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Published in: Brain Structure and Function 6/2020

01-07-2020 | Vascular Dementia | Original Article

Hemodynamic latency is associated with reduced intelligence across the lifespan: an fMRI DCM study of aging, cerebrovascular integrity, and cognitive ability

Authors: Ariana E. Anderson, Mirella Diaz-Santos, Spencer Frei, Bianca H. Dang, Pashmeen Kaur, Patrick Lyden, Richard Buxton, Pamela K. Douglas, Robert M. Bilder, Mahtash Esfandiari, Karl J. Friston, Usha Nookala, Susan Y. Bookheimer

Published in: Brain Structure and Function | Issue 6/2020

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Abstract

Changes in neurovascular coupling are associated with both Alzheimer’s disease and vascular dementia in later life, but this may be confounded by cerebrovascular risk. We hypothesized that hemodynamic latency would be associated with reduced cognitive functioning across the lifespan, holding constant demographic and cerebrovascular risk. In 387 adults aged 18–85 (mean = 48.82), dynamic causal modeling was used to estimate the hemodynamic response function in the left and right V1 and V3-ventral regions of the visual cortex in response to a simple checkerboard block design stimulus with minimal cognitive demands. The hemodynamic latency (transit time) in the visual cortex was used to predict general cognitive ability (Full-Scale IQ), controlling for demographic variables (age, race, education, socioeconomic status) and cerebrovascular risk factors (hypertension, alcohol use, smoking, high cholesterol, BMI, type 2 diabetes, cardiac disorders). Increased hemodynamic latency in the visual cortex predicted reduced cognitive function (p < 0.05), holding constant demographic and cerebrovascular risk. Increased alcohol use was associated with reduced overall cognitive function (Full Scale IQ 2.8 pts, p < 0.05), while cardiac disorders (Full Scale IQ 3.3 IQ pts; p < 0.05), high cholesterol (Full Scale IQ 3.9 pts; p < 0.05), and years of education (2 IQ pts/year; p < 0.001) were associated with higher general cognitive ability. Increased hemodynamic latency was associated with reduced executive functioning (p < 0.05) as well as reductions in verbal concept formation (p < 0.05) and the ability to synthesize and analyze abstract visual information (p < 0.01). Hemodynamic latency is associated with reduced cognitive ability across the lifespan, independently of other demographic and cerebrovascular risk factors. Vascular health may predict cognitive ability long before the onset of dementias.
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Literature
go back to reference Ances BM, Liang CL, Leontiev O, Perthen JE, Fleisher AS, Lansing AE, Buxton RB (2009) Effects of aging on cerebral blood flow, oxygen metabolism, and blood oxygenation level dependent responses to visual stimulation. Hum Brain Mapp 30(4):1120–1132PubMedCrossRef Ances BM, Liang CL, Leontiev O, Perthen JE, Fleisher AS, Lansing AE, Buxton RB (2009) Effects of aging on cerebral blood flow, oxygen metabolism, and blood oxygenation level dependent responses to visual stimulation. Hum Brain Mapp 30(4):1120–1132PubMedCrossRef
go back to reference Anstey KJ, Lipnicki DM, Low L-F (2008) Cholesterol as a risk factor for dementia and cognitive decline: a systematic review of prospective studies with meta-analysis. Am J Geriatr Psychiatry 16(5):343–354CrossRefPubMed Anstey KJ, Lipnicki DM, Low L-F (2008) Cholesterol as a risk factor for dementia and cognitive decline: a systematic review of prospective studies with meta-analysis. Am J Geriatr Psychiatry 16(5):343–354CrossRefPubMed
