Quantitative study of changes in oxidative metabolism during visual stimulation using absolute relaxation rates

In the context of quantitative functional MRI (fMRI), deoxyhemoglobin (dHb) content is the essential physiological parameter for calibrating the blood oxygenation level‐dependent (BOLD) signal. In studies on humans, the baseline dHb content or its equivalent has been evaluated indirectly by means of carbon dioxide breathing as a physiological reference condition. In this study with normal volunteers, quantitative mapping of baseline dHb content was performed in a direct manner by measuring the reversible contribution of the effective transverse relaxation rate. The BOLD signal change in the visual cortex during 8 Hz flicker visual stimulation was calibrated based on the quantitative map of baseline dHb content. The calibrated relaxation rate change that represents the stimulation‐induced fractional change of dHb content decreased by 14% within the activated visual cortex. Simultaneous measurement of cerebral blood flow (CBF) with BOLD showed an increase of 59%. From the calibrated relaxation rate and CBF changes, the cerebral metabolic rate of oxygen (CMRO2) was calculated to increase by 19–28% within the activated visual cortex. The ratio of the CBF increase to the CMRO2 increase was 2–3:1, which agreed well with results of similar quantitative fMRI studies for humans. The method proposed here for quantitative evaluation of the BOLD signal may be applicable not only to fMRI for normal human subjects, but also to physiologically altered or diseased states, because it requires no physiological perturbation. Copyright © 2005 John Wiley & Sons, Ltd.

[1]  David L. Thomas,et al.  Measuring Cerebral Blood Flow Using Magnetic Resonance Imaging Techniques , 1999, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[2]  J. Reichenbach,et al.  Quantitative differentiation between BOLD models in fMRI , 2001, Magnetic resonance in medicine.

[3]  Seong‐gi Kim Cmrr,et al.  Comparison of blood oxygenattion and cerebral blood flow effect in fMRI: Estimation of relative oxygen consumption change , 1997, Magnetic resonance in medicine.

[4]  Gregory G. Brown,et al.  BOLD and Perfusion Response to Finger-Thumb Apposition after Acetazolamide Administration: Differential Relationship to Global Perfusion , 2003, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[5]  G. Crelier,et al.  Linear coupling between cerebral blood flow and oxygen consumption in activated human cortex. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[6]  S G Kim,et al.  Changes in Human Regional Cerebral Blood Flow and Cerebral Blood Volume during Visual Stimulation Measured by Positron Emission Tomography , 2001, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[7]  H. An,et al.  Quantitative measurements of cerebral metabolic rate of oxygen utilization using MRI: a volunteer study , 2001, NMR in biomedicine.

[8]  Y. Wang,et al.  Blood oxygen saturation assessment in vivo using T2 * estimation , 1998, Magnetic resonance in medicine.

[9]  Norihiko Fujita,et al.  Quantitative mapping of cerebral deoxyhemoglobin content using MR imaging , 2003, NeuroImage.

[10]  Gary H. Glover,et al.  Changes of Cerebral Blood Flow, Oxygenation, and Oxidative Metabolism during Graded Motor Activation , 2002, NeuroImage.

[11]  S. Ogawa Brain magnetic resonance imaging with contrast-dependent oxygenation , 1990 .

[12]  M. D’Esposito,et al.  Alterations in the BOLD fMRI signal with ageing and disease: a challenge for neuroimaging , 2003, Nature Reviews Neuroscience.

[13]  G. Glover,et al.  Assessment of cerebral oxidative metabolism with breath holding and fMRI , 1999, Magnetic resonance in medicine.

[14]  M. Mintun,et al.  Nonoxidative glucose consumption during focal physiologic neural activity. , 1988, Science.

[15]  G. Crelier,et al.  Investigation of BOLD signal dependence on cerebral blood flow and oxygen consumption: The deoxyhemoglobin dilution model , 1999, Magnetic resonance in medicine.

