Slab-selective, BOLD-corrected VASO at 7 Tesla provides measures of cerebral blood volume reactivity with high signal-to-noise ratio
Corresponding Author
Laurentius Huber
Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany
Correspondence to: Laurentius Huber, M.Sc., Nuclear Magnetic Resonance Unit, Max Planck Institute for Human Cognitive and Brain Sciences, Stephanstrasse 1 A, 04103 Leipzig, Germany. E-mail: [email protected]Search for more papers by this authorDimo Ivanov
Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany
Maastricht Brain Imaging Centre, Maastricht University, Maastricht, The Netherlands
Search for more papers by this authorSteffen N. Krieger
Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany
Monash Biomedical Imaging, Monash University, Melbourne, Victoria, Australia
Search for more papers by this authorMarkus N. Streicher
Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany
Search for more papers by this authorToralf Mildner
Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany
Search for more papers by this authorBenedikt A. Poser
Maastricht Brain Imaging Centre, Maastricht University, Maastricht, The Netherlands
Department of Medicine, John A. Burns School of Medicine, University of Hawaii, Honolulu, Hawaii, USA
Donders Institute, Centre for Cognitive Neuroimaging, Radboud University Nijmegen, Nijmegen, The Netherlands
Search for more papers by this authorHarald E. Möller
Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany
Search for more papers by this authorRobert Turner
Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany
Search for more papers by this authorCorresponding Author
Laurentius Huber
Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany
Correspondence to: Laurentius Huber, M.Sc., Nuclear Magnetic Resonance Unit, Max Planck Institute for Human Cognitive and Brain Sciences, Stephanstrasse 1 A, 04103 Leipzig, Germany. E-mail: [email protected]Search for more papers by this authorDimo Ivanov
Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany
Maastricht Brain Imaging Centre, Maastricht University, Maastricht, The Netherlands
Search for more papers by this authorSteffen N. Krieger
Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany
Monash Biomedical Imaging, Monash University, Melbourne, Victoria, Australia
Search for more papers by this authorMarkus N. Streicher
Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany
Search for more papers by this authorToralf Mildner
Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany
Search for more papers by this authorBenedikt A. Poser
Maastricht Brain Imaging Centre, Maastricht University, Maastricht, The Netherlands
Department of Medicine, John A. Burns School of Medicine, University of Hawaii, Honolulu, Hawaii, USA
Donders Institute, Centre for Cognitive Neuroimaging, Radboud University Nijmegen, Nijmegen, The Netherlands
Search for more papers by this authorHarald E. Möller
Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany
Search for more papers by this authorRobert Turner
Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany
Search for more papers by this authorAbstract
Purpose
MRI methods sensitive to functional changes in cerebral blood volume (CBV) may map neural activity with better spatial specificity than standard functional MRI (fMRI) methods based on blood oxygen level dependent (BOLD) effect. The purpose of this study was to develop and investigate a vascular space occupancy (VASO) method with high sensitivity to CBV changes for use in human brain at 7 Tesla (T).
Methods
To apply 7T VASO, several high-field-specific obstacles must be overcome, e.g., low contrast-to-noise ratio (CNR) due to convergence of blood and tissue T1, increased functional BOLD signal change contamination, and radiofrequency field inhomogeneities. In the present method, CNR was increased by keeping stationary tissue magnetization in a steady-state different from flowing blood, using slice-selective saturation pulses. Interleaved acquisition of BOLD and VASO signals allowed correction for BOLD contamination.
Results
During visual stimulation, a relative CBV change of 28% ± 5% was measured, confined to gray matter in the occipital lobe with high sensitivity.
Conclusion
By carefully considering all the challenges of high-field VASO and filling behavior of the relevant vasculature, the proposed method can detect and quantify CBV changes with high CNR in human brain at 7T. Magn Reson Med 72:137–148, 2014. © 2013 Wiley Periodicals, Inc.
REFERENCES
- 1Kim T, Kim SG. 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; 12: 1211–1222.
- 2Lu H, Patel S, Luo F, Li SJ, Hillard CJ, Ward BD, Hyde JS. Spatial correlations of laminar BOLD and CBV responses to rat whisker stimulation with neuronal activity localized by Fos expression. Magn Reson Med 2004; 52: 1060–1068.
- 3Kennerley AJ, Mayhew JE, Redgrave P, Berwick J. Vascular origins of BOLD and CBV fMRI signals: statistical mapping and histological sections compared. Open Neuroimag J 2010; 4: 1–8.
- 4Lu H, Golay X, Pekar JJ, van Zijl PCM. Functional magnetic resonance imaging based on changes in vascular space occupancy. Magn Reson Med 2003; 50: 263–274.
- 5Jin T, Kim S-G. Improved cortical-layer specificity of vascular space occupancy fMRI with slab inversion relative to spin-echo BOLD at 9.4T. Neuroimage 2008; 40: 59–67.
