Age dependence of hemodynamic response characteristics in human functional magnetic resonance imaging

Neurobiology of Aging

Volumn 34, Issue 5, 2013, Pages 1469-1485

  Gauthier, Claudine J ^a,b   Madjar, Cécile ^b   Desjardins Crépeau, Laurence ^b,c   Bellec, Pierre ^a,b   Bherer, Louis ^b,c   Hoge, Richard D ^a,b  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

^b CRIUGM   (Canada)

^c UNIVERSITÉ DU QUÉBEC À MONTRÉAL   (Canada)

Author keywords

BOLD signal biases; Calibrated fMRI; Cerebral blood flow; Cognitive aging; Hypercapnia; Modified Stroop task; Oxidative metabolism; Vascular reactivity

Indexed keywords

ADULT; AEROBIC METABOLISM; AGE; AGE DISTRIBUTION; AMPLITUDE MODULATION; ARTICLE; BLOOD VESSEL REACTIVITY; BOLD SIGNAL; BRAIN BLOOD FLOW; BRAIN BLOOD VESSEL; BRAIN METABOLISM; BRAIN REGION; CONTROLLED STUDY; EVOKED CORTICAL RESPONSE; FEMALE; FRONTAL CORTEX; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUNCTIONAL NEUROIMAGING; GRAY MATTER; HEMODYNAMIC MONITORING; HUMAN; HUMAN EXPERIMENT; LEFT HEMISPHERE; MALE; MENTAL PERFORMANCE; NORMAL HUMAN; PARIETAL CORTEX; PRIORITY JOURNAL; REACTION TIME; RIGHT HEMISPHERE; SPIN LABELING;

ADULT; AGING; BLOOD FLOW VELOCITY; BRAIN; CEREBROVASCULAR CIRCULATION; COGNITION; FEMALE; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; OXYGEN CONSUMPTION;

EID: 84873426002     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2012.11.002     Document Type: Article

References (99)