[16]  Bojana Stefanovic,et al.  Human whole‐blood relaxometry at 1.5T: Assessment of diffusion and exchange models , 2004, Magnetic resonance in medicine.

[17]  Seong-Gi Kim,et al.  Relative changes of cerebral arterial and venous blood volumes during increased cerebral blood flow: Implications for BOLD fMRI , 2001, Magnetic resonance in medicine.

[18]  B R Rosen,et al.  Mr contrast due to intravascular magnetic susceptibility perturbations , 1995, Magnetic resonance in medicine.

[19]  S. Posse,et al.  Effect of graded hypo‐ and hypercapnia on fMRI contrast in visual cortex: Quantification of T  *2 changes by multiecho EPI , 2001, Magnetic resonance in medicine.

[20]  T. L. Davis,et al.  Calibrated functional MRI: mapping the dynamics of oxidative metabolism. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[21]  Peter C M van Zijl,et al.  Experimental measurement of extravascular parenchymal BOLD effects and tissue oxygen extraction fractions using multi‐echo VASO fMRI at 1.5 and 3.0 T , 2005, Magnetic resonance in medicine.

[22]  E. Haacke,et al.  Theory of NMR signal behavior in magnetically inhomogeneous tissues: The static dephasing regime , 1994, Magnetic resonance in medicine.

[23]  Ravi S. Menon,et al.  Functional brain mapping by blood oxygenation level-dependent contrast magnetic resonance imaging. A comparison of signal characteristics with a biophysical model. , 1993, Biophysical journal.

[24]  C. S. Poon,et al.  Practical T2 quantitation for clinical applications , 1992, Journal of magnetic resonance imaging : JMRI.

[25]  Egill Rostrup,et al.  Determination of relative CMRO2 from CBF and BOLD changes: Significant increase of oxygen consumption rate during visual stimulation , 1999, Magnetic resonance in medicine.

[26]  J. R. Baker,et al.  The intravascular contribution to fmri signal change: monte carlo modeling and diffusion‐weighted studies in vivo , 1995, Magnetic resonance in medicine.

[27]  F W Wehrli,et al.  Method for image-based measurement of the reversible and irreversible contribution to the transverse-relaxation rate. , 1996, Journal of magnetic resonance. Series B.

[28]  Peter Andersen,et al.  Simultaneous oxygenation and perfbsion imaging study of functional activity in primary visual cortex at different visual stimulation frequency: Quantitative correlation between BOLD and CBF changes , 1998, Magnetic resonance in medicine.

[29]  John C Gore,et al.  Changes in CBF‐BOLD coupling detected by MRI during and after repeated transient hypercapnia in rat , 2002, Magnetic resonance in medicine.

[30]  N Fujita,et al.  Extravascular contribution of blood oxygenation level‐dependent signal changes: A numerical analysis based on a vascular network model , 2001, Magnetic resonance in medicine.

[31]  H. Yamauchi,et al.  Effects of Acetazolamide on Cerebral Blood Flow, Blood Volume, and Oxygen Metabolism: A Positron Emission Tomography Study with Healthy Volunteers , 2001, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[32]  Weili Lin,et al.  Quantitative Measurements of Cerebral Blood Oxygen Saturation Using Magnetic Resonance Imaging , 2000, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[33]  S. Ogawa,et al.  Oxygenation‐sensitive contrast in magnetic resonance image of rodent brain at high magnetic fields , 1990, Magnetic resonance in medicine.

[34]  D. Tank,et al.  Brain magnetic resonance imaging with contrast dependent on blood oxygenation. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[35]  W. Powers Cerebral hemodynamics in ischemic cerebrovascular disease , 1991, Annals of neurology.

[36]  M. Raichle,et al.  The Effects of Changes in PaCO2 Cerebral Blood Volume, Blood Flow, and Vascular Mean Transit Time , 1974, Stroke.

[37