go back to reference Anttila T, Helkala E-L, Viitanen M, Kåreholt I, Fratiglioni L, Winblad B, Soininen H, Tuomilehto J, Nissinen A, Kivipelto M (2004) Alcohol drinking in middle age and subsequent risk of mild cognitive impairment and dementia in old age: a prospective population based study. BMJ 329(7465):539PubMedPubMedCentralCrossRef Anttila T, Helkala E-L, Viitanen M, Kåreholt I, Fratiglioni L, Winblad B, Soininen H, Tuomilehto J, Nissinen A, Kivipelto M (2004) Alcohol drinking in middle age and subsequent risk of mild cognitive impairment and dementia in old age: a prospective population based study. BMJ 329(7465):539PubMedPubMedCentralCrossRef
go back to reference Bahrani AA, Powell DK, Yu G, Johnson ES, Jicha GA, Smith CD (2017) White matter hyperintensity associations with cerebral blood flow in elderly subjects stratified by cerebrovascular risk. J Stroke Cerebrov Dis 26(4):779–786CrossRef Bahrani AA, Powell DK, Yu G, Johnson ES, Jicha GA, Smith CD (2017) White matter hyperintensity associations with cerebral blood flow in elderly subjects stratified by cerebrovascular risk. J Stroke Cerebrov Dis 26(4):779–786CrossRef
go back to reference Birkenhäger WH, Forette F, Seux M-L, Wang J-G, Staessen JA (2001) Blood pressure, cognitive functions, and prevention of dementias in older patients with hypertension. Arch Intern Med 161(2):152–156PubMedCrossRef Birkenhäger WH, Forette F, Seux M-L, Wang J-G, Staessen JA (2001) Blood pressure, cognitive functions, and prevention of dementias in older patients with hypertension. Arch Intern Med 161(2):152–156PubMedCrossRef
go back to reference Braak H, Alafuzoff I, Arzberger T, Kretzschmar H, Del Tredici K (2006) Staging of Alzheimer disease-associated neurofibrillary pathology using paraffin sections and immunocytochemistry. Acta Neuropathol 112(4):389–404PubMedPubMedCentralCrossRef Braak H, Alafuzoff I, Arzberger T, Kretzschmar H, Del Tredici K (2006) Staging of Alzheimer disease-associated neurofibrillary pathology using paraffin sections and immunocytochemistry. Acta Neuropathol 112(4):389–404PubMedPubMedCentralCrossRef
go back to reference Breteler MM (2000) Vascular risk factors for Alzheimer’s disease: an epidemiologic perspective. Neurobiol Aging 21(2):153–160PubMedCrossRef Breteler MM (2000) Vascular risk factors for Alzheimer’s disease: an epidemiologic perspective. Neurobiol Aging 21(2):153–160PubMedCrossRef
go back to reference Buckner RL, Snyder AZ, Sanders AL, Raichle ME, Morris JC (2000) Functional brain imaging of young, nondemented, and demented older adults. J Cognit Neurosci 12(Supplement 2):24–34CrossRef Buckner RL, Snyder AZ, Sanders AL, Raichle ME, Morris JC (2000) Functional brain imaging of young, nondemented, and demented older adults. J Cognit Neurosci 12(Supplement 2):24–34CrossRef
go back to reference Buxton RB, Wong EC, Frank LR (1998) Dynamics of blood flow and oxygenation changes during brain activation: the balloon model. Magn Reson Med 39(6):855–864PubMedCrossRef Buxton RB, Wong EC, Frank LR (1998) Dynamics of blood flow and oxygenation changes during brain activation: the balloon model. Magn Reson Med 39(6):855–864PubMedCrossRef
