Hostname: page-component-586b7cd67f-2plfb Total loading time: 0 Render date: 2024-11-25T19:29:11.289Z Has data issue: false hasContentIssue false
  • English
  • Français

Functional Magnetic Resonance Imaging of Working Memory Reveals Frontal Hypoactivation in Middle-Aged Adults with Cognitive Complaints

Published online by Cambridge University Press:  31 August 2011

Andreana P. Haley ,
Danielle E. Eagan ,
Mitzi M. Gonzales ,
Fedora O. Biney  and
Rachel A. Cooper
Andreana P. Haley*
Affiliation:
Department of Psychology, The University of Texas at Austin, Austin, Texas University of Texas Imaging Research Center, Austin, Texas
Danielle E. Eagan
Affiliation:
Department of Psychology, The University of Texas at Austin, Austin, Texas
Mitzi M. Gonzales
Affiliation:
Department of Psychology, The University of Texas at Austin, Austin, Texas
Fedora O. Biney
Affiliation:
Department of Psychology, The University of Texas at Austin, Austin, Texas
Rachel A. Cooper
Affiliation:
Department of Psychology, The University of Texas at Austin, Austin, Texas
*
Correspondence and reprint requests to: Andreana P. Haley, Department of Psychology, The University of Texas at Austin, 1 University Station, A8000, Austin, TX 78712. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Older adults with cardiovascular disease (CVD) often complain about cognitive difficulties including reduced processing speed and attention. On cross-sectional examination, such reports relate more closely to mood than to cognitive performance; yet, in longitudinal studies, these complaints have foreshadowed cognitive decline over time. To test the hypothesis that self-reported cognitive difficulties reflect early changes in brain function, we examined cognitive complaints and depression in relation to blood oxygen level dependent (BOLD) response to a cognitive task in middle-aged adults at risk for CVD. Forty-nine adults (ages 40 to 60 years) completed a measure of perceived cognitive dysfunction (Cognitive Difficulties Scale), medical history questionnaire, neuropsychological assessment and functional magnetic resonance imaging (fMRI) during a working memory task. Increased report of cognitive difficulties was significantly associated with weaker task-related activation in the right superior frontal/ middle frontal gyrus (F(4,44) = 3.26; p = .020, CDS ß = −0.39; p = .009) and the right inferior frontal gyrus (F(4,44) = 3.14; p = .024, CDS ß = −0.45; p = .003), independent of age, education, and self-reported depressive symptoms. Lower activation intensity in the right superior frontal gyrus was related to trends toward poorer task performance. Thus, self-reported cognitive difficulties among cognitively normal middle-aged adults may provide important clinical information about early brain vulnerability that should be carefully monitored. (JINS, 2011, 17, 915–924)

Keywords

Subjective cognitive complaintsCognitionCardiovascular diseasesfMRIWorking memoryAging
Type
Regular Articles
Information
Journal of the International Neuropsychological Society , Volume 17 , Issue 5 , September 2011 , pp. 915 - 924
Copyright
Copyright © The International Neuropsychological Society 2011