1. Ances B.M., Liang C.L., Leontiev O., Perthen J.E., Fleisher A.S., Lansing A.E., Buxton R.B. Effects of aging on cerebral blood flow, oxygen metabolism, and blood oxygenation level dependent responses to visual stimulation. Hum. Brain Mapp. 2009, 30:1120-1132.
2. Baltes P.B., Lindenberger U. Emergence of a powerful connection between sensory and cognitive functions across the adult life span: a new window to the study of cognitive aging?. Psychol. Aging 1997, 12:12-21.
3. Banzett R.B., Lansing R.W., Evans K.C., Shea S.A. Stimulus-response characteristics of CO2-induced air hunger in normal subjects. Respir. Physiol. 1996, 103:19-31.
4. Beckmann C.F., Jenkinson M., Smith S.M. General multilevel linear modeling for group analysis in FMRI. Neuroimage 2003, 20:1052-1063.
5. Blockley N.P., Griffeth V.E., Buxton R.B. A general analysis of calibrated BOLD methodology for measuring CMRO(2) responses: comparison of a new approach with existing methods. Neuroimage 2012, 60:279-289.
6. Bohnen N., Jolles J., Twijnstra A. Modification of the Stroop Color Word Test improves differentiation between patients with mild head injury and matched controls. Clinical Neuropsychologist 1992, 6:178-184.
7. Brown W.R., Thore C.R. Review: cerebral microvascular pathology in ageing and neurodegeneration. Neuropathol. Appl. Neurobiol. 2011, 37:56-74.
8. Bulte D.P., Kelly M., Germuska M., Xie J., Chappell M.A., Okell T.W., Bright M.G., Jezzard P. Quantitative measurement of cerebral physiology using respiratory-calibrated MRI. Neuroimage 2012, 60:582-591.
9. Buxton R.B. Interpreting oxygenation-based neuroimaging signals: the importance and the challenge of understanding brain oxygen metabolism. Front. Neuroenergetics 2010, 2:8.
10. Cabeza R. Hemispheric asymmetry reduction in older adults: the HAROLD model. Psychol. Aging 2002, 17:85-100.
11. Cabeza R., Nyberg L., Park D.C. Cognitive Neuroscience of Aging: Linking Cognitive and Cerebral Aging 2005, Oxford University Press, Oxford.
12. Campbell A.M., Beaulieu C. Pulsed arterial spin labeling parameter optimization for an elderly population. J. Magn. Reson. Imaging 2006, 23:398-403.
13. Cappell K.A., Gmeindl L., Reuter-Lorenz P.A. Age differences in prefontal recruitment during verbal working memory maintenance depend on memory load. Cortex 2010, 46:462-473.
14. Chen J.J., Pike G.B. Global cerebral oxidative metabolism during hypercapnia and hypocapnia in humans: implications for BOLD fMRI. J. Cereb. Blood Flow Metab. 2010, 30:1094-1099.
15. Chen J.J., Rosas H.D., Salat D.H. Age-associated reductions in cerebral blood flow are independent from regional atrophy. Neuroimage 2011, 55:468-478.
16. Chiarelli P.A., Bulte D.P., Wise R., Gallichan D., Jezzard P. A calibration method for quantitative BOLD fMRI based on hyperoxia. Neuroimage 2007, 37:808-820.
17. Cox R.W., Jesmanowicz A. Real-time 3D image registration for functional MRI. Magn. Reson. Med. 1999, 42:1014-1018.
18. Davis S.W., Dennis N.A., Daselaar S.M., Fleck M.S., Cabeza R. Que PASA? The posterior-anterior shift in aging. Cereb. Cortex 2008, 18:1201-1209.
19. Davis T.L., Kwong K.K., Weisskoff R.M., Rosen B.R. Calibrated functional MRI: mapping the dynamics of oxidative metabolism. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:1834-1839.
20. Delis D.C., Kaplan E., Kramer J.H. Delis-Kaplan Executive Function System (D-KEFS) 2001, The Psychological Corporation, San Antonio, TX.
21. DiGirolamo G.J., Kramer A.F., Barad V., Cepeda N.J., Weissman D.H., Milham M.P., Wszalek T.M., Cohen N.J., Banich M.T., Webb A., Belopolsky A.V., McAuley E. General and task-specific frontal lobe recruitment in older adults during executive processes: a fMRI investigation of task-switching. Neuroreport 2001, 12:2065-2071.
