatry, University of California, San Diego, California
*
Correspondence and reprint requests to: Christina E. Wierenga, VA San Diego Healthcare System, 3350 La Jolla Village Dr., MC 151B, San Diego, CA 92161. E-mail: cwierenga@ucsd.edu

Abstract

Objectives: Subjective cognitive decline (SCD), or self-reported cognitive decline despite normal neuropsychological test performance, is a risk factor for objective cognitive decline and Alzheimer’s disease (AD). While brain mechanisms contributing to SCD are not well defined, studies show associations with vascular risk factors and altered cerebral blood flow (CBF), raising the hypothesis that those with SCD might be experiencing vascular dysregulation, or a disruption in the normal relationship between CBF and cognition. We examined whether the association between CBF and verbal memory performance differs between those with SCD (SCD+) and those without SCD (SCD-). Methods: Linear mixed-effects models were used to investigate whether the voxel-wise relationship between arterial spin labeling (ASL) MRI-measured CBF and verbal memory performance was modified by SCD among a group of 70 cognitively normal older adults (35 SCD+, 35 SCD-; mean age=72) matched on age, gender, and symptoms of depression. Results: Results indicated that the SCD- group exhibited positive associations between verbal memory and CBF within the posterior cingulate cortex, middle temporal gyrus, and inferior frontal gyrus, whereas the SCD+ group displayed negative associations between verbal memory and CBF within the posterior cingulate cortex, middle temporal gyrus, hippocampus, fusiform gyrus, and inferior frontal gyrus. Conclusions: Findings suggest that, while higher CBF is supportive of memory function in those without SCD, higher CBF may no longer support memory function in those presenting with SCD, perhaps reflecting neurovascular dysregulation. (JINS, 2018, 24, 213–223)

Type
Research Articles
Copyright
Copyright © The International Neuropsychological Society 2017 

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

Bangen, K.J., Restom, K., Liu, T.T., Wierenga, C.E., Jak, A.J., Salmon, D.P., & Bondi, M.W. (2012). Assessment of Alzheimer’s disease risk with functional magnetic resonance imaging: An arterial spin labeling study. Journal of Alzheimer’s Disease, 31(Suppl 3), S59S74. doi:10.3233/JAD-2012-120292 Google Scholar
Barnes, L.L., Schneider, J.A., Boyle, P.A., Bienias, J.L., & Bennett, D.A. (2006). Memory complaints are related to Alzheimer disease pathology in older persons. Neurology, 67(9), 15811585. doi:10.1212/01.wnl.0000242734.16663.09 CrossRefGoogle ScholarPubMed
Bertsch, K., Hagemann, D., Hermes, M., Walter, C., Khan, R., & Naumann, E. (2009). Resting cerebral blood flow, attention, and aging. Brain Research, 1267, 7788. doi:10.1016/j.brainres.2009.02.053 Google Scholar
Brown, G.G., Zorrilla, L.T.E., Georgy, B., Kindermann, S.S., Wong, E.C., & Buxton, R.B. (2003). BOLD and Perfusion Response to Finger-Thumb Apposition after Acetazolamide Administration: Differential Relationship to Global Perfusion. Journal of Cerebral Blood Flow & Metabolism, 23(7), 829837. doi:10.1097/01.WCB.0000071887.63724.B2 Google Scholar
Chalela, J.A., Alsop, D.C., Gonzalez-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(3), 680687. doi:10.1161/01.STR.31.3.680 Google Scholar
Cherbuin, N., Sargent-Cox, K., Easteal, S., Sachdev, P., & Anstey, K.J. (2015). Hippocampal atrophy is associated with subjective memory decline: The PATH Through Life Study. The American Journal of Geriatric Psychiatry, 23(5), 446455. doi:10.1016/j.jagp.2014.07.009 Google Scholar
Cox, R.W. (1996). AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Computers and Biomedical Research, an International Journal, 29(3), 162173 Google Scholar