- 6Hua J, Jones CK, Qin Q, van Zijl PC. Implementation of vascular-space-occupancy MRI at 7T. Magn Reson Med 2013; 69: 1003–1013.
- 7Rooney WD, Johnson G, Li X, Cohen ER, Kim S-G, Ugurbil K, Springer CS. Magnetic field and tissue dependencies of human brain longitudinal H2O relaxation in vivo. Magn Reson Med 2007; 57: 308–318.
- 8Lu H, van Zijl PCM. Experimental measurement of extravascular parenchymal BOLD effect and tissue oxygen extraction fraction using multi-echo VASO fMRI at 1.5 and 3.0 T. Magn Reson Med 2005; 53: 808–816.
- 9Hetzer S, Mildner T, Moller HE. A modified EPI sequence for high-resolution imaging at ultra-short echo time. Magn Reson Med 2011; 65: 165–175.
- 10Hua J, Donahue MJ, Zhao JM, Grgac K, Huang AJ, Zhou J, van Zijl PC. Magnetization transfer enhanced vascular-space-occupancy (MT-VASO) functional MRI. Magn Reson Med 2009; 61: 944–951.
- 11Wu WC, Buxton RB, Wong EC. Vascular space occupancy weighted imaging with control of residual blood signal and higher contrast-to-noise ratio. IEEE Trans Med Imaging 2007; 26: 1319–1327.
- 12Wu CW, Chuang KH, Wai YY, Wan YL, Chen JH, Liu HL. Vascular space occupancy-dependent functional MRI by tissue suppression. J Magn Reson Imaging 2008; 28: 219–226.
- 13Shen Y, Kauppinen RA, Vidyasagar R, Golay X. A functional magnetic resonance imaging technique based on nulling extravascular gray matter signal. J Cereb Blood Flow Metab 2009; 29: 144–156.
- 14Jin T, Kim SG. Spatial dependence of CBV-fMRI: a comparison between VASO and contrast agent based methods. Conf Proc IEEE Eng Med Biol Soc 2006; 1: 25–28.
- 15Kim SG. Quantification of relative cerebral blood-Flow change by flow-sensitive alternating inversion-recovery (FAIR) technique - application to functional mapping. Magn Reson Med 1995; 34: 293–301.
- 16Dobre MC, Ugurbil K, Marjanska M. Determination of longitudinal relaxation time (T1) at high magnetic field strengths. Magn Reson Imaging 2006; 25: 733–735.
- 17Grgac K, van Zijl PC, Qin Q. Hematocrit and oxygenation dependence of blood (1) H(2) O T(1) at 7 tesla. Magn Reson Med 2013; 70: 1153–1159.
- 18Zhang X, Petersen ET, Ghariq E, De Vis JB, Webb AG, Teeuwisse WM, Hendrikse J, van Osch MJ. In vivo blood T(1) measurements at 1.5 T, 3 T, and 7 T. Magn Reson Med 2013; 70: 1082–1086.
- 19Francis ST, Bowtell RW, Gowland PA. Modeling and optimization of look-locker spin labeling for measuring perfusion and transit time changes in activation studies taking into account arterial blood volume. Magn Reson Imaging 2008; 59: 316–325.
- 20Wong EC, Buxton R, Frank LR. Implementation of quantitative perfusion imaging techniques for functional brain mapping using pulsed arterial spin labeling. NMR Biomed 1997; 10: 237–249.
10.1002/(SICI)1099-1492(199706/08)10:4/5<237::AID-NBM475>3.0.CO;2-X CAS PubMed Web of Science® Google Scholar
- 21Chen Y, Wang DJ, Detre JA. Comparison of arterial transit times estimated using arterial spin labeling. MAGMA 2012; 25: 135–144.
- 22Norris DG, Haase A. Variable excitation angle AFP pulses. Magn Reson Med 1989; 9: 435–440.
- 23Pawlik G, Rackl A, Bing RJ. Quantitative capillary topography and blood flow in the cerebral cortex of cats: an in vivo microscopic study. Brain Res 1981; 208: 35–58.
- 24Kleinfeld D, Mitra PP, Helmchen F, Denk W. Fluctuations and stimulus-induced changes in blood flow observed in individual capillaries in layers 2 through 4 of rat neocortex. Proc Natl Acad Sci U S A 1998; 95: 15741.
- 25Hillman EMC, Devor A, Bouchard MB, Dunn AK, Krauss GW, Skoch J, Bacskai BJ, Dale AM, Boas DA. Depth-resolved optical imaging and microscopy of vascular compartment dynamics during somatosensory stimulation. Neuroimage 2007; 35: 89–104.