22. Dove A., Pollmann S., Schubert T., Wiggins C.J., von Cramon D.Y. Prefrontal cortex activation in task switching: an event-related fMRI study. Brain Res. Cogn. Brain Res. 2000, 9:103-109.
23. Folstein M.F., Folstein S.E., McHugh P.R. " Mini-mental state" A practical method for grading the cognitive state of patients for the clinician. J. Psychiatr. Res. 1975, 12:189-198.
24. Forbes M.L., Hendrich K.S., Kochanek P.M., Williams D.S., Schiding J.K., Wisniewski S.R., Kelsey S.F., DeKosky S.T., Graham S.H., Marion D.W., Ho C. Assessment of cerebral blood flow and CO2 reactivity after controlled cortical impact by perfusion magnetic resonance imaging using arterial spin-labeling in rats. J. Cereb. Blood Flow Metab. 1997, 17:865-874.
25. Gauthier C.J., Desjardins-Crépeau L., Madjar C., Bherer L., Hoge R.D. Absolute quantification of resting oxygen metabolism and metabolic reactivity during functional activation using QUO2 MRI. Neuroimage 2012, 63:1353-1363.
26. Gauthier C.J., Hoge R.D. A generalized procedure for calibrated MRI incorporating hyperoxia and hypercapnia. Hum. Brain Mapp. 2012, 10.1002/hbm.21495.
27. Gauthier C.J., Hoge R.D. Magnetic resonance imaging of resting OEF and CMRO2 using a generalized calibration model for hypercapnia and hyperoxia. Neuroimage 2012, 60:1212-1225.
28. Gauthier C.J., Madjar C., Tancredi F.B., Stefanovic B., Hoge R.D. Elimination of visually evoked BOLD responses during carbogen inhalation: implications for calibrated MRI. Neuroimage 2011, 54:1001-1011.
29. Girouard H., Iadecola C. Neurovascular coupling in the normal brain and in hypertension, stroke, and Alzheimer disease. J. Appl. Physiol. 2006, 100:328-335.
30. Glover G.H. Deconvolution of impulse response in event-related BOLD fMRI. Neuroimage 1999, 9:416-429.
31. Gold B.T., Powell D.K., Xuan L., Jicha G.A., Smith C.D. Age-related slowing of task switching is associated with decreased integrity of frontoparietal white matter. Neurobiol. Aging 2010, 31:512-522.
32. Goode S.D., Krishan S., Alexakis C., Mahajan R., Auer D.P. Precision of cerebrovascular reactivity assessment with use of different quantification methods for hypercapnia functional MR imaging. AJNR Am. J. Neuroradiol. 2009, 30:972-977.
33. Graham G.D., Zhong J., Petroff O.A., Constable R.T., Prichard J.W., Gore J.C. BOLD MRI monitoring of changes in cerebral perfusion induced by acetazolamide and hypercarbia in the rat. Magn. Reson. Med. 1994, 31:557-560.
34. Griswold M.A., Jakob P.M., Heidemann R.M., Nittka M., Jellus V., Wang J., Kiefer B., Haase A. Generalized autocalibrating partially parallel acquisitions (GRAPPA). Magn. Reson. Med. 2002, 47:1202-1210.
35. Hattori N., Bergsneider M., Wu H.M., Glenn T.C., Vespa P.M., Hovda D.A., Phelps M.E., Huang S.C. Accuracy of a method using short inhalation of (15)O-O(2) for measuring cerebral oxygen extraction fraction with PET in healthy humans. J. Nucl. Med. 2004, 45:765-770.
36. Hino J.K., Short B.L., Rais-Bahrami K., Seale W.R. Cerebral blood flow and metabolism during and after prolonged hypercapnia in newborn lambs. Crit. Care Med. 2000, 28:3505-3510.
37. Hoge R.D., Atkinson J., Gill B., Crelier G.R., Marrett S., Pike G.B. Investigation of BOLD signal dependence on cerebral blood flow and oxygen consumption: the deoxyhemoglobin dilution model. Magn. Reson. Med. 1999, 42:849-863.
38. Hoge R.D., Atkinson J., Gill B., Crelier G.R., Marrett S., Pike G.B. Linear coupling between cerebral blood flow and oxygen consumption in activated human cortex. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:9403-9408.
39. Horvath I., Sandor N.T., Ruttner Z., McLaughlin A.C. Role of nitric oxide in regulating cerebrocortical oxygen consumption and blood flow during hypercapnia. J. Cereb. Blood Flow Metab. 1994, 14:503-509.