go back to reference Buxton RB, Uludağ K, Dubowitz DJ, Liu TT (2004) Modeling the hemodynamic response to brain activation. Neuroimage 23:S220–S233CrossRefPubMed Buxton RB, Uludağ K, Dubowitz DJ, Liu TT (2004) Modeling the hemodynamic response to brain activation. Neuroimage 23:S220–S233CrossRefPubMed
go back to reference Chang C-CH, Zhao Y, Lee C-W, Ganguli M (2012) Smoking, death, and Alzheimer’s disease: a case of competing risks. Alzheimer Dis Assoc Disord 26(4):300PubMedPubMedCentralCrossRef Chang C-CH, Zhao Y, Lee C-W, Ganguli M (2012) Smoking, death, and Alzheimer’s disease: a case of competing risks. Alzheimer Dis Assoc Disord 26(4):300PubMedPubMedCentralCrossRef
go back to reference Claus JJ, Breteler M, Hasan D, Krenning E, Bots M, Grobbee D, Van Swieten J, Van Harskamp F, Hofman A (1998) Regional cerebral blood flow and cerebrovascular risk factors in the elderly population. Neurobiol Aging 19(1):57–64PubMedCrossRef Claus JJ, Breteler M, Hasan D, Krenning E, Bots M, Grobbee D, Van Swieten J, Van Harskamp F, Hofman A (1998) Regional cerebral blood flow and cerebrovascular risk factors in the elderly population. Neurobiol Aging 19(1):57–64PubMedCrossRef
go back to reference de la Torre JC (2012) Cerebral hemodynamics and vascular risk factors: setting the stage for Alzheimer's disease. Journal of Alzheimer's Disease 32(3):553–567PubMedCrossRef de la Torre JC (2012) Cerebral hemodynamics and vascular risk factors: setting the stage for Alzheimer's disease. Journal of Alzheimer's Disease 32(3):553–567PubMedCrossRef
go back to reference Dolan H, Crain B, Troncoso J, Resnick SM, Zonderman AB, Obrien RJ (2010) Atherosclerosis, dementia, and Alzheimer disease in the Baltimore Longitudinal Study of Aging cohort. Ann Neurol 68(2):231–240PubMedPubMedCentral Dolan H, Crain B, Troncoso J, Resnick SM, Zonderman AB, Obrien RJ (2010) Atherosclerosis, dementia, and Alzheimer disease in the Baltimore Longitudinal Study of Aging cohort. Ann Neurol 68(2):231–240PubMedPubMedCentral
go back to reference Dumoulin SO, Wandell BA (2008) Population receptive field estimates in human visual cortex. Neuroimage 39(2):647–660PubMedCrossRef Dumoulin SO, Wandell BA (2008) Population receptive field estimates in human visual cortex. Neuroimage 39(2):647–660PubMedCrossRef
go back to reference Elias MF, Wolf PA, D'Agostino RB, Cobb J, White LR (1993) Untreated blood pressure level is inversely related to cognitive functioning: the Framingham Study. Am J Epidemiol 138(6):353–364PubMedCrossRef Elias MF, Wolf PA, D'Agostino RB, Cobb J, White LR (1993) Untreated blood pressure level is inversely related to cognitive functioning: the Framingham Study. Am J Epidemiol 138(6):353–364PubMedCrossRef
go back to reference Evans R, Emsley C, Gao S, Sahota A, Hall K, Farlow M, Hendrie H (2000) Serum cholesterol, APOE genotype, and the risk of Alzheimer’s disease: a population-based study of African Americans. Neurology 54(1):240–240PubMedCrossRef Evans R, Emsley C, Gao S, Sahota A, Hall K, Farlow M, Hendrie H (2000) Serum cholesterol, APOE genotype, and the risk of Alzheimer’s disease: a population-based study of African Americans. Neurology 54(1):240–240PubMedCrossRef
go back to reference Evans R, Hui S, Perkins A, Lahiri D, Poirier J, Farlow M (2004) Cholesterol and APOE genotype interact to influence Alzheimer disease progression. Neurology 62(10):1869–1871PubMedCrossRef Evans R, Hui S, Perkins A, Lahiri D, Poirier J, Farlow M (2004) Cholesterol and APOE genotype interact to influence Alzheimer disease progression. Neurology 62(10):1869–1871PubMedCrossRef
