Improved fMRI calibration: Precisely controlled hyperoxic versus hypercapnic stimuli

NeuroImage

Volumn 54, Issue 2, 2011, Pages 1102-1111

  Mark, Clarisse I ^a   Fisher, Joseph A ^b   Pike, G Bruce ^a  

^a MCGILL UNIVERSITY   (Canada)

^b UNIVERSITY HEALTH NETWORK   (Canada)

Author keywords

BOLD calibration; Cerebral blood flow; Computer controlled respiratory actuator; FMRI; Hypercapnia; Hyperoxia

Indexed keywords

ADULT; ARTICLE; BLOOD GAS PARAMETERS; BLOOD OXYGEN LEVEL DEPENDENT; BRAIN BLOOD FLOW; BRAIN METABOLISM; CALIBRATION; END TIDAL CARBON DIOXIDE TENSION; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; HYPERCAPNIA; HYPEROXIA; IMAGE ANALYSIS; MALE; OXYGEN CONSUMPTION; OXYGEN TENSION; PRIORITY JOURNAL; SPIN LABELING;

ADOLESCENT; ADULT; BRAIN; CALIBRATION; CARBON DIOXIDE; CEREBROVASCULAR CIRCULATION; FEMALE; HUMANS; HYPERCAPNIA; HYPEROXIA; MAGNETIC RESONANCE IMAGING; MALE; OXYGEN; OXYGEN CONSUMPTION; YOUNG ADULT;

EID: 78649653567     PISSN: 10538119     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2010.08.070     Document Type: Article

References (76)

