A theoretical framework for estimating cerebral oxygen metabolism changes using the calibrated-BOLD method: Modeling the effects of blood volume distribution, hematocrit, oxygen extraction fraction, and tissue signal properties on the BOLD signal

NeuroImage

Volumn 58, Issue 1, 2011, Pages 198-212

  Griffeth, Valerie E M ^a   Buxton, Richard B ^b  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Blood oxygenation level dependent; Cerebral blood flow; Cerebral metabolic rate of oxygen; Functional MRI; Mathematical modeling

Indexed keywords

DEOXYHEMOGLOBIN;

ACCURACY; ARTICLE; BLOOD OXYGENATION; BLOOD VOLUME; BOLD SIGNAL; BRAIN OXYGEN CONSUMPTION; CALIBRATION; CONCEPTUAL FRAMEWORK; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HEMATOCRIT; MATHEMATICAL MODEL; OXYGEN EXTRACTION FRACTION; PRIORITY JOURNAL; PROCESS OPTIMIZATION; SIGNAL DETECTION; TISSUE OXYGENATION;

ALGORITHMS; BLOOD VOLUME; CALIBRATION; CEREBROVASCULAR CIRCULATION; COMPUTER SIMULATION; HEMATOCRIT; HEMOGLOBINS; HUMANS; HYPERCAPNIA; KINETICS; MAGNETIC RESONANCE IMAGING; MODELS, NEUROLOGICAL; MODELS, STATISTICAL; OXYGEN; OXYGEN CONSUMPTION; SIGNAL PROCESSING, COMPUTER-ASSISTED;

EID: 79960641101     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2011.05.077     Document Type: Article

References (66)