go back to reference Friston KJ, Mechelli A, Turner R, Price CJ (2000) Nonlinear responses in fMRI: the Balloon model, Volterra kernels, and other hemodynamics. NeuroImage 12(4):466–477PubMedCrossRef Friston KJ, Mechelli A, Turner R, Price CJ (2000) Nonlinear responses in fMRI: the Balloon model, Volterra kernels, and other hemodynamics. NeuroImage 12(4):466–477PubMedCrossRef
go back to reference Girouard H, Iadecola C (2006) Neurovascular coupling in the normal brain and in hypertension, stroke, and Alzheimer disease. J Appl Physiol 100(1):328–335PubMedCrossRef Girouard H, Iadecola C (2006) Neurovascular coupling in the normal brain and in hypertension, stroke, and Alzheimer disease. J Appl Physiol 100(1):328–335PubMedCrossRef
go back to reference Gröschel K, Terborg C, Schnaudigel S, Ringer T, Riecker A, Witte O, Kastrup A (2007) Effects of physiological aging and cerebrovascular risk factors on the hemodynamic response to brain activation: a functional transcranial Doppler study. Eur J Neurol 14(2):125–131PubMedCrossRef Gröschel K, Terborg C, Schnaudigel S, Ringer T, Riecker A, Witte O, Kastrup A (2007) Effects of physiological aging and cerebrovascular risk factors on the hemodynamic response to brain activation: a functional transcranial Doppler study. Eur J Neurol 14(2):125–131PubMedCrossRef
go back to reference Hamzei F, Knab R, Weiller C, Röther J (2003) The influence of extra-and intracranial artery disease on the BOLD signal in FMRI. Neuroimage 20(2):1393–1399PubMedCrossRef Hamzei F, Knab R, Weiller C, Röther J (2003) The influence of extra-and intracranial artery disease on the BOLD signal in FMRI. Neuroimage 20(2):1393–1399PubMedCrossRef
go back to reference Heatherton TF, Kozlowski LT, Frecker RC, Fagerström K-O (1991) The Fagerström test for nicotine dependence: a revision of the Fagerstrom Tolerance Questionnaire. Br J Addict 86(9):1119–1127CrossRefPubMed Heatherton TF, Kozlowski LT, Frecker RC, Fagerström K-O (1991) The Fagerström test for nicotine dependence: a revision of the Fagerstrom Tolerance Questionnaire. Br J Addict 86(9):1119–1127CrossRefPubMed
go back to reference Heinzle J, Koopmans PJ, den Ouden HE, Raman S, Stephan KE (2016) A hemodynamic model for layered BOLD signals. Neuroimage 125:556–570PubMedCrossRef Heinzle J, Koopmans PJ, den Ouden HE, Raman S, Stephan KE (2016) A hemodynamic model for layered BOLD signals. Neuroimage 125:556–570PubMedCrossRef
go back to reference Hirao K, Ohnishi T, Hirata Y, Yamashita F, Mori T, Moriguchi Y, Matsuda H, Nemoto K, Imabayashi E, Yamada M (2005) The prediction of rapid conversion to Alzheimer's disease in mild cognitive impairment using regional cerebral blood flow SPECT. Neuroimage 28(4):1014–1021PubMedCrossRef Hirao K, Ohnishi T, Hirata Y, Yamashita F, Mori T, Moriguchi Y, Matsuda H, Nemoto K, Imabayashi E, Yamada M (2005) The prediction of rapid conversion to Alzheimer's disease in mild cognitive impairment using regional cerebral blood flow SPECT. Neuroimage 28(4):1014–1021PubMedCrossRef
go back to reference Jafarian A, Litvak V, Cagnan H, Friston KJ, Zeidman P (2019) Neurovascular coupling: insights from multi-modal dynamic causal modelling of fMRI and MEG. arXiv:1903.07478 Jafarian A, Litvak V, Cagnan H, Friston KJ, Zeidman P (2019) Neurovascular coupling: insights from multi-modal dynamic causal modelling of fMRI and MEG. arXiv:​1903.​07478