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

Beck, A.T., Steer, R.A., Brown, G.K. (1996). Manual for the Beck Depression Inventory-II. San Antonio, TX: Psychological Corporation.Google Scholar
Bookheimer, S.Y., Strojwas, M.H., Cohen, M.S., Saunders, A.M., Pericak-Vance, M.A., Mazziotta, J.C., Smal, G.W. (2000). Patterns of brain activation in people at risk for Alzheimer's disease. The New England Journal of Medicine, 343(7), 450–456.CrossRefGoogle ScholarPubMed
Center for Disease Control and Prevention. (2009). Promoting preventive services for adults 50-64: Community and clinical partnerships. Atlanta, GA: National Association of Chronic Disease Directors.Google Scholar
Chang, L., Speck, O., Miller, E.N., Braun, J., Jovicich, J., Koch, C., Ernst, T. (2001). Neural correlates of attention and working memory deficits in HIV patients. Neurology, 57(6), 1001–1007.CrossRefGoogle ScholarPubMed
Cohen, R.A., Poppas, A., Forman, D.E., Hoth, K.F., Haley, A.P., Gunstad, J., Gerhard-Herman, M. (2009). Vascular and cognitive functions associated with cardiovascular disease in the elderly. Journal of Clinical and Experimental Neuropsychology, 31(1), 96–110.CrossRefGoogle ScholarPubMed
Cox, R.W. (1996). AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Computers and Biomedical Research, 29(3), 162–173.Google Scholar
de Groot, J.C., de Leeuw, F.E., Oudkerk, M., Hofman, A., Jolles, J., Breteler, M.M. (2001). Cerebral white matter lesions and subjective cognitive dysfunction: the Rotterdam Scan Study. Neurology, 56(11), 1539–1545.Google Scholar
Delis, D.C., Kramer, J.H., Kaplan, E., Ober, B.A. (2000). California Verbal Learning Test: Second Edition. San Antonio, TX: Psychological Corporation.Google Scholar
Derouesné, C., Lacomblez, L., Thibault, S., LePoncin, M. (1999). Memory complaints in young and elderly subjects. International Journal of Geriatric Psychiatry, 14(4), 291–301.3.0.CO;2-7>CrossRefGoogle Scholar
Dufouil, C., Fuhrer, R., Alpérovitch, A. (2005). Subjective cognitive complaints and cognitive decline: consequence or predictor? The epidemiology of vascular aging study. Journal of the American Geriatrics Society, 53(4), 616–621.CrossRefGoogle ScholarPubMed
Eslinger, P., Damasio, A.R., Benton, A.L. (1984). The Iowa screening battery for mental decline. Iowa City, IA: University of Iowa College of Medicine.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 Psychiatric Research, 12(3), 189–198.CrossRefGoogle ScholarPubMed
Forman, D.E., Cohen, R.A., Hoth, K.F., Haley, A.P., Poppas, A., Moser, D.J., Gerhard-Herman, M. (2008). Vascular health and cognitive function in older adults with cardiovascular disease. Artery Research, 2(1), 35–43.CrossRefGoogle ScholarPubMed
Gaugler, J.E., Yu, F., Krichbaum, K., Wyman, J.F. (2009). Predictors of nursing home admission for persons with dementia. Medical Care, 47(2), 191–198.CrossRefGoogle ScholarPubMed
Glodzik-Sobanska, L., Reisberg, B., De Santi, S., Bab, 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), 177–184.CrossRefGoogle ScholarPubMed
Gonzales, M.M., Tarumi, T., Tanaka, H., Sugawara, J., Swann-Sternberg, T., Goudarzi, K., Haley, A.P. (2010). Functional imaging of working memory and peripheral endothelial function in middle-aged adults. Brain and Cognition, 73(2), 146–151.CrossRefGoogle ScholarPubMed
Gunstad, J., Cohen, R.A., Paul, R.H., Tate, D.F., Hoth, K.F., Poppas, A. (2006). Understanding reported cognitive dysfunction in older adults with cardiovascular disease. Neuropsychiatric Disease and Treatment, 2(2), 213–218.CrossRefGoogle ScholarPubMed
Gunstad, J., Cohen, R.A., Tate, D.F., Paul, R.H., Poppas, A., Hoth, K., Jefferson, A.L. (2005). Blood pressure variability and white matter hyperintensities in older adults with cardiovascular disease. Blood Pressure, 14(6), 353–358.CrossRefGoogle ScholarPubMed
Haley, A.P., Forman, D.E., Poppas, A., Hoth, K.F., Gunstad, J., Jefferson, A.L., Cohen, R.A. (2007). Carotid artery intima-media thickness and cognition in cardiovascular disease. International Journal of Cardiology, 121(2), 148–154.CrossRefGoogle ScholarPubMed
Haley, A.P., Gunstad, J., Cohen, R.A., Jerskey, B.A., Mulligan, R., Sweet, L.H. (2008). Neural correlates of visuospatial working memory in healthy young adults at risk for hypertension. Brain Imaging and Behavior, 2, 192–199.CrossRefGoogle Scholar