Dai, W., Lopez, O.L., Carmichael, O.T., Becker, J.T., Kuller, L.H., & Gach, H.M. (2009). Mild cognitive impairment and Alzheimer disease: Patterns of altered cerebral blood flow at MR imaging. Radiology, 250(3), 856866. doi:10.1148/radiol.2503080751 Google Scholar
Erk, S., Spottke, A., Meisen, A., Wagner, M., Walter, H., & Jessen, F. (2011). Evidence of neuronal compensation during episodic memory in subjective memory impairment. Archives of General Psychiatry, 68(8), 845852. doi:10.1001/archgenpsychiatry.2011.80 Google Scholar
Frederiksen, K.S. (2013). Corpus callosum in aging and dementia. Danish Medical Journal, 60(10), B4721.Google Scholar
Glodzik-Sobanska, L., Reisberg, B., De Santi, S., Babb, J.S., Pirraglia, E., Rich, K.E., & de Leon, M.J. (2007). Subjective memory complaints: Presence, severity and future outcome in normal older subjects. Dementia and Geriatric Cognitive Disorders, 24(3), 177184. doi:10.1159/000105604 Google Scholar
Grasby, P.M., Frith, C.D., Friston, K.J., Bench, C., Frackowiak, R.S.J., & Dolan, R.J. (1993). Functional mapping of brain areas implicated in auditory—verbal memory function. Brain, 116(1), 120. doi:10.1093/brain/116.1.1 Google Scholar
Hays, C.C., Zlatar, Z.Z., & Wierenga, C.E. (2016). The utility of cerebral blood flow as a biomarker of preclinical Alzheimer’s disease. Cellular and Molecular Neurobiology, 36(2), 167179. doi:10.1007/s10571-015-0261-z Google Scholar
Heo, S., Prakash, R.S., Voss, M.W., Erickson, K.I., Ouyang, C., Sutton, B.P., & Kramer, A.F. (2010). Resting hippocampal blood flow, spatial memory and aging. Brain Research, 1315, 119127. doi:10.1016/j.brainres.2009.12.020 CrossRefGoogle ScholarPubMed
Hohman, T.J., Beason-Held, L.L., Lamar, M., & Resnick, S.M. (2011). Subjective cognitive complaints and longitudinal changes in memory and brain function. Neuropsychology, 25(1), 125130. doi:10.1037/a0020859 Google Scholar
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(5), 368375. doi:10.1097/JGP.0b013e31819431d5 Google Scholar
Jessen, F., Amariglio, R.E., van Boxtel, M., Breteler, M., Ceccaldi, M., Chételat, G., & Wagner, M. (2014). A conceptual framework for research on subjective cognitive decline in preclinical Alzheimer’s disease. Alzheimer’s & Dementia, 10(6), 844852. doi:10.1016/j.jalz.2014.01.001 Google Scholar
Johnson, N.A., Jahng, G.-H., Weiner, M.W., Miller, B.L., Chui, H.C., Jagust, W.J., & Schuff, N. (2005). Pattern of cerebral hypoperfusion in Alzheimer disease and mild cognitive impairment measured with arterial spin-labeling MR imaging: initial experience. Radiology, 234(3), 851859. doi:10.1148/radiol.2343040197 Google Scholar
Jonker, C., Geerlings, M.I., & Schmand, B. (2000). Are memory complaints predictive for dementia? A review of clinical and population-based studies. International Journal of Geriatric Psychiatry, 15(11), 983991.Google Scholar
Jung, Y., Wong, E.C., & Liu, T.T. (2010). Multiphase pseudocontinuous arterial spin labeling (MP-PCASL) for robust quantification of cerebral blood flow. Magnetic Resonance in Medicine, 64(3), 799810. doi:10.1002/mrm.22465.Google Scholar
Lista, S., Molinuevo, J.L., Cavedo, E., Rami, L., Amouyel, P., Teipel, S.J., & Hampel, H. (2015). Evolving evidence for the value of neuroimaging methods and biological markers in subjects categorized with subjective cognitive decline. Journal of Alzheimer’s Disease, 48(s1), S171S191. doi:10.3233/JAD-150202 Google Scholar
Liu, T.T., & Wong, E.C. (2005). A signal processing model for arterial spin labeling functional MRI. NeuroImage, 24(1), 207215. doi:10.1016/j.neuroimage.2004.09.047 Google Scholar
Lo, E.H., & Rosenberg, G.A. (2009). The Neurovascular Unit in Health and Disease Introduction. Stroke, 40(3 Suppl 1), S2S3. doi:10.1161/STROKEAHA.108.534404 CrossRefGoogle ScholarPubMed