go back to reference Jarvik GP, Wijsman EM, Kukull WA, Schellenberg G, Yu C, Larson EB (1995) Interactions of apolipoprotein E genotype, total cholesterol level, age, and sex in prediction of Alzheimer's disease. A case-control study. Neurology 45(6):1092–1096PubMedCrossRef Jarvik GP, Wijsman EM, Kukull WA, Schellenberg G, Yu C, Larson EB (1995) Interactions of apolipoprotein E genotype, total cholesterol level, age, and sex in prediction of Alzheimer's disease. A case-control study. Neurology 45(6):1092–1096PubMedCrossRef
go back to reference Johnston SC, Hauser SL (2010) The challenge of publishing newsworthy epidemiology. Ann Neurol 68(2):A8–A10PubMedCrossRef Johnston SC, Hauser SL (2010) The challenge of publishing newsworthy epidemiology. Ann Neurol 68(2):A8–A10PubMedCrossRef
go back to reference Lang PJ, Bradley MM, Fitzsimmons JR, Cuthbert BN, Scott JD, Moulder B, Nangia V (1998) Emotional arousal and activation of the visual cortex: an fMRI analysis. Psychophysiology 35(2):199–210PubMedCrossRef Lang PJ, Bradley MM, Fitzsimmons JR, Cuthbert BN, Scott JD, Moulder B, Nangia V (1998) Emotional arousal and activation of the visual cortex: an fMRI analysis. Psychophysiology 35(2):199–210PubMedCrossRef
go back to reference Launer LJ, Masaki K, Petrovitch H, Foley D, Havlik RJ (1995) The association between midlife blood pressure levels and late-life cognitive function: the Honolulu-Asia Aging Study. JAMA 274(23):1846–1851PubMedCrossRef Launer LJ, Masaki K, Petrovitch H, Foley D, Havlik RJ (1995) The association between midlife blood pressure levels and late-life cognitive function: the Honolulu-Asia Aging Study. JAMA 274(23):1846–1851PubMedCrossRef
go back to reference Leuba G, Kraftsik R (1994) Changes in volume, surface estimate, three-dimensional shape and total number of neurons of the human primary visual cortex from midgestation until old age. Anat Embryol 190(4):351–366CrossRef Leuba G, Kraftsik R (1994) Changes in volume, surface estimate, three-dimensional shape and total number of neurons of the human primary visual cortex from midgestation until old age. Anat Embryol 190(4):351–366CrossRef
go back to reference Mentis MJ, Horwitz B, Grady CL, Alexander GE, VanMeter JW, Maisog JM, Pietrini P, Schapiro MB, Rapoport SI (1996) Visual cortical dysfunction in Alzheimer's disease evaluated with a temporally graded" stress test" during PET. Am J Psychiatry. 153:23–40 Mentis MJ, Horwitz B, Grady CL, Alexander GE, VanMeter JW, Maisog JM, Pietrini P, Schapiro MB, Rapoport SI (1996) Visual cortical dysfunction in Alzheimer's disease evaluated with a temporally graded" stress test" during PET. Am J Psychiatry. 153:23–40
go back to reference Muldoon MF, Ryan CM, Matthews KA, Manuck SB (1997) Serum cholesterol and intellectual performance. Psychosom Med 59(4):382–387PubMedCrossRef Muldoon MF, Ryan CM, Matthews KA, Manuck SB (1997) Serum cholesterol and intellectual performance. Psychosom Med 59(4):382–387PubMedCrossRef
go back to reference Nobili F, Rodriguez G, Marenco S, De Carli F, Gambaro M, Castello C, Pontremoli R, Rosadini G (1993) Regional cerebral blood flow in chronic hypertension. A correlative study. Stroke 24(8):1148–1153PubMedCrossRef Nobili F, Rodriguez G, Marenco S, De Carli F, Gambaro M, Castello C, Pontremoli R, Rosadini G (1993) Regional cerebral blood flow in chronic hypertension. A correlative study. Stroke 24(8):1148–1153PubMedCrossRef