- 26Nakagawa H, Lin S-Z, Bereczki D, Gesztelyi G, Otsuka T, Wei L, Hans F-J, Acuff VR, Chen J-L, Pettigrew KD, et al. Blood volumes, hematocrits, and transit-times in parenchymal microvascular systems of the rat brain. In: LB Denis, editor. Diffusion and perfusion magnetic resonance imaging: application to functional MRI. New York: Raven Press; 1995. p 193–204.
- 27Jespersen SN, Ostergaard L. The roles of cerebral blood flow, capillary transit time heterogeneity, and oxygen tension in brain oxygenation and metabolism. J Cereb Blood Flow Metab 2012; 32: 264–277.
- 28Lu H, Hua J, van Zijl PC. Noninvasive functional imaging of cerebral blood volume with vascular-space-occupancy (VASO) MRI. NMR Biomed 2013; 26: 932–948.
- 29Donahue MJ, Hoogduin H, van Zijl PC, Jezzard P, Luijten PR, Hendrikse J. Blood oxygenation level-dependent (BOLD) total and extravascular signal changes and DeltaR2* in human visual cortex at 1.5, 3.0 and 7.0 T. NMR Biomed 2011; 24: 25–34.
- 30Martindale J, Kennerley AJ, Johnston D, Zheng Y, Mayhew JE. Theory and generalization of Monte Carlo models of the BOLD signal source. Magn Reson Med 2008; 59: 607–618.
- 31Hurley AC, Al-Radaideh A, Bai L, Aickelin U, Coxon R, Glover P, Gowland PA. Tailored RF pulse for magnetization inversion at ultrahigh field. Magn Reson Med 2010; 63: 51–58.
- 32Shin W, Geng X, Gu H, Zhan W, Zou Q, Yang Y. Automated brain tissue segmentation based on fractional signal mapping from inversion recovery Look-Locker acquisition. Neuroimage 2010; 52: 1347–1354.
- 33Huk AC, Dougherty RF, Heeger DJ. Retinotopy and functional subdivision of human areas MT and MST. J Neurosci 2002; 22: 7195–7205.
- 34Ho Y-CL, Peterson RT, Zimine I, Golay X. Similarities and differences in arterial responses to hypercapnia and visual stimulation. J Cereb Blood Flow Metab 2011; 31: 560–571.
- 35Worsley KJ. Statistical analysis of activation images. In: Jezzard P, Matthews PM, Smith SM, editors. Functional Magnetic Resonance Imaging: An Introduction to Methods. UK: Oxford University Press; 2001.
- 36Jochimsen TH, von Mengershausen M. ODIN-object-oriented development interface for NMR. J Magn Reson 2004; 170: 67–78.
- 37Lu H, Law M, Johnson G, Ge Y, van Zijl PCM. Novel approach to the measurement of absolute cerebral blood volume using vascular-space-occupancy magnetic resonance imaging. Magn Reson Med 2005; 54: 1403–1411.
- 38Giovacchini G, Chang MC, Channing MA, et al. Brain incorporation of 11c-arachidonic acid in young healthy humans measured with positron emission tomography. J Cereb Blood Flow Metab 2002; 22: 1453–1462.
- 39Belliveau JW, Kennedy DN, McKinstry RC, Buchbinder BR, Weisskoff RM, Cohen MS, Vevea JM, Brady TJ, Rosen BR. Functional mapping of the human visual cortex by magnetic resonance imaging. Science 1991; 254: 716–719.
- 40Piechnik SK, Evans J, Bary LH, Wise RG, Jezzard P. Functional changes in CSF volume estimated using measurement of water T2 relaxation. Magn Reson Imaging 2009; 61: 579–586.
- 41Ito 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.
- 42Lu H, Zhao C, Ge Y, Lewis-Amezcua K. Baseline blood oxygenation modulates response amplitude: physiologic basis for intersubject variations in functional MRI signals. Magn Reson Med 2008; 60: 364–372.
- 43Tjandra T, Brooks JCW, Figueiredo P, Wise R, Matthews PM, Tracey I. Quantitative assessment of the reproducibility of functional activation measured with BOLD and MR perfusion imaging: implications for clinical trial design. Neuroimage 2005; 27: 393–401.
- 44Leontiev O, Buxton RB. Reproducibility of BOLD, perfusion, and CMRO2 measurements with calibrated-BOLD fMRI. Neuroimage 2007; 35: 175–184.
- 45Mandeville JB, Marota JJ, Ayata C, Zaharchuk G, Moskowitz MA, Rosen BR, Weisskoff RM. Evidence of a cerebrovascular postarteriole windkessel with delayed compliance. J Cereb Blood Flow Metab 1999; 19: 679–689.
