Robustly measuring vascular reactivity differences with breath-hold: Normalising stimulus-evoked and resting state BOLD fMRI data

NeuroImage

Volumn 54, Issue 1, 2011, Pages 369-379

  Murphy, Kevin ^a   Harris, Ashley D ^a   Wise, Richard G ^a  

^a CARDIFF UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON DIOXIDE; OXYGEN;

ACCURACY; ADULT; ARTICLE; BLOOD VESSEL REACTIVITY; BREATH HOLDING; CONTROLLED STUDY; DATA BASE; END TIDAL CARBON DIOXIDE TENSION; EVOKED RESPONSE; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HEMODYNAMICS; HUMAN; HUMAN EXPERIMENT; IMAGE ANALYSIS; IMAGE DISPLAY; MALE; NERVE STIMULATION; NORMAL HUMAN; OXYGEN BLOOD LEVEL; PRESSURE MEASUREMENT; PRIORITY JOURNAL;

ADULT; ANALYSIS OF VARIANCE; BLOOD VOLUME; BRAIN; BRAIN MAPPING; BREATH TESTS; CARBON DIOXIDE; CEREBROVASCULAR CIRCULATION; HUMANS; MAGNETIC RESONANCE IMAGING; MAXIMAL VOLUNTARY VENTILATION; OXYGEN; REGRESSION ANALYSIS; RESPIRATORY MECHANICS; REST; TIDAL VOLUME;

EID: 77957953386     PISSN: 10538119     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2010.07.059     Document Type: Article

References (64)