go back to reference Notkola I-L, Sulkava R, Pekkanen J, Erkinjuntti T, Ehnholm C, Kivinen P, Tuomilehto J, Nissinen A (1998) Serum total cholesterol, apolipoprotein E FC12 e4 allele, and Alzheimer’s disease. Neuroepidemiology 17(1):14–20PubMedCrossRef Notkola I-L, Sulkava R, Pekkanen J, Erkinjuntti T, Ehnholm C, Kivinen P, Tuomilehto J, Nissinen A (1998) Serum total cholesterol, apolipoprotein E FC12 e4 allele, and Alzheimer’s disease. Neuroepidemiology 17(1):14–20PubMedCrossRef
go back to reference Novak V (2012) Cognition and hemodynamics. Curr Cardiov Risk Rep 6(5):380–396CrossRef Novak V (2012) Cognition and hemodynamics. Curr Cardiov Risk Rep 6(5):380–396CrossRef
go back to reference Østergaard L, Aamand R, Gutiérrez-Jiménez E, Ho Y-CL, Blicher JU, Madsen SM, Nagenthiraja K, Dalby RB, Drasbek KR, Møller A (2013) The capillary dysfunction hypothesis of Alzheimer's disease. Neurobiol Aging 34(4):1018–1031PubMedCrossRef Østergaard L, Aamand R, Gutiérrez-Jiménez E, Ho Y-CL, Blicher JU, Madsen SM, Nagenthiraja K, Dalby RB, Drasbek KR, Møller A (2013) The capillary dysfunction hypothesis of Alzheimer's disease. Neurobiol Aging 34(4):1018–1031PubMedCrossRef
go back to reference Penny WD, Friston KJ, Ashburner JT, Kiebel SJ, Nichols TE (2011) Statistical parametric mapping: the analysis of functional brain images. Elsevier, Amsterdam Penny WD, Friston KJ, Ashburner JT, Kiebel SJ, Nichols TE (2011) Statistical parametric mapping: the analysis of functional brain images. Elsevier, Amsterdam
go back to reference Pineiro R, Pendlebury S, Johansen-Berg H, Matthews P (2002) Altered hemodynamic responses in patients after subcortical stroke measured by functional MRI. Stroke 33(1):103–109PubMedCrossRef Pineiro R, Pendlebury S, Johansen-Berg H, Matthews P (2002) Altered hemodynamic responses in patients after subcortical stroke measured by functional MRI. Stroke 33(1):103–109PubMedCrossRef
go back to reference Riecker A, Grodd W, Klose U, Schulz JB, Gröschel K, Erb M, Ackermann H, Kastrup A (2003) Relation between regional functional MRI activation and vascular reactivity to carbon dioxide during normal aging. J Cereb Blood Flow Metab 23(5):565–573PubMedCrossRef Riecker A, Grodd W, Klose U, Schulz JB, Gröschel K, Erb M, Ackermann H, Kastrup A (2003) Relation between regional functional MRI activation and vascular reactivity to carbon dioxide during normal aging. J Cereb Blood Flow Metab 23(5):565–573PubMedCrossRef
go back to reference Rigoux L, Stephan KE, Friston KJ, Daunizeau J (2014) Bayesian model selection for group studies—revisited. Neuroimage 84:971–985PubMedCrossRef Rigoux L, Stephan KE, Friston KJ, Daunizeau J (2014) Bayesian model selection for group studies—revisited. Neuroimage 84:971–985PubMedCrossRef
go back to reference Robbins MA, Elias MF, Elias PK, Budge MM (2005) Blood pressure and cognitive function in an African-American and a Caucasian-American sample: the Maine-Syracuse Study. Psychosom Med 67(5):707–714PubMedCrossRef Robbins MA, Elias MF, Elias PK, Budge MM (2005) Blood pressure and cognitive function in an African-American and a Caucasian-American sample: the Maine-Syracuse Study. Psychosom Med 67(5):707–714PubMedCrossRef
go back to reference Rytsar R, Fornari E, Frackowiak RS, Ghika JA, Knyazeva MG (2011) Inhibition in early Alzheimer's disease: an fMRI-based study of effective connectivity. Neuroimage 57(3):1131–1139PubMedCrossRef Rytsar R, Fornari E, Frackowiak RS, Ghika JA, Knyazeva MG (2011) Inhibition in early Alzheimer's disease: an fMRI-based study of effective connectivity. Neuroimage 57(3):1131–1139PubMedCrossRef