Loewenthal, K.M. (2001). An introduction to psychological tests and scales. Abingdon, UK: Psychology Press.Google Scholar
Meltzer, C.C., Cantwell, M.N., Greer, P.J., Ben-Eliezer, D., Smith, G., Frank, G., & Price, J.C. (2000). Does cerebral blood flow decline in healthy aging? A PET study with partial-volume correction. Journal of Nuclear Medicine, 41(11), 18421848.Google ScholarPubMed
Mitchell, A.J. (2008). The clinical significance of subjective memory complaints in the diagnosis of mild cognitive impairment and dementia: A meta-analysis. International Journal of Geriatric Psychiatry, 23(11), 11911202. doi:10.1002/gps.2053 Google Scholar
Mitchell, A.J., Beaumont, H., Ferguson, D., Yadegarfar, M., & Stubbs, B. (2014). Risk of dementia and mild cognitive impairment in older people with subjective memory complaints: Meta-analysis. Acta Psychiatrica Scandinavica, 130(6), 439451. doi:10.1111/acps.12336 Google Scholar
Mosconi, L., De Santi, S., Brys, M., Tsui, W.H., Pirraglia, E., Glodzik-Sobanska, L., & de Leon, M.J. (2008). Hypometabolism and altered cerebrospinal fluid markers in normal apolipoprotein E E4 carriers with subjective memory complaints. Biological Psychiatry, 63(6), 609618. doi:10.1016/j.biopsych.2007.05.030 Google Scholar
Okonkwo, O.C., Xu, G., Oh, J.M., Dowling, N.M., Carlsson, C.M., Gallagher, C.L., & Johnson, S.C. (2014). Cerebral blood flow is diminished in asymptomatic middle-aged adults with maternal history of Alzheimer’s disease. Cerebral Cortex, 24(4), 978988. doi:10.1093/cercor/bhs381 Google Scholar
Ostergaard, L., Aamand, R., Gutierrez-Jimenez, E., Ho, Y.C., Blicher, J.U., Madsen, S.M., & West, M.J. (2013). The capillary dysfunction hypothesis of Alzheimer’s disease. Neurobiology of Aging, 34(4), 10181031.CrossRefGoogle ScholarPubMed
Paradise, M.B., Glozier, N.S., Naismith, S.L., Davenport, T.A., & Hickie, I.B. (2011). Subjective memory complaints, vascular risk factors and psychological distress in the middle-aged: A cross-sectional study. BMC Psychiatry, 11, 108. doi:10.1186/1471-244X-11-108 Google Scholar
Parkes, L.M., Rashid, W., Chard, D.T., & Tofts, P.S. (2004). Normal cerebral perfusion measurements using arterial spin labeling: reproducibility, stability, and age and gender effects. Magnetic Resonance in Medicine: Official Journal of the Society of Magnetic Resonance in Medicine / Society of Magnetic Resonance in Medicine, 51(4), 736743. doi:10.1002/mrm.20023 Google Scholar
Pearce, N. (2016). Analysis of matched case-control studies. BMJ, 352, i969. doi:10.1136/bmj.i969 Google Scholar
Rabin, L.A., Smart, C.M., Crane, P.K., Amariglio, R.E., Berman, L.M., Boada, M., & Sikkes, S.A.M. (2015). Subjective cognitive decline in older adults: An overview of self-report measures used across 19 international research studies. Journal of Alzheimer’s Disease, 48(0 1), S63S86. doi:10.3233/JAD-150154 Google Scholar
Reisberg, B., & Gauthier, S. (2008). Current evidence for subjective cognitive impairment (SCI) as the pre-mild cognitive impairment (MCI) stage of subsequently manifest Alzheimer’s disease. International Psychogeriatrics / IPA, 20(1), 116. doi:10.1017/S1041610207006412 CrossRefGoogle ScholarPubMed
Reisberg, B., Shulman, M.B., Torossian, C., Leng, L., & Zhu, W. (2010). Outcome over seven years of healthy adults with and without subjective cognitive impairment. Alzheimer’s & Dementia, 6(1), 1124. doi:10.1016/j.jalz.2009.10.002 Google Scholar
Roy, C.S., & Sherrington, C.S. (1890). On the regulation of the blood-supply of the brain. The Journal of Physiology, 11(1–2), 85108, 158.7–158.17.Google Scholar
Salthouse, T.A. (2011). Neuroanatomical substrates of age-related cognitive decline. Psychological Bulletin, 137(5), 753784. doi:10.1037/a0023262 Google Scholar