40. Ibaraki M., Miura S., Shimosegawa E., Sugawara S., Mizuta T., Ishikawa A., Amano M. Quantification of cerebral blood flow and oxygen metabolism with 3-dimensional PET and 15O: validation by comparison with 2-dimensional PET. J. Nucl. Med. 2008, 49:50-59.
41. Ibaraki M., Shinohara Y., Nakamura K., Miura S., Kinoshita F., Kinoshita T. Interindividual variations of cerebral blood flow, oxygen delivery, and metabolism in relation to hemoglobin concentration measured by positron emission tomography in humans. J. Cereb. Blood Flow Metab. 2010, 30:1296-1305.
42. Ishii K., Sasaki M., Kitagaki H., Sakamoto S., Yamaji S., Maeda K. Regional difference in cerebral blood flow and oxidative metabolism in human cortex. J. Nucl. Med. 1996, 37:1086-1088.
43. Ito H., Ibaraki M., Kanno I., Fukuda H., Miura S. Changes in cerebral blood flow and cerebral oxygen metabolism during neural activation measured by positron emission tomography: comparison with blood oxygenation level-dependent contrast measured by functional magnetic resonance imaging. J. Cereb. Blood Flow Metab. 2005, 25:371-377.
44. Ito H., Kanno I., Ibaraki M., Suhara T., Miura S. Relationship between baseline cerebral blood flow and vascular responses to changes in PaCO2 measured by positron emission tomography in humans: implication of inter-individual variations of cerebral vascular tone. Acta Physiol. (Oxf.) 2008, 193:325-330.
45. Jenkinson M., Bannister P., Brady M., Smith S. Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage 2002, 17:825-841.
46. Jenkinson M., Smith S. A global optimisation method for robust affine registration of brain images. Med. Image Anal. 2001, 5:143-156.
47. Jimura K., Braver T.S. Age-related shifts in brain activity dynamics during task switching. Cereb. Cortex 2010, 20:1420-1431.
48. Jones M., Berwick J., Hewson-Stoate N., Gias C., Mayhew J. The effect of hypercapnia on the neural and hemodynamic responses to somatosensory stimulation. Neuroimage 2005, 27:609-623.
49. Kruger G., Glover G.H. Physiological noise in oxygenation-sensitive magnetic resonance imaging. Magn. Reson. Med. 2001, 46:631-637.
50. Langenecker S.A., Nielson K.A., Rao S.M. fMRI of healthy older adults during Stroop interference. Neuroimage 2004, 21:192-200.
51. Lecrux C., Hamel E. The neurovascular unit in brain function and disease. Acta Physiol. (Oxf.) 2011, 203:47-59.
52. Leenders K.L., Perani D., Lammertsma A.A., Heather J.D., Buckingham P., Healy M.J., Gibbs J.M., Wise R.J., Hatazawa J., Herold S., Beaney R.P., Brooks D.J., Spinks S., Rhodes C., Frackowiak R.S.J. Cerebral blood flow, blood volume and oxygen utilization. Normal values and effect of age. Brain 1990, 113:27-47.
53. Leung H.C., Skudlarski P., Gatenby J.C., Peterson B.S., Gore J.C. An event-related functional MRI study of the stroop color word interference task. Cereb. Cortex 2000, 10:552-560.
54. Li S.C., Sikstrom S. Integrative neurocomputational perspectives on cognitive aging, neuromodulation, and representation. Neurosci. Biobehav. Rev. 2002, 26:795-808.
55. Liu T.T., Wong E.C. A signal processing model for arterial spin labeling functional MRI. Neuroimage 2005, 24:207-215.
56. Logothetis N.K., Pauls J., Augath M., Trinath T., Oeltermann A. Neurophysiological investigation of the basis of the fMRI signal. Nature 2001, 412:150-157.
57. Lu H., Xu F., Rodrigue K.M., Kennedy K.M., Cheng Y., Flicker B., Hebrank A.C., Uh J., Park D.C. Alterations in cerebral metabolic rate and blood supply across the adult lifespan. Cereb. Cortex 2011, 21:1426-1434.
58. MacDonald A.W., Cohen J.D., Stenger V.A., Carter C.S. Dissociating the role of the dorsolateral prefrontal and anterior cingulate cortex in cognitive control. Science 2000, 288:1835-1838.
59. Magri C., Schridde U., Murayama Y., Panzeri S., Logothetis N.K. The amplitude and timing of the BOLD signal reflects the relationship between local field potential power at different frequencies. J. Neurosci. 2012, 32:1395-1407.