go back to reference Schmidt M (1996) Rey auditory verbal learning test: a handbook. Western Psychological Services, Los Angeles Schmidt M (1996) Rey auditory verbal learning test: a handbook. Western Psychological Services, Los Angeles
go back to reference Smith AT, Greenlee MW, Singh KD, Kraemer FM, Hennig J (1998) The processing of first-and second-order motion in human visual cortex assessed by functional magnetic resonance imaging (fMRI). J Neurosci 18(10):3816–3830PubMedPubMedCentralCrossRef Smith AT, Greenlee MW, Singh KD, Kraemer FM, Hennig J (1998) The processing of first-and second-order motion in human visual cortex assessed by functional magnetic resonance imaging (fMRI). J Neurosci 18(10):3816–3830PubMedPubMedCentralCrossRef
go back to reference Solomon A, Kivipelto M, Wolozin B, Zhou J, Whitmer RA (2009) Midlife serum cholesterol and increased risk of Alzheimer’s and vascular dementia three decades later. Dement Geriatr Cogn Disord 28(1):75–80PubMedPubMedCentralCrossRef Solomon A, Kivipelto M, Wolozin B, Zhou J, Whitmer RA (2009) Midlife serum cholesterol and increased risk of Alzheimer’s and vascular dementia three decades later. Dement Geriatr Cogn Disord 28(1):75–80PubMedPubMedCentralCrossRef
go back to reference Sotero RC, Trujillo-Barreto NJ, Jiménez JC, Carbonell F, Rodríguez-Rojas R (2009) Identification and comparison of stochastic metabolic/hemodynamic models (sMHM) for the generation of the BOLD signal. J Comput Neurosci 26(2):251–269PubMedCrossRef Sotero RC, Trujillo-Barreto NJ, Jiménez JC, Carbonell F, Rodríguez-Rojas R (2009) Identification and comparison of stochastic metabolic/hemodynamic models (sMHM) for the generation of the BOLD signal. J Comput Neurosci 26(2):251–269PubMedCrossRef
go back to reference Stano JF (2004) Wechsler abbreviated scale of intelligence. Rehab Counsel Bull 48(1):56CrossRef Stano JF (2004) Wechsler abbreviated scale of intelligence. Rehab Counsel Bull 48(1):56CrossRef
go back to reference Stephan KE, Penny WD, Daunizeau J, Moran RJ, Friston KJ (2009) Bayesian model selection for group studies. Neuroimage 46(4):1004–1017PubMedCrossRef Stephan KE, Penny WD, Daunizeau J, Moran RJ, Friston KJ (2009) Bayesian model selection for group studies. Neuroimage 46(4):1004–1017PubMedCrossRef
go back to reference Sue Baron I (2004) Delis-Kaplan executive function system. Child Neuropsychol 10(2):147–152CrossRef Sue Baron I (2004) Delis-Kaplan executive function system. Child Neuropsychol 10(2):147–152CrossRef
go back to reference Trammell JP, MacRae PG, Davis G, Bergstedt D, Anderson AE (2017) The relationship of cognitive performance and the theta-alpha power ratio is age-dependent: an EEG study of short term memory and reasoning during task and resting-state in healthy young and old adults. Front Aging Neurosci 9:364PubMedPubMedCentralCrossRef Trammell JP, MacRae PG, Davis G, Bergstedt D, Anderson AE (2017) The relationship of cognitive performance and the theta-alpha power ratio is age-dependent: an EEG study of short term memory and reasoning during task and resting-state in healthy young and old adults. Front Aging Neurosci 9:364PubMedPubMedCentralCrossRef