Scheef, L., Spottke, A., Daerr, M., Joe, A., Striepens, N., Kolsch, H., & Jessen, F. (2012). Glucose metabolism, gray matter structure, and memory decline in subjective memory impairment. Neurology, 79(13), 13321339. doi:10.1212/WNL.0b013e31826c1a8d Google Scholar
Schmand, B., Jonker, C., Geerlings, M.I., & Lindeboom, J. (1997). Subjective memory complaints in the elderly: Depressive symptoms and future dementia. The British Journal of Psychiatry, 171(4), 373376. doi:10.1192/bjp.171.4.373 Google Scholar
Stewart, R., Godin, O., Crivello, F., Maillard, P., Mazoyer, B., Tzourio, C., & Dufouil, C. (2011). Longitudinal neuroimaging correlates of subjective memory impairment: 4-year prospective community study. The British Journal of Psychiatry, 198(3), 199205. doi:10.1192/bjp.bp.110.078683 Google Scholar
Stuart, E.A. (2010). Matching methods for causal inference: A review and a look forward. Statistical Science, 25(1), 121. doi:10.1214/09-STS313 Google Scholar
Sun, Y., Yang, F.-C., Lin, C.-P., & Han, Y. (2015). Biochemical and neuroimaging studies in subjective cognitive decline: Progress and perspectives. CNS Neuroscience & Therapeutics, 21(10), 768775. doi:10.1111/cns.12395 Google Scholar
Sun, Z. (2015). Aging, arterial stiffness, and hypertension. Hypertension, 65(2), 252256. doi:10.1161/HYPERTENSIONAHA.114.03617 Google Scholar
Verfaillie, S.C.J., Adriaanse, S.M., Binnewijzend, M.A.A., Benedictus, M.R., Ossenkoppele, R., Wattjes, M.P., & Barkhof, F. (2015). Cerebral perfusion and glucose metabolism in Alzheimer’s disease and frontotemporal dementia: Two sides of the same coin? European Radiology, 25(10), 30503059. 10.1007/s00330-015-3696-1 Google Scholar
Wang, L., van Belle, G., Crane, P.K., Kukull, W.A., Bowen, J.D., McCormick, W.C., & Larson, E.B. (2004). Subjective memory deterioration and future dementia in people aged 65 and older. Journal of the American Geriatrics Society, 52(12), 20452051. doi:10.1111/j.1532-5415.2004.52568.x Google Scholar
Wang, Y., West, J., Risacher, S., McDonald, B., Tallman, E., Ghetti, B., & Saykin, A. (2013). Characterization of regional cerebral blood flow in mild cognitive impairment and older adults with cognitive complaints. Alzheimer’s & Dementia, 9(4), P71. doi:10.1016/j.jalz.2013.05.114 Google Scholar
Wang, Z. (2014). Characterizing early Alzheimer’s disease and disease progression using hippocampal volume and arterial spin labeling perfusion MRI. Journal of Alzheimer’s Disease, 42(Suppl 4), S495S502. doi:10.3233/JAD-141419 Google Scholar
Wierenga, C.E., Dev, S.I., Shin, D.D., Clark, L.R., Bangen, K.J., Jak, A.J., & Bondi, M.W. (2012). Effect of mild cognitive impairment and APOE genotype on resting cerebral blood flow and its association with cognition. Journal of Cerebral Blood Flow & Metabolism, 32(8), 15891599. doi:10.1038/jcbfm.2012.58 CrossRefGoogle ScholarPubMed
Wierenga, C.E., Hays, C.C., & Zlatar, Z.Z. (2014). Cerebral blood flow measured by arterial spin labeling MRI as a preclinical marker of Alzheimer’s disease. Journal of Alzheimer’s Disease, 42(Suppl 4), S411S419. doi:10.3233/JAD-141467 Google Scholar
Zhang, J.H., Badaut, J., Tang, J., Obenaus, A., Hartman, R., & Pearce, W.J. (2012). The vascular neural network—a new paradigm in stroke pathophysiology. Nature Reviews Neurology, 8(12), 711716. doi:10.1038/nrneurol.2012.210 Google Scholar
Zlatar, Z.Z., Bischoff-Grethe, A., Hays, C.C., Liu, T.T., Meloy, M.J., Rissman, R.A., & Wierenga, C.E. (2016). Higher brain perfusion may not support memory functions in cognitively normal carriers of the ApoE ε4 allele compared to non-carriers. Frontiers in Aging Neuroscience, 151. doi:10.3389/fnagi.2016.00151 Google Scholar
Zlokovic, B.V. (2010). Neurodegeneration and the neurovascular unit. Nature Medicine, 16(12), 13701371. doi:10.1038/nm1210-1370 Google Scholar