- 46Dechent P, Schuetze G, Helms G, Merboldt KD, Frahm J. Basal cerebral blood volume during the poststimulation undershoot in BOLD MRI of the human brain. J Cereb Blood Flow Metab 2010; 31: 82–89.
- 47Poser BA, Norris DG. Measurement of activation-related changes in cerebral blood volume: VASO with single-shot HASTE acquisition. Magn Reson Mater Phys 2007; 20: 63–67.
- 48van Zijl PC, Hua J, Lu H. The BOLD post-stimulus undershoot, one of the most debated issues in fMRI. Neuroimage 2012; 62: 1092–1102.
- 49Buxton RB, Wong EC, Frank LR. Dynamics of blood flow and oxygenation changes during brain activation: the balloon model. Magn Reson Med 1998; 39: 855–864.
- 50Morki B. The Monro-Kellie hypothesis: applications in CSF volume depletion. Neurology 2001; 56: 1746–1748.
- 51Scouten A, Constable RT. VASO-based calculations of CBV change: accounting for the dynamic CSF volume. Magn Reson Med 2008; 58: 308–315.
- 52Jin T, Kim SG. Change of the cerebrospinal fluid volume during brain activation investigated by T(1rho)-weighted fMRI. Neuroimage 2010; 51: 1378–1383.
- 53Donahue MJ, Lu H, Jones CK, Edden RA, Pekar JJ, van Zijl PC. Theoretical and experimental investigation of the VASO contrast mechanism. Magn Reson Med 2006; 56: 1261–1273.
- 54Scouten A, Constable RT. Application and limitations of whole-brain MAGIC VASO fuctional fmaging. Magn Reson Med 2007; 58: 306–315.
- 55Jin T, Kim SG. Cortical layer-dependent dynamic blood oxygenation, cerebral blood flow and cerebral blood volume responses during visual stimulation. Neuroimage 2008; 43: 1–9.
- 56Zhao F, Jin T, Wang P, Hu X, Kim SG. Sources of phase changes in BOLD and CBV-weighted fMRI. Magn Reson Med 2007; 57: 520–527.
- 57Kim SG, Harel N, Jin T, Kim T, Lee P, Zhao F. Cerebral blood volume MRI with intravascular superparamagnetic iron oxide nanoparticles. NMR Biomed 2013; 26: 949–962.
- 58Kennerley AJ, Berwick J, Martindale J, Johnston D, Papadakis N, Mayhew JE. Concurrent fMRI and optical measures for the investigation of the hemodynamic response function. Magn Reson Med 2005; 54: 354–365.
- 59Kim T, Hendrich KS, Masamoto K, Kim SG. 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.
- 60Wu CW, Liu H-L, Chen J-H, Yang Y. Effects of CBV, CSF, and blood-brain barrier permeability on accuracy of PASL and VASO measurement. Magn Reson Med 2010; 63: 601–608.
- 61Poser BA, Norris DG. 3D single-shot VASO using a Maxwell gradient compensated GRASE sequence. Magn Reson Med 2009; 62: 255–262.
- 62Donahue MJ, Blicher JU, Ostergaard L, Feinberg DA, MacIntosh BJ, Miller KL, 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.
- 63Poser BA, Norris DG. Application of whole-brain CBV-weighted fMRI to a cognitive stimulation paradigm: robust activation detection in a stroop task experiment using 3D GRASE VASO. Hum Brain Mapp 2011; 32: 974–981.
- 64Ciris PA, Qiu M, Constable TR. Non-invasive quantification of absolute cerebral blood volume applicable to the whole human brain. In Proceedings of the 20th Annual Meeting of ISMRM, Melbourne, Australia, 2012. Abstract 381.
- 65Calamante F, Thomas DL, Pell GS, Wiersma J, Turner R. Measuring cerebral blood flow using magnetic resonance imaging techniques. J Cereb Blood Flow Metab 1999; 19: 701–735.
- 66Huber L, Goense J, Ivanov D, Krieger SN, Turner R, Möller HE. Cerebral blood volume changes in negative BOLD regions during visual stimulation in humans at 7T. In Proceedings of the 21st Annual Meeting of ISMRM, Salt Lake Citiy, Utah, 2013. Abstract 918.
- 67Goense J, Merkle H, Logothetis NK. High-resolution fMRI reveals laminar differences in neurovascular coupling between positive and negative BOLD responses. Neuron 2012; 76: 629–639.
- 68Huber L, Ivanov D, Krieger SN, Gauthier C, Roggenhofer E, Henseler I, Turner R, Moller HE. Measurements of cerebral blood volume and BOLD signal during hypercapnia and functional stimulation in humans at 7T: application to calibrated BOLD. In Proceedings of the 21st Annual Meeting of ISMRM, Salt Lake Citiy, Utah, USA, 2013. Abstract 918.