Haley, A.P., Hoth, K.F., Gunstad, J., Paul, R.H., Jefferson, A.L., Tate, D.F., Cohen, R.A. (2009). Subjective cognitive complaints relate to white matter hyperintensities and future cognitive decline in patients with cardiovascular disease. The American Journal of Geriatric Psychiatry, 17(11), 976–985.CrossRefGoogle ScholarPubMed
Haley, A.P., Sweet, L.H., Gunstad, J., Forman, D.E., Poppas, A., Paul, R.H., Cohen, R.A. (2007). Verbal working memory and atherosclerosis in patients with cardiovascular disease: an fMRI study. Journal of Neuroimaging, 17(3), 227–233.Google Scholar
Hoth, K.F., Tate, D.F., Poppas, A., Forman, D.E., Gunstad, J., Moser, D.J., Cohen, R.A. (2007). Endothelial function and white matter hyperintensities in older adults with cardiovascular disease. Stroke, 38(2), 308–312.Google Scholar
Humphreys, C.T., Moser, D.J., Hynes, S.M., Reese, R.L., Haynes, W.G. (2007). Predictors of subjective cognitive difficulties in older adults with atherosclerotic vascular disease. American Journal of Geriatric Psychiatry, 15(4), 328–334.CrossRefGoogle ScholarPubMed
Irani, F., Sweet, L.H., Haley, A.P., Gunstad, J., Jerskey, B.A., Mulligan, R.C., Cohen, R.A. (2009). An fMRI study of verbal working memory, cardiac output, and ejection fraction in elderly patients with cardiovascular disease. Brain Imaging and Behavior, 3, 350–357.CrossRefGoogle ScholarPubMed
Jefferson, A.L., Poppas, A., Paul, R.H., Cohen, R.A. (2007). Systemic hypoperfusion is associated with executive dysfunction in geriatric cardiac patients. Neurobiology of Aging, 28(3), 477–483.CrossRefGoogle ScholarPubMed
Jefferson, A.L., Tate, D.F., Poppas, A., Brickman, A.M., Paul, R.H., Gunstad, J., Cohen, R.A. (2007). Lower cardiac output is associated with greater white matter hyperintensities in older adults with cardiovascular disease. Journal of the American Geriatric Society, 55(7), 1044–1048.CrossRefGoogle ScholarPubMed
Jennings, J.R., Muldoon, M.F., Price, J., Christie, I.C., Meltzer, C.C. (2008). Cerebrovascular support for cognitive processing in hypertensive patients is altered by blood pressure treatment. Hypertension, 52(1), 65–71.CrossRefGoogle ScholarPubMed
Jennings, J.R., Muldoon, M.F., Ryan, C., Price, J.C., Greer, P., Sutton-Tyrrel, K., Meltzer, C.C. (2005). Reduced cerebral blood flow response and compensation among patients with untreated hypertension. Neurology, 64(8), 1358–1365.CrossRefGoogle ScholarPubMed
Johnstone, T., Ores Walsh, K.S., Greischar, L.L., Alexander, A.L., Fox, A.S., Davidson, R.J., Oakes, T.R. (2006). Motion correction and the use of motion covariates in multiple-subject fMRI analysis. Human Brain Mapping, 27(10), 779–788.CrossRefGoogle ScholarPubMed
Jorm, A.F., Christensen, H., Korten, A.E., Jacomb, P.A., Henderson, A.S. (2001). Memory complaints as a precursor of memory impairment in older people: a longitudinal analysis over 7–8 years. Psychological Medicine, 31(3), 441–449.Google Scholar
Jungwirth, S., Fischer, P., Weissgram, S., Kirchmeyr, W., Bauer, P., Tragl, K.-H. (2004). Subjective memory complaints and objective memory impairment in the Vienna-Transdanube aging community. Journal of the American Geriatrics Society, 52(2), 263–268.CrossRefGoogle ScholarPubMed
Khatri, P., Babyak, M., Clancy, C., Davis, R., Croughwel, N., Newman, M., Blumenthal, J.A. (1999). Perception of cognitive function in older adults following coronary artery bypass surgery. Health Psychology, 18(3), 301–306.Google Scholar
Kim, J.-M., Stewart, R., Kim, S.-W., Yang, S.-J., Shin, I.-S., Yoon, J.-S. (2006). A prospective study of changes in subjective memory complaints and onset of dementia in South Korea. The American Journal of Geriatric Psychiatry, 14(11), 949–956.CrossRefGoogle ScholarPubMed
Klove, H. (1963). Clinical neuropsychology. In F.M. Forster (Ed.), The medical clinics of North America. New York: Saunders.Google Scholar
Lautenschlager, N.T., Flicker, L., Vasikaran, S., Leedman, P., Almeida, O.P. (2005). Subjective memory complaints with and without objective memory impairment: relationship with risk factors for dementia. American Journal of Geriatric Psychiatry, 13(8), 731–734.Google Scholar
Lezak, M.D. (1995). Neuropsychological assessment. New York, NY: Oxford University Press.Google Scholar
McKhan, G.M., Selnes, O.A., Grega, M.A., Bailey, M.M., Pham, L.D., Baumgartner, W.A., Zeger, S.L. (2009). Subjective memory symptoms in surgical and nonsurgical coronary artery patients: 6-year follow-up. The Annals of Thoracic Surgery, 87(1), 27–35.Google Scholar