go back to reference Wan X, Riera J, Iwata K, Takahashi M, Wakabayashi T, Kawashima R (2006) The neural basis of the hemodynamic response nonlinearity in human primary visual cortex: Implications for neurovascular coupling mechanism. Neuroimage 32(2):616–625PubMedCrossRef Wan X, Riera J, Iwata K, Takahashi M, Wakabayashi T, Kawashima R (2006) The neural basis of the hemodynamic response nonlinearity in human primary visual cortex: Implications for neurovascular coupling mechanism. Neuroimage 32(2):616–625PubMedCrossRef
go back to reference West KL, Zuppichini MD, Turner MP, Sivakolundu DK, Zhao Y, Abdelkarim D, Spence JS, Rypma B (2019) BOLD hemodynamic response function changes significantly with healthy aging. NeuroImage 188:198–207PubMedCrossRef West KL, Zuppichini MD, Turner MP, Sivakolundu DK, Zhao Y, Abdelkarim D, Spence JS, Rypma B (2019) BOLD hemodynamic response function changes significantly with healthy aging. NeuroImage 188:198–207PubMedCrossRef
go back to reference Wierenga CE, Dev SI, Shin DD, Clark LR, Bangen KJ, Jak AJ, Rissman RA, Liu TT, Salmon DP, Bondi MW (2012) Effect of mild cognitive impairment and APOE genotype on resting cerebral blood flow and its association with cognition. J Cereb Blood Flow Metab 32(8):1589–1599PubMedPubMedCentralCrossRef Wierenga CE, Dev SI, Shin DD, Clark LR, Bangen KJ, Jak AJ, Rissman RA, Liu TT, Salmon DP, Bondi MW (2012) Effect of mild cognitive impairment and APOE genotype on resting cerebral blood flow and its association with cognition. J Cereb Blood Flow Metab 32(8):1589–1599PubMedPubMedCentralCrossRef
go back to reference Wierenga CE, Hays CC, Zlatar ZZ (2014) Cerebral blood flow measured by arterial spin labeling MRI as a preclinical marker of Alzheimer's disease. J Alzheimer's Dis 42(s4):S411–S419CrossRef Wierenga CE, Hays CC, Zlatar ZZ (2014) Cerebral blood flow measured by arterial spin labeling MRI as a preclinical marker of Alzheimer's disease. J Alzheimer's Dis 42(s4):S411–S419CrossRef
go back to reference Wu L-T, McNeely J, Subramaniam GA, Sharma G, VanVeldhuisen P, Schwartz RP (2016) Design of the NIDA clinical trials network validation study of tobacco, alcohol, prescription medications, and substance use/misuse (TAPS) tool. Contemp Clin Trials 50:90–97PubMedPubMedCentralCrossRef Wu L-T, McNeely J, Subramaniam GA, Sharma G, VanVeldhuisen P, Schwartz RP (2016) Design of the NIDA clinical trials network validation study of tobacco, alcohol, prescription medications, and substance use/misuse (TAPS) tool. Contemp Clin Trials 50:90–97PubMedPubMedCentralCrossRef
go back to reference Zhou J, Yu J-T, Wang H-F, Meng X-F, Tan C-C, Wang J, Wang C, Tan L (2015) Association between stroke and Alzheimer's disease: systematic review and meta-analysis. J Alzheimer Dis 43(2):479–489CrossRef Zhou J, Yu J-T, Wang H-F, Meng X-F, Tan C-C, Wang J, Wang C, Tan L (2015) Association between stroke and Alzheimer's disease: systematic review and meta-analysis. J Alzheimer Dis 43(2):479–489CrossRef
Metadata
Title
Hemodynamic latency is associated with reduced intelligence across the lifespan: an fMRI DCM study of aging, cerebrovascular integrity, and cognitive ability
Authors
Ariana E. Anderson
Mirella Diaz-Santos
Spencer Frei
Bianca H. Dang
Pashmeen Kaur
Patrick Lyden
Richard Buxton
Pamela K. Douglas
Robert M. Bilder
Mahtash Esfandiari
Karl J. Friston
Usha Nookala
Susan Y. Bookheimer
Publication date
01-07-2020
Publisher
Springer Berlin Heidelberg
Published in
Brain Structure and Function / Issue 6/2020
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-020-02083-w

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