1. Abbott D.F., Opdam H.I., Briellmann R.S., Jackson G.D. Brief breath holding may confound functional magnetic resonance imaging studies. Hum. Brain Mapp. 2005, 24:284-290.
2. Bandettini P.A., Wong E.C. A hypercapnia-based normalization method for improved spatial localization of human brain activation with fMRI. NMR Biomed. 1997, 10:197-203.
3. Bandettini P.A., Wong E.C., Hinks R.S., Tikofsky R.S., Hyde J.S. Time course EPI of human brain function during task activation. Magn. Reson. Med. 1992, 25:390-397.
4. Beckmann C.F., Jenkinson M., Smith S.M. General multilevel linear modeling for group analysis in FMRI. Neuroimage 2003, 20:1052-1063.
5. Behzadi Y., Liu T.T. Caffeine reduces the initial dip in the visual BOLD response at 3T. Neuroimage 2006, 32:9-15.
6. Birn R.M., Diamond J.B., Smith M.A., Bandettini P.A. Separating respiratory-variation-related fluctuations from neuronal-activity-related fluctuations in fMRI. Neuroimage 2006, 31:1536-1548.
7. Birn R.M., Murphy K., Bandettini P.A. The effect of respiration variations on independent component analysis results of resting state functional connectivity. Hum. Brain Mapp. 2008, 29:740-750.
8. Biswal B., Yetkin F.Z., Haughton V.M., Hyde J.S. Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn. Reson. Med. 1995, 34:537-541.
9. Biswal B., Hudetz A.G., Yetkin F.Z., Haughton V.M., Hyde J.S. Hypercapnia reversibly suppresses low-frequency fluctuations in the human motor cortex during rest using echo-planar MRI. J. Cereb. Blood Flow Metab. 1997, 17:301-308.
10. Bright M.G., Bulte D.P., Jezzard P., Duyn J.H. Characterization of regional heterogeneity in cerebrovascular reactivity dynamics using novel hypocapnia task and BOLD fMRI. Neuroimage 2009, 48:166-175.
11. 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.
12. 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.
13. Cohen E.R., Rostrup E., Sidaros K., Lund T.E., Paulson O.B., Ugurbil K., Kim S.G. Hypercapnic normalization of BOLD fMRI: comparison across field strengths and pulse sequences. Neuroimage 2004, 23:613-624.
14. Corfield D.R., Murphy K., Josephs O., Adams L., Turner R. Does hypercapnia-induced cerebral vasodilation modulate the hemodynamic response to neural activation?. Neuroimage 2001, 13:1207-1211.
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. PNAS 1998, 95:1834-1839.
17. Fox M.D., Raichle M.E. Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat. Rev. Neurosci. 2007, 8:700-711.
18. Fox M.D., Snyder A.Z., Vincent J.L., Corbetta M., Van Essen D.C., Raichle M.E. The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:9673-9678.
19. Friston K.J., Fletcher P., Josephs O., Holmes A., Rugg M.D., Turner R. Event-related fMRI: characterizing differential responses. Neuroimage 1998, 7:30-40.
20. Handwerker D.A., Ollinger J.M., D'Esposito M. Variation of BOLD hemodynamic responses across subjects and brain regions and their effects on statistical analyses. Neuroimage 2004, 21:1639-1651.
21. Handwerker D.A., Gazzaley A., Inglis B.A., D'Esposito M. Reducing vascular variability of fMRI data across aging populations using a breathholding task. Hum. Brain Mapp. 2007, 28:846-859.
22. Harper R.M., Gozal D., Bandler R., Spriggs D., Lee J., Alger J. Regional brain activation in humans during respiratory and blood pressure challenges. Clin. Exp. Pharmacol. Physiol. 1998, 25:483-486.
23. 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. PNAS 1999, 96:9403-9408.
24. Iannetti G.D., Wise R.G. BOLD functional MRI in disease and pharmacological studies: room for improvement?. Magn. Reson. Imaging 2007, 25:978-988.
25. Iannetti G.D., Zambreanu L., Wise R.G., Buchanan T.J., Huggins J.P., Smart T.S., Vennart W., Tracey I. Pharmacological modulation of pain-related brain activity during normal and central sensitization states in humans. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:18195-18200.
26. Ito H., Yokoyama I., Iida H., Kinoshita T., Hatazawa J., Shimosegawa E., Okudera T., Kanno I. Regional differences in cerebral vascular response to PaCO2 changes in humans measured by positron emission tomography. J. Cereb. Blood Flow Metab. 2000, 20:1264-1270.
27. 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.
28. Kastrup A., Li T.Q., Takahashi A., Glover G.H., Moseley M.E. Functional magnetic resonance imaging of regional cerebral blood oxygenation changes during breath holding. Stroke 1998, 29:2641-2645.
29. Kastrup A., Kruger G., Glover G.H., Neumann-Haefelin T., Moseley M.E. Regional variability of cerebral blood oxygenation response to hypercapnia. Neuroimage 1999, 10:675-681.
30. Kastrup A., Li T.Q., Glover G.H., Moseley M.E. Cerebral blood flow-related signal changes during breath-holding. AJNR Am. J. Neuroradiol. 1999, 20:1233-1238.
31. Kastrup A., Kruger G., Neumann-Haefelin T., Moseley M.E. Assessment of cerebrovascular reactivity with functional magnetic resonance imaging: comparison of CO(2) and breath holding. Magn. Reson. Imaging 2001, 19:13-20.
32. Kwong K.K., Belliveau J.W., Chesler D.A., Goldberg I.E., Weisskoff R.M., Poncelet B.P., Kennedy D.N., Hoppel B.E., Cohen M.S., Turner R., et al. Dynamic magnetic resonance imaging of human brain activity during primary sensory stimulation. PNAS 1992, 89:5675-5679.
33. Leontiev O., Buxton R.B. Reproducibility of BOLD, perfusion, and CMRO2 measurements with calibrated-BOLD fMRI. Neuroimage 2007, 35:175-184.