1. Ances B., Loeontiev O., Perthen J., Liang C., Lansing A., Buxton R. Regional differences in the coupling of cerebral blood flow and oxygen metabolism changes in response to activation: implications for BOLD-fMRI. NeuroImage 2008, 39:1510-1521.
2. Ashkanian M., Borghammer P., Gjedde A., Ostergaard L., Vafaee M. Improvement of brain tissue oxygenation by inhalation of carbogen. Neuroscience 2008, 156:932-938.
3. Berkowitz B. Role of dissolved plasma oxygen in hyperoxia-induced contrast. Magn. Reson. Imaging 1997, 15:123-126.
4. Bezdek J.C., Hall L., Clarke L.P. Review of MR image segmentation techniques using pattern recognition. Med. Phys. 1993, 20:1033-1048.
5. Boxerman J., Bandettini P.A., Kwong K.K., Baker J., Davis T., Rosen B., Weisskoff R.M. The intravascular contribution to fMRI signal change: Monte Carlo modeling and diffusion-weighted studies in vivo. Magn. Reson. Med. 1995, 34:4-10.
6. Bulte D.P., Alfonsi J., Bells S., Noseworthy M. Vasomodulation of BOLD signal in skeletal muscle. J. Magn. Reson. Imaging 2006, 24:886-890.
7. Bulte D.P., Chiarelli P.A., Wise R.G., Jezzard P. Cerebral perfusion response to hyperoxia. J. Cereb. Blood Flow Metab. 2007, 27:69-75.
8. Bulte D.P., Drescher K., Jezzard P. Comparison of hypercapnia-based calibration techniques for measurement of cerebral oxygen metabolism with MRI. Magn. Reson. Med. 2009, 61:391-398.
9. Buxton R.B. Introduction to Functional Magnetic Resonance Imaging: Principles and Techniques 2003, Cambridge University Press, Cambridge.
10. Chen Y., Parrish T. Is ASL-BOLD equivalent to standard BOLD?. OHBM Conf Proc, Chicago, Illinois 2007, 265.
11. 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.
12. Chen J.J., Pike G.B. The BOLD-specific flow-volume relationship during hypercapnia and hypocapnia. ISMRM Conf Proc, Hawaii, Honolulu 2009, 1627.
13. Chen J.J., Pike G. Global cerebral oxidative metabolism during hypercapnia and hypocapnia in humans: implications for BOLD fMRI. J. Cereb. Blood Flow Metab. 2010, 30:1094-1099.
14. 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.
15. Chiarelli P.A., Bulte D.P., Piechnik S., Jezzard P. Sources of systematic bias in hypercapnia-calibrated functional MRI estimation of oxygen metabolism. NeuroImage 2007, 34:35-43.
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. Comroe, J., 1979. Physiology of Respiration: An Introduction, 2nd Revised edition ed. Year Book Medical Publishers Chicago, IL, USA.
18. Cox R.W. AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Comput. Biomed. Res. 1996, 29:162-173.
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. Evans A.C., Collins D.L., Mills S.R., Brown E.D., Kelly R.L., Peters T.M. 3D statistical neuroanatomical models from 305 MRI volumes. IEEE Nucl. Sci. Symp. Med. Imaging Conf. Rec. 1993, 1813-1817.
21. Floyd T.F., Clark J.M., Gelfand R., Detre J.A., Ratcliffe S., Guvakov D., Lambertsen C.J., Eckenhoff R.G. Independent cerebral vasoconstrictive effects of hyperoxia and accompanying arterial hypocapnia at 1ATA. J. Appl. Physiol. 2003, 95:2453-2461.
22. Frackowiak R.S.J., Lenzi G.L., Jones T., Heather J. Quantitative measurement of regional cerebral blood flow and oxygen metabolism in man using 15-O and positron emission tomography: theory, procedure, and normal values. J. Comput. Assist. Tomogr. 1980, 4:727-736.
23. 2 cerebral blood volume, blood flow, and vascular mean transit time. Stroke 1974, 5:630-639.
24. Gustard S., Williams E.J., Hall E.J., Picard 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.
25. Hoge R., Atkinson J., Gill B., Crelier G., Marrett S., Pike G. Investigation of BOLD signal dependence on cerebral blood flow and oxygen consumption: the deoxyhemoglobin dilution model. Magn. Reson. Med. 1999, 42:849-863.
26. Hoge R.D., Atkinson J., Gill B., Crelier G., Marrett S., Pike G.B. Stimulus-dependent BOLD and perfusion dynamics in human V1. NeuroImage 1999, 9:573-585.
27. 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.