McNair, D., Kahn, R.J. (1983). Self-assessment of cognitive deficits. In T. Crook, S. Ferris, R. Bartus (Ed.), Assessment in geriatric psychopharmacology (pp. 137–143). New Canaan, CT: Mark Powley Associates Inc.Google Scholar
Minet, T.S., Da Silva, R.V., Ortiz, K.Z., Bertolucci, P.H. (2008). Subjective memory complaints in an elderly sample: a cross-sectional study. International Journal of Geriatric Psychiatry, 23(1), 49–54.Google Scholar
Minet, T.S., Dean, J.L., Firbank, M., English, P., O'Brien, J.T. (2005). Subjective memory complaints, white-matter lesions, depressive symptoms, and cognition in elderly patients. The American Journal of Geriatric Psychiatry, 13(8), 665–671.CrossRefGoogle 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(9), 1159–1165.Google Scholar
Nakagawa, S. (2004). A farewell to Bonferroni: the problem of low statistical power and publication bias. Behavioral Ecology, 15(6), 1044–1045.Google Scholar
Newman, S., Klinger, L., Ven, G., Smith, P., Harrison, M., Treasure, T. (1989). Subjective reports of cognition in relation to assessed cognitive performance following coronary artery bypass surgery. Journal of Psychosomatic Research, 33(2), 227–233.CrossRefGoogle ScholarPubMed
Oldfield, R.C. (1971). The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia, 9(1), 97–113.Google Scholar
Paul, R.H., Gunstad, J., Poppas, A., Tate, D.F., Foreman, D., Brickman, A.M., Cohen, R.A. (2005). Neuroimaging and cardiac correlates of cognitive function among patients with cardiac disease. Cerebrovascular Diseases, 20(2), 129–133.CrossRefGoogle ScholarPubMed
Ravizza, S.M., Delgado, M.R., Chein, J.M., Becker, J.T., Fiez, J.A. (2004). Functional dissociations within the inferior parietal cortex in verbal working memory. Neuroimage, 22(2), 562–573.Google Scholar
Reitan, R. (1958). Validity of the Trail Making Test as an indicator of organic brain damage. Perceptual Motor Skills, 8, 271–276.CrossRefGoogle Scholar
Sachdev, P., Chen, X., Wen, W. (2008). White matter hyperintensities in mid-adult life. Current Opinions in Psychiatry, 21(3), 268–274.CrossRefGoogle ScholarPubMed
Saykin, A.J., Flashman, L.A., Frutiger, S.A., Johnson, S.C., Mamourian, A.C., Moritz, C.H., Weaver, J.B. (1999). Neuroanatomic substrates of semantic memory impairment in Alzheimer's disease: patterns of functional MRI activation. Journal of the International Neuropsychol Society, 5(5), 377–392.CrossRefGoogle ScholarPubMed
Selnes, O.A., Grega, M.A., Borowicz, L.M., Barry, S., Zeger, S., McKhan, G.M. (2004). Self-reported memory symptoms with coronary artery disease: a prospective study of CABG patients and nonsurgical controls. Cognitive and Behavioral Neurology, 17(3), 148–156.CrossRefGoogle ScholarPubMed
Singhal, A. (2009). The early origins of atherosclerosis. Advances in Experimental Medicine and Biology, 646, 51–58.CrossRefGoogle ScholarPubMed
Stewart, R., Dufouil, C., Godin, O., Ritchie, K., Maillard, P., Delcroix, N., Tzourio, C. (2008). Neuroimaging correlates of subjective memory deficits in a community population. Neurology, 70(18), 1601–1607.CrossRefGoogle Scholar
Sweet, L.H., Rao, S.M., Primeau, M., Durgerian, S., Cohen, R.A. (2006). Functional magnetic resonance imaging response to increased verbal working memory demands among patients with multiple sclerosis. Human Brain Mapping, 27(1), 28–36.CrossRefGoogle ScholarPubMed
Sweet, L.H., Rao, S.M., Primeau, M., Mayer, A.R., Cohen, R.A. (2004). Functional magnetic resonance imaging of working memory among multiple sclerosis patients. Journal of Neuroimaging, 14(2), 150–157.CrossRefGoogle ScholarPubMed
Talairach, J., Tournoux, P. (1988). Co-planar stereotaxic atlas of the human brain 3-D proportional system: An approach to cerebral imaging. New York, NY: Thieme Medical Publishers.Google Scholar
Tobiansky, R., Blizard, R., Livingston, G., Man, A. (1995). The Gospel Oak Study stage IV: the clinical relevance of subjective memory impairment in older people. Psychological Medicine, 25(4), 779–786.Google Scholar
Vingerhoets, G., de Soete, G., Jannes, C. (1995). Subjective complaints versus neuropsychological test performance after cardiopulmonary bypass. Journal of Psychosomatic Research, 39(7), 843–853.Google Scholar
Wechsler, D. (1999). Wechsler abbreviated scale of intelligence manual. San Antonio, TX: Harcourt Assessment Company.Google Scholar
World Health Organization. (2005). Preventing chronic diseases: a vital investment: WHO global report. Geneva, Switzerland: WHO.Google Scholar