34. Li T.Q., Kastrup A., Takahashi A.M., Moseley M.E. Functional MRI of human brain during breath holding by BOLD and FAIR techniques. Neuroimage 1999, 9:243-249.
35. Liu H.L., Huang J.C., Wu C.T., Hsu Y.Y. Detectability of blood oxygenation level-dependent signal changes during short breath hold duration. Magn. Reson. Imaging 2002, 20:643-648.
36. Logothetis N.K. What we can do and what we cannot do with fMRI. Nature 2008, 453:869-878.
37. Lu H., Yezhuvath U.S., Xiao G. Improving fMRI sensitivity by normalization of basal physiologic state. Hum. Brain Mapp. 2010, 31:80-87.
38. Macefield V.G., Gandevia S.C., Henderson L.A. Neural sites involved in the sustained increase in muscle sympathetic nerve activity induced by inspiratory capacity apnea: a fMRI study. J. Appl. Physiol. 2006, 100:266-273.
39. Magon S., Basso G., Farace P., Ricciardi G.K., Beltramello A., Sbarbati A. Reproducibility of BOLD signal change induced by breath holding. Neuroimage 2009, 45:702-712.
40. Markus H.S., Harrison M.J. Estimation of cerebrovascular reactivity using transcranial Doppler, including the use of breath-holding as the vasodilatory stimulus. Stroke 1992, 23:668-673.
41. Mitsis G.D., Zhang R., Levine B.D., Marmarelis V.Z. Modeling of nonlinear physiological systems with fast and slow dynamics. II. Application to cerebral autoregulation. Ann. Biomed. Eng. 2002, 30:555-565.
42. Murphy K., Birn R.M., Handwerker D.A., Jones T.B., Bandettini P.A. The impact of global signal regression on resting state correlations: are anti-correlated networks introduced?. Neuroimage 2009, 44:893-905.
43. Ogawa S., Tank D.W., Menon R., Ellermann J.M., Kim S.G., Merkle H., Ugurbil K. Intrinsic signal changes accompanying sensory stimulation: functional brain mapping with magnetic resonance imaging. PNAS 1992, 89:5951-5955.
44. Panerai R.B., Simpson D.M., Deverson S.T., Mahony P., Hayes P., Evans D.H. Multivariate dynamic analysis of cerebral blood flow regulation in humans. IEEE Trans. Biomed. Eng. 2000, 47:419-423.
45. Posse S., Kemna L.J., Elghahwagi B., Wiese S., Kiselev V.G. Effect of graded hypo- and hypercapnia on fMRI contrast in visual cortex: quantification of T(*)(2) changes by multiecho EPI. Magn. Reson. Med. 2001, 46:264-271.
46. Poulin M.J., Liang P.J., Robbins P.A. Dynamics of the cerebral blood flow response to step changes in end-tidal PCO2 and PO2 in humans. J. Appl. Physiol. 1996, 81:1084-1095.
47. Rack-Gomer A.L., Liau J., Liu T.T. Caffeine reduces resting-state BOLD functional connectivity in the motor cortex. Neuroimage 2009, 46:56-63.
48. Ramsay S.C., Murphy K., Shea S.A., Friston K.J., Lammertsma A.A., Clark J.C., Adams L., Guz A., Frackowiak R.S. Changes in global cerebral blood flow in humans: effect on regional cerebral blood flow during a neural activation task. J. Physiol. 1993, 471:521-534.
49. Robbins P.A., Conway J., Cunningham D.A., Khamnei S., Paterson D.J. A comparison of indirect methods for continuous estimation of arterial PCO2 in men. J. Appl. Physiol. 1990, 68:1727-1731.
50. Rostrup E., Law I., Blinkenberg M., Larsson H.B., Born A.P., Holm S., Paulson O.B. Regional differences in the CBF and BOLD responses to hypercapnia: a combined PET and fMRI study. Neuroimage 2000, 11:87-97.
51. Sasse S.A., Berry R.B., Nguyen T.K., Light R.W., Mahutte C.K. Arterial blood gas changes during breath-holding from functional residual capacity. Chest 1996, 110:958-964.
52. Scouten A., Schwarzbauer C. Paced respiration with end-expiration technique offers superior BOLD signal repeatability for breath-hold studies. Neuroimage 2008, 43:250-257.
53. Shulman G.L., Corbetta M., Buckner R.L., Raichle M.E., Fiez J.A., Miezin F.M., Petersen S.E. Top-down modulation of early sensory cortex. Cereb. Cortex 1997, 7:193-206.
54. Smith S.M., Jenkinson M., Woolrich M.W., Beckmann C.F., Behrens T.E., Johansen-Berg H., Bannister P.R., De Luca M., Drobnjak I., Flitney D.E., Niazy R.K., Saunders J., Vickers J., Zhang Y., De Stefano N., Brady J.M., Matthews P.M. Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 2004, 23(Suppl 1):S208-S219.
55. Thomason M.E., Glover G.H. Controlled inspiration depth reduces variance in breath-holding-induced BOLD signal. Neuroimage 2008, 39:206-214.
56. Thomason M.E., Burrows B.E., Gabrieli J.D., Glover G.H. Breath holding reveals differences in fMRI BOLD signal in children and adults. Neuroimage 2005, 25:824-837.
57. Thomason M.E., Foland L.C., Glover G.H. Calibration of BOLD fMRI using breath holding reduces group variance during a cognitive task. Hum. Brain Mapp. 2007, 28:59-68.
58. van der Zande F.H., Hofman P.A., Backes W.H. Mapping hypercapnia-induced cerebrovascular reactivity using BOLD MRI. Neuroradiology 2005, 47:114-120.
59. Wise R.G., Ide K., Poulin M.J., Tracey I. Resting fluctuations in arterial carbon dioxide induce significant low frequency variations in BOLD signal. Neuroimage 2004, 21:1652-1664.
60. Woolrich M. Robust group analysis using outlier inference. Neuroimage 2008, 41:286-301.
61. 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.
62. 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.
63. Young W.L., Prohovnik I., Ornstein E., Ostapkovich N., Matteo R.S. Cerebral blood flow reactivity to changes in carbon dioxide calculated using end-tidal versus arterial tensions. J. Cereb. Blood Flow Metab. 1991, 11:1031-1035.
64. 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.