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. Blockley N.P., Francis S.T., Gowland P.A. Perturbation of the BOLD response by a contrast agent and interpretation through a modified balloon model. NeuroImage 2009, 48:84-93.
3. Bolar D.S., Rosen B.R., Evans K.C., Sorensen A.G., Adalsteinsson E. Depression of cortical gray matter CMRO2 in awake humans during hypercapnia. Proceedings of the ISMRM, Stockholm 2010, 516.
4. Boxerman J.L., Hamberg L.M., Rosen B.R., Weisskoff R.M. MR contrast due to intravascular magnetic susceptibility perturbations. Magn. Reson. Med. 1995, 34:555-566.
5. Buxton R.B. Modeling the effects of changes in arterial blood volume on the BOLD signal. Proceedings of the ISMRM, Honolulu 2009.
6. Buxton R.B. Interpreting oxygenation-based neuroimaging signals: the importance and the challenge of understanding brain oxygen metabolism. Front Neuroenergetics 2010, 2:8.
7. Buxton R.B., Wong E.C., Frank L.R. Dynamics of blood flow and oxygenation changes during brain activation: the balloon model. Magn. Reson. Med. 1998, 39:855-864.
8. Buxton R.B., Uludag K., Dubowitz D.J., Liu T.T. Modeling the hemodynamic response to brain activation. NeuroImage 2004, 23(Suppl 1):S220-S233.
9. Chen J.J., Pike G.B. BOLD-specific cerebral blood volume and blood flow changes during neuronal activation in humans. NMR Biomed. 2009, 22:1054-1062.
10. Chen J.J., Pike G.B. Human whole blood T2 relaxometry at 3Tesla. Magn. Reson. Med. 2009, 61:249-254.
11. Chen J.J., Pike G.B. MRI measurement of the BOLD-specific flow-volume relationship during hypercapnia and hypocapnia in humans. NeuroImage 2010, 53:383-391.
12. Chiarelli P.A., Bulte D.P., Gallichan D., Piechnik S.K., Wise R., Jezzard P. Flow-metabolism coupling in human visual, motor, and supplementary motor areas assessed by magnetic resonance imaging. Magn. Reson. Med. 2007, 57:538-547.
13. 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.
14. Chugh B.P., Lerch J.P., Yu L.X., Pienkowski M., Harrison R.V., Henkelman R.M., Sled J.G. Measurement of cerebral blood volume in mouse brain regions using micro-computed tomography. NeuroImage 2009, 47:1312-1318.
15. Cox R.W. AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Comput. Biomed. Res. 1996, 29:162-173.
16. 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.
17. Donahue M.J., Blicher J.U., Ostergaard L., Feinberg D.A., MacIntosh B.J., Miller K.L., Gunther M., Jezzard P. Cerebral blood flow, blood volume, and oxygen metabolism dynamics in human visual and motor cortex as measured by whole-brain multi-modal magnetic resonance imaging. J. Cereb. Blood Flow Metab. 2009, 29:1856-1866.
18. Fox P.T., Raichle M.E. Focal physiological uncoupling of cerebral blood flow and oxidative metabolism during somatosensory stimulation in human subjects. Proc. Natl. Acad. Sci. U. S. A. 1986, 83:1140-1144.
19. Friston K.J., Mechelli A., Turner R., Price C.J. Nonlinear responses in fMRI: the Balloon model, Volterra kernels, and other hemodynamics. NeuroImage 2000, 12:466-477.
20. Griffeth V.E.M., Perthen J.E., Buxton R.B. Prospects for quantitative fMRI: investigating the effects of caffeine on baseline oxygen metabolism and the response to a visual stimulus in humans. Neuroimage 2011, (Electronic publication ahead of print).
21. Grubb R.L., Raichle M.E., Eichling J.O., Ter-Pogossian M.M. The effects of changes in PaCO2 on cerebral blood volume, blood flow, and vascular mean transit time. Stroke 1974, 5:630-639.
22. Guckel F.J., Brix G., Hennerici M., Lucht R., Ueltzhoffer C., Neff W. Regional cerebral blood flow and blood volume in patients with subcortical arteriosclerotic encephalopathy (SAE). Eur. Radiol. 2007, 17:2483-2490.
23. Gustard S., Williams E.J., Hall L.D., Pickard J.D., Carpenter T.A. Influence of baseline hematocrit on between-subject BOLD signal change using gradient echo and asymmetric spin echo EPI. Magn. Reson. Imaging 2003, 21:599-607.
24. He X., Yablonskiy D.A. Quantitative BOLD: mapping of human cerebral deoxygenated blood volume and oxygen extraction fraction: default state. Magn. Reson. Med. 2007, 57:115-126.
25. Hillman E.M., Devor A., Bouchard M.B., Dunn A.K., Krauss G.W., Skoch J., Bacskai B.J., Dale A.M., Boas D.A. Depth-resolved optical imaging and microscopy of vascular compartment dynamics during somatosensory stimulation. NeuroImage 2007, 35:89-104.
26. 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.
27. Hyder F., Sanganahalli B.G., Herman P., Coman D., Maandag N.J., Behar K.L., Blumenfeld H., Rothman D.L. Neurovascular and neurometabolic couplings in dynamic calibrated fMRI: transient oxidative neuroenergetics for block-design and event-related paradigms. Front Neuroenergetics 2010, 2.
28. 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.
29. 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.
30. Kim T., Kim S.G. Quantification of cerebral arterial blood volume using arterial spin labeling with intravoxel incoherent motion-sensitive gradients. Magn. Reson. Med. 2006, 55:1047-1057.
31. Kim T., Kim S.G. Cortical layer-dependent arterial blood volume changes: improved spatial specificity relative to BOLD fMRI. NeuroImage 2010, 49:1340-1349.
32. Kim T., Kim S.G. Temporal dynamics and spatial specificity of arterial and venous blood volume changes during visual stimulation: implication for BOLD quantification. J. Cereb. Blood Flow Metab. 2010, 31(5):1211-1222.
33. Kim S.G., Rostrup E., Larsson H.B.W., Ogawa S., Paulson O.B. Determination of relative CMRO2 from CBF and BOLD changes: significant increase of oxygen consumption rate during visual stimulation. Magn. Reson. Med. 1999, 41:1152-1161.
34. Kim T., Hendrich K.S., Masamoto K., Kim S.G. Arterial versus total blood volume changes during neural activity-induced cerebral blood flow change: implication for BOLD fMRI. J. Cereb. Blood Flow Metab. 2007, 27:1235-1247.