28. Iadecola C. Regulation of the cerebral microcirculation during neural activity: is nitric oxide the missing link?. Trends Neurosci. 1996, 16:206-214.
29. Iadecola C., Zhang F. Nitric oxide-dependent and -independent components of cerebrovasodilation elicited by hypercapnia. Am. J. Anesthesiol. 1994, 266:R546-R552.
30. Ito H., Takahashi K., Hatazawa J., Kim S.-G., Kanno I. Changes in human regional cerebral blood flow and cerebral blood volume during visual stimulation measured by positron emission tomography. J. Cereb. Blood Flow Metab. 2001, 21:608-612.
31. Ito H., Kanno I., Ibaraki M., Hatazawa J., Miura S. Changes in human cerebral blood flow and cerebral blood volume during hypercapnia and hypocapnia measured by positron emission tomography. J. Cereb. Blood Flow Metab. 2003, 23:665-670.
32. 2 in subjects at rest. J. Physiol. 2008, 15:3675-3682.
33. Kastrup A., Krueger G., Neumann-Haefelin T., Glover G.H., Moseley M.E. Changes of cerebral blood flow, oxygenation, and oxydative metabolism during graded motor activation. NeuroImage 2002, 15:74-82.
34. Kemna L.J., Posse S., Tellmann L., Schmidtz T., Herzog H. Interdependence of regional and global cerebral blood flow during visual stimulation: an O-15-butanol position emission tomography study. J. Cereb. Blood Flow Metab. 2001, 21:664-670.
35. Kety S., Schmidth C. The effects of altered arterial tensions of carbon dioxide and oxygen on cerebral blood flow and cerebral oxygen consumption of normal young men. J. Clin. Invest. 1948, 27:484-492.
36. Kim S., Rostrup E., Larsson H., Ogawa S., Pau Ison O. 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.
37. Kim T., Hendrich 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.
38. 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.
39. Kolbitsch C., Lorenz I.H., Hörmann C., Hinteregger M., Löckinger A., Moser P.L., Kremser C., Schocke M., Felber S., Pfeiffer K.P., Benzer A. The influence of hyperoxia on the regional cerebral blood flow (rCBF), regional cerebral blood volume (rCBV) and the cerebral blood flow velocity in the middle cerebral artery (CBFVMCA) in human volunteers. Magn. Reson. Imaging 2002, 20:535-541.
40. 2. Magn. Reson. Med. 1995, 33:448-452.
41. Lee S.-P., Duong T., Yang G., Iadecola C., Kim S.-G. Relative changes of cerebral arterial and venous blood volumes during increased cerebral blood flow: implications for BOLD fMRI. Magn. Reson. Med. 2001, 45:791-800.
42. Leenders K., Perina D., Lammertsman A., Heather J., Buckingham P., Healy M., Gibbs J., Wise R., Hatazawa J., Herold S. Cerebral blood flow, blood volume and oxygen utilization. Normal values and effect of age. Brain 1990, 113:27-47.
43. Leontiev O., Buxton R.B. Reproducibility of BOLD, perfusion, and CMRO2 measurements with calibrated-BOLD fMRI. NeuroImage 2007, 35:175-184.
44. Losert C., Peller M., Schneider P., Reiser M. Oxygen-enhanced MRI of the brain. Magn. Reson. Med. 2002, 48:271-277.
45. 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.
46. Lu H., Donahue M.J., van Zijl P.C.M. Detrimental effects of BOLD signal in arterial spin labeling fMRI at high field strength. Magn. Reson. Med. 2006, 56:546-552.
47. Lu H., Zhao C., Ge Y., Lewis-Amezcua K. Baseline blood oxygenation modulates response amplitude: physiological basis for intersubject variations in functional MRI signals. Magn. Reson. Med. 2008, 60:364-372.
48. Mark C., Slessarev M., Shoji I., Han J., Fisher J., Pike B. Precise control of end-tidal carbon dioxide and oxygen improves BOLD and ASL cerebrovascular reactivity measures. Magn. Reson. Med. 2010, 64(3):749-756.
49. Ogawa S., Lee T.M., Barrere B. The sensitivity of magnetic resonance image signals of a rat brain to changes in the cerebral venous blood oxygenation. Magn. Reson. Med. 1993, 29:205-210.
50. Permutter J., Herscovitch P., Powers W., Fox P., Raichle M.E. Standardized mean regional method for calculating global positron emission tomographic measurements. J. Cereb. Blood Flow Metab. 1985, 5:476-480.
51. 2 in humans. J. Appl. Physiol. 1996, 81:1084-1095.