60. Mandell D.M., Han J.S., Poublanc J., Crawley A.P., Stainsby J.A., Fisher J.A., Mikulis D.J. Mapping cerebrovascular reactivity using blood oxygen level-dependent MRI in patients with arterial steno-occlusive disease: comparison with arterial spin labeling MRI. Stroke 2008, 39:2021-2028.
61. Marchal G., Rioux P., Petit-Taboue M.C., Sette G., Travere J.M., Le Poec C., Courtheoux P., Derlon J.M., Baron J.C. Regional cerebral oxygen consumption, blood flow, and blood volume in healthy human aging. Arch. Neurol. 1992, 49:1013-1020.
62. Mark C.I., Slessarev M., Ito S., Han J., Fisher J.A., Pike G.B. Precise control of end-tidal carbon dioxide and oxygen improves BOLD and ASL cerebrovascular reactivity measures. Magn. Reson. Med. 2010, 64:749-756.
63. McPherson R.W., Derrer S.A., Traystman R.J. Changes in cerebral CO2 responsivity over time during isoflurane anesthesia in the dog. J. Neurosurg. Anesthesiol 1991, 3:12-19.
64. Milham M.P., Erickson K.I., Banich M.T., Kramer A.F., Webb A., Wszalek T., Cohen N.J. Attentional control in the aging brain: insights from an fMRI study of the stroop task. Brain Cogn. 2002, 49:277-296.
65. Mintun M.A., Vlassenko A.G., Shulman G.L., Snyder A.Z. Time-related increase of oxygen utilization in continuously activated human visual cortex. Neuroimage 2002, 16:531-537.
66. Mohtasib R.S., Lumley G., Goodwin J.A., Emsley H.C., Sluming V., Parkes L.M. Calibrated fMRI during a cognitive Stroop task reveals reduced metabolic response with increasing age. Neuroimage 2012, 59:1143-1151.
67. O'Rourke M.F., Hashimoto J. Mechanical factors in arterial aging: a clinical perspective. J. Am. Coll. Cardiol. 2007, 50:1-13.
68. Park D.C., Reuter-Lorenz P. The adaptive brain: aging and neurocognitive scaffolding. Annu. Rev. Psychol. 2009, 60:173-196.
69. Prakash R.S., Voss M.W., Erickson K.I., Lewis J.M., Chaddock L., Malkowski E., Alves H., Kim J., Szabo A., White S.M., Wojcicki T.R., Klamm E.L., McAuley E., Kramer A.F. Cardiorespiratory fitness and attentional control in the aging brain. Front. Hum. Neurosci. 2011, 4:229.
70. Reitan R.M. Validity of the Trail Making Test as an indicator of organic brain damage. Perceptual and Motor Skills 1958, 8:271-276.
71. Reuter-Lorenz P.A., Cappell K.A. Neurocognitive aging and the compensation hypothesis. Curr. Direct. Psychol. Sci. 2008, 17:177-182.
72. Reuter-Lorenz P.A., Park D.C. Human neuroscience and the aging mind: a new look at old problems. J. Gerontol. B Psychol. Sci. Soc. Sci. 2010, 65:405-415.
73. Salat D.H., Buckner R.L., Snyder A.Z., Greve D.N., Desikan R.S., Busa E., Morris J.C., Dale A.M., Fischl B. Thinning of the cerebral cortex in aging. Cereb. Cortex 2004, 14:721-730.
74. Samanez-Larkin G.R., D'Esposito M. Group comparisons: imaging the aging brain. Soc. Cogn. Affect. Neurosci. 2008, 3:290-297.
75. Schneider-Garces N.J., Gordon B.A., Brumback-Peltz C.R., Shin E., Lee Y., Sutton B.P., Maclin E.L., Gratton G., Fabiani M. Span, CRUNCH, and beyond: working memory capacity and the aging brain. J. Cogn. Neurosci. 2010, 22:655-669.
76. Shmuel A., Yacoub E., Pfeuffer J., Van de Moortele P.F., Adriany G., Hu X., Ugurbil K. Sustained negative BOLD, blood flow and oxygen consumption response and its coupling to the positive response in the human brain. Neuron 2002, 36:1195-1210.
77. Slessarev M., Han J., Mardimae A., Prisman E., Preiss D., Volgyesi G., Ansel C., Duffin J., Fisher J.A. Prospective targeting and control of end-tidal CO2 and O2 concentrations. J. Physiol. 2007, 581:1207-1219.
78. Smith S.M. Fast robust automated brain extraction. Hum. Brain Mapp. 2002, 17:143-155.
79. Sonntag W.E., Lynch C.D., Cooney P.T., Hutchins P.M. Decreases in cerebral microvasculature with age are associated with the decline in growth hormone and insulin-like growth factor 1. Endocrinology 1997, 138:3515-3520.