35. Kliefoth A.B., Grubb R.L., Raichle M.E. Depression of cerebral oxygen utilization by hypercapnia in the rhesus monkey. J. Neurochem. 1979, 32:661-663.
36. Leontiev O., Buxton R.B. Reproducibility of BOLD, perfusion, and CMRO(2) measurements with calibrated-BOLD fMRI. NeuroImage 2007, 35:175-184.
37. Lin A.L., Fox P.T., Yang Y., Lu H., Tan L.H., Gao J.H. Evaluation of MRI models in the measurement of CMRO2 and its relationship with CBF. Magn. Reson. Med. 2008, 60:380-389.
38. Lin A.L., Fox P.T., Hardies J., Duong T.Q., Gao J.H. Nonlinear coupling between cerebral blood flow, oxygen consumption, and ATP production in human visual cortex. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:8446-8451.
39. Lu H., Ge Y. Quantitative evaluation of oxygenation in venous vessels using T2-relaxation-under-spin-tagging MRI. Magn. Reson. Med. 2008, 60:357-363.
40. Lu H., Golay X., Pekar J.J., Van Zijl P.C. Sustained poststimulus elevation in cerebral oxygen utilization after vascular recovery. J. Cereb. Blood Flow Metab. 2004, 24:764-770.
41. Mandeville J.B., Marota J.J.A., Ayata C., Zaharchuk G., Moskowitz M.A., Rosen B.R., Weisskoff R.M. Evidence of a cerebrovascular post-arteriole Windkessel with delayed compliance. J. Cereb. Blood Flow Metabol. 1999, 19:679-689.
42. Marchal G., Rioux P., Petit-Taboue M.-C., Sette G., Travere J.-M., LePoec 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.
43. Mark C.I., Fisher J.A., Pike G.B. Improved fMRI calibration: precisely controlled hyperoxic versus hypercapnic stimuli. NeuroImage 2011, 54:1102-1111.
44. Obata T., Liu T.T., Miller K.L., Luh W.M., Wong E.C., Frank L.R., Buxton R.B. Discrepancies between BOLD and flow dynamics in primary and supplementary motor areas: application of the balloon model to the interpretation of BOLD transients. NeuroImage 2004, 21:144-153.
45. Ogawa S., Menon R.S., Tank D.W., Kim S.-G., Merkle H., Ellerman J.M., Ugurbil K. Functional brain mapping by blood oxygenation level - dependent contrast magnetic resonance imaging: a comparison of signal characteristics with a biophysical model. Biophys. J. 1993, 64:803-812.
46. Perthen J.E., Lansing A.E., Liau J., Liu T.T., Buxton R.B. Caffeine-induced uncoupling of cerebral blood flow and oxygen metabolism: a calibrated BOLD fMRI study. NeuroImage 2008, 40:237-247.
47. Qin Q., Grgac K., van Zijl P.C. Determination of whole-brain oxygen extraction fractions by fast measurement of blood T(2) in the jugular vein. Magn. Reson. Med. 2011, 65:471-479.
48. Roland P.E., Eriksson L., Stone-Elander S., Widen L. Does mental activity change the oxidative metabolism of the brain?. J. Neurochem. 1987, 7:2373-2389.
49. Rostrup E., Knudsen G.M., Law I., Holm S., Larsson H.B., Paulson O.B. The relationship between cerebral blood flow and volume in humans. NeuroImage 2005, 24:1-11.
50. Sakai F., Nakazawa K., Tazaki Y., Ishii K., Hino H., Igarashi H., Kanda T. Regional cerebral blood volume and hematocrit measured in normal human volunteers by single-photon emission computed tomography. J. Cereb. Blood Flow Metab. 1985, 5:207-213.
51. Sakai F., Igarashi H., Suzuki S., Tazaki Y. Cerebral blood flow and cerebral hematocrit in patients with cerebral ischemia measured by single-photon emission computed tomography. Acta Neurol. Scand. Suppl. 1989, 127:9-13.
52. Schutz S.L. Oxygen saturation monitoring by pulse oximetry. AACN procedure manual for critical care 2001, Elsevier Saunders, St. Louis, Mo. 4th ed. D.J. Lynn-McHale, K.K. Carlson (Eds.).
53. Sicard K.M., Duong T.Q. Effects of hypoxia, hyperoxia, and hypercapnia on baseline and stimulus-evoked BOLD, CBF, and CMRO2 in spontaneously breathing animals. NeuroImage 2005, 25:850-858.
54. Silvennoinen M.J., Clingman C.S., Golay X., Kauppinen R.A., van Zijl P.C. Comparison of the dependence of blood R2 and R2* on oxygen saturation at 1.5 and 4.7Tesla. Magn. Reson. Med. 2003, 49:47-60.
55. Spees W.M., Yablonskiy D.A., Oswood M.C., Ackerman J.J. Water proton MR properties of human blood at 1.5Tesla: magnetic susceptibility, T(1), T(2), T*(2), and non-Lorentzian signal behavior. Magn. Reson. Med. 2001, 45:533-542.
56. Stefanovic B., Warnking J.M., Pike G.B. Hemodynamic and metabolic responses to neuronal inhibition. NeuroImage 2004, 22:771-778.
57. 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.
58. Stefanovic B., Hutchinson E., Yakovleva V., Schram V., Russell J.T., Belluscio L., Koretsky A.P., Silva A.C. Functional reactivity of cerebral capillaries. J. Cereb. Blood Flow Metab. 2008, 28:961-972.
59. Stephan K.E., Weiskopf N., Drysdale P.M., Robinson P.A., Friston K.J. Comparing hemodynamic models with DCM. NeuroImage 2007, 38:387-401.
60. Tsai A.G., Johnson P.C., Intaglietta M. Oxygen gradients in the microcirculation. Physiol. Rev. 2003, 83:933-963.
61. Uludag K., Muller-Bierl B., Ugurbil K. An integrative model for neuronal activity-induced signal changes for gradient and spin echo functional imaging. NeuroImage 2009, 48:150-165.
62. Weber B., Keller A.L., Reichold J., Logothetis N.K. The microvascular system of the striate and extrastriate visual cortex of the macaque. Cereb. Cortex 2008, 18:2318-2330.
63. 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.
64. Zappe A.C., Uludag K., Logothetis N.K. Direct measurement of oxygen extraction with fMRI using 6% CO2 inhalation. Magn. Reson. Imaging 2008, 26:961-967.
65. Zhao J.M., Clingman C.S., Narvainen M.J., Kauppinen R.A., van Zijl P.C. Oxygenation and hematocrit dependence of transverse relaxation rates of blood at 3T. Magn. Reson. Med. 2007, 58:592-597.
66. Zheng Y., Pan Y., Harris S., Billings S., Coca D., Berwick J., Jones M., Kennerley A., Johnston D., Martin C., Devonshire I.M., Mayhew J. A dynamic model of neurovascular coupling: implications for blood vessel dilation and constriction. Neuroimage 2010, 52(3):1135-1147.