52. Prisman E., Slessarev M., Azami T., Nayot D., Milosevic M., Fisher J.A. Modified oxygen mask to induc target levels of hyperoxia and hypercarbia during radiotherapy: a more effective alternative to carbogen. Int. J. Radiat. Biol. 2007, 457-462.
53. 2 on blood oxygen level-dependent (BOLD) MRI. J. Magn. Reson. Imaging 2008, 27:185-191.
54. Raichle M., Gusnard D. Appraising the brain's energy budget. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:10237-10239.
55. Reinstrup P., Ryding E., Ohlsson T., Dahm P.L., Uski T. Cerebral blood volume (CBV) in humans during normo- and hypocapnia. Anesthesiology 2001, 95:1079-1082.
56. 2 in men. J. Appl. Physiol. 1990, 68:1727-1731.
57. Rostrup E., Blinkenberg M., Larsson H.B.W., Born A.P., Paulson O.B. Regional differences in the CBF and BOLD responses to hypercapnia: a combined PET and fMRI study. NeuroImage 2000, 11:87-97.
58. Rostrup E., Knudsen G.M., Law I., Holm S., Larsson H.B.W., Paulson O.B. The relationship between cerebral blood flow and volume in humans. NeuroImage 2005, 24:1-11.
59. 2 dissociation computations. J. Appl. Physiol. 1979, 46:599-602.
60. Sicard K., Duong T. Effects of hypoxia, hyperoxia, and hypercapnia on the baseline and stimulus-evoked BOLD, CBF, and CMRO2 in spontaneously breathing animals. NeuroImage 2005, 25:850-858.
61. 2 concentrations. J. Physiol. 2007, 581:1207-1219.
62. 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.
63. Stephan K.E., Weiskopf N., Drysdale P.M., Robinson P.A., Friston K.J. Comparing hemodynamic models with DCM. NeuroImage 2007, 38:387-401.
64. Uludag K., Dubowitz D., Yoder E., Restom K., Liu T., Buxton R. Coupling of cerebral blood flow and oxygen consumption during physiological activation and deactivation measured with fMRI. NeuroImage 2004, 23:148-155.
65. Van de Louw A., Cracco C., Cerf C., Harf A., Duvaldestin P., Lemaire F., Brochard L. Accuray of pulse oximetry in the intensive care unit. Intensive Care Med. 2001, 27:1606-1613.
66. Vazquez A.L., Fukuda M., Tasker M.L., Masamoto K., Kim S.-G. Changes in cerebral arterial, tissue and venous oxygenation with evoked neual stimulation: implications for hemoglobin-based functional neuroimaging. J. Cereb. Blood Flow Metab. 2010, 30:428-439.
67. Warnking J.M., Pike G.B. Bandwidth-modulated adiabatic RF pulses for uniform selective saturation and inversion. Magn. Reson. Med. 2004, 52:1190-1199.
68. Warnking J.M., Pike G.B. Reducing contamination while closing the gap: BASSI RF pulses in PASL. Magn. Reson. Med. 2006, 55:865-873.
69. Watson N.A., Beardst S.C., Altaf N., Kassner A., Jackson A. The effect of hyperoxia on cerebral blood flow: a study in healthy volunteers using magnetic resonance phase-contrast. Eur. J. Anaesthesiol. 2000, 17:152-159.
70. Wise R.G., Pattinson K.T.S., Bulte D.P., Chiarelli P.A., Mayhew S.D., Balanos G.M., O'Connor D.F., Pragnell T.R., Robbins P.A., Tracey I., Jezzard P. Dynamic forcing of end-tidal carbon dioxide and oxygen applied to functional magnetic resonance imaging. J. Cereb. Blood Flow Metab. 2007, 27:1521-1532.
71. Wong E.C., Buxton R.B., Frank L.R. Implementation of quantitative perfusion imaging techniques for functional brain mapping using pulses arterial spin labeling. NMR Biomed. 1997, 10:237-249.
72. Wong E.C., Buxton R.B., Frank L.R. Quantitative imaging of perfusion using a single substraction (QUIPSS and QUIPSSII). Magn. Reson. Med. 1998, 39:702-708.
73. Worsley K., Liao C., Aston J., Petre V., Duncan G., Morales F., Evans A. A general statistical analysis for fMRI data. NeuroImage 2002, 15:1-15.
74. Ye F.Q., Frank J.A., Weinberger D.R., McLaughlin A.C. Noise reduction in 3D perfusion imaging by attenuating the static signal in arterial spin tagging (ASSIST). Magn. Reson. Med. 2000, 44:92-100.
75. Zappe A., Uludag K., Oeltermann A., Ugurbil K., Logothetis N. The influence of moderate hypercapnia on neural activity in the anesthetied nonhuman primate. Cereb. Cortex 2008, 18:2666-2673.
76. Zhao F., Jin T., Wang P., Kim S.-G. Improved spatial localization of post-stimulus BOLD undershoot relative to positive BOLD. NeuroImage 2007, 34:1084-1092.