80. Stefanovic B., Warnking J.M., Rylander K.M., Pike G.B. The effect of global cerebral vasodilation on focal activation hemodynamics. Neuroimage 2006, 30:726-734.
81. Tancredi F.B., Gauthier C.J., Madjar C., Bolar D.S., Fisher J.A., Wang D.J., Hoge R.D. Comparison of pulsed and pseudocontinuous arterial spin-labeling for measuring CO(2) -induced cerebrovascular reactivity. J. Magn. Reson. Imaging 2012, 36:312-321.
82. Triantafyllou C., Hoge R.D., Krueger G., Wiggins C.J., Potthast A., Wiggins G.C., Wald L.L. Comparison of physiological noise at 1.5 T, 3 T and 7 T and optimization of fMRI acquisition parameters. Neuroimage 2005, 26:243-250.
83. Wahlund L.O., Barkhof F., Fazekas F., Bronge L., Augustin M., Sjogren M., Wallin A., Ader H., Leys D., Pantoni L., Pasquier F., Erkinjuntti T., Scheltens P. A new rating scale for age-related white matter changes applicable to MRI and CT. Stroke 2001, 32:1318-1322.
84. Wang J., Aguirre G.K., Kimberg D.Y., Roc A.C., Li L., Detre J.A. Arterial spin labeling perfusion fMRI with very low task frequency. Magn. Reson. Med. 2003, 49:796-802.
85. Wasylyshyn C., Verhaeghen P., Sliwinski M.J. Aging and task switching: a meta-analysis. Psychol. Aging 2011, 26:15-20.
86. Wechsler D. WAIS-III Administration and Scoring Manual 1997, The Psychological Corporation.
87. Williams D.S., Detre J.A., Leigh J.S., Koretsky A.P. Magnetic resonance imaging of perfusion using spin inversion of arterial water. Proc. Natl. Acad. Sci. U. S. A. 1992, 89:212-216.
88. Woolrich M. Robust group analysis using outlier inference. Neuroimage 2008, 41:286-301.
89. Woolrich M.W., Behrens T.E., Beckmann C.F., Jenkinson M., Smith S.M. Multilevel linear modelling for FMRI group analysis using Bayesian inference. Neuroimage 2004, 21:1732-1747.
90. Woolrich M.W., Ripley B.D., Brady M., Smith S.M. Temporal autocorrelation in univariate linear modeling of FMRI data. Neuroimage 2001, 14:1370-1386.
91. Wu W.C., Fernandez-Seara M., Detre J.A., Wehrli F.W., Wang J. A theoretical and experimental investigation of the tagging efficiency of pseudocontinuous arterial spin labeling. Magn. Reson. Med. 2007, 58:1020-1027.
92. Xu F., Uh J., Brier M.R., Hart J., Yezhuvath U.S., Gu H., Yang Y., Lu H. The influence of carbon dioxide on brain activity and metabolism in conscious humans. J. Cereb. Blood Flow Metab. 2011, 31:58-67.
93. Yamauchi H., Okazawa H., Kishibe Y., Sugimoto K., Takahashi M. Changes in blood flow and oxygen metabolism during visual stimulation in carotid artery disease: effect of baseline perfusion and oxygen metabolism. Stroke 2002, 33:1294-1300.
94. Yamaguchi T., Kanno I., Uemura K., Shishido F., Inugami A., Ogawa T., Murakami M., Suzuki K. Reduction in regional cerebral metabolic rate of oxygen during human aging. Stroke 1986, 17:1220-1228.
95. Yeung N., Nystrom L.E., Aronson J.A., Cohen J.D. Between-task competition and cognitive control in task switching. J. Neurosci. 2006, 26:1429-1438.
96. Yun J.Y., Lee D.Y., Seo E.H., Choo I.H., Park S.Y., Kim S.G., Woo J.I. Neural correlates of stroop performance in Alzheimer's disease: a FDG-PET study. Dement. Geriatr. Cogn. Dis. Extra 2011, 1:190-201.
97. Zappe A.C., Uludag K., Oeltermann A., Ugurbil K., Logothetis N.K. The influence of moderate hypercapnia on neural activity in the anesthetized nonhuman primate. Cereb. Cortex 2008, 18:2666-2673.
98. Zhang Y., Brady M., Smith S. Segmentation of brain MR images through a hidden Markov random field model and the expectation-maximization algorithm. IEEE Trans Med. Imaging 2001, 20:45-57.
99. Zysset S., Schroeter M.L., Neumann J., von Cramon D.Y. Stroop interference, hemodynamic response and aging: an event-related fMRI study. Neurobiol. Aging 2007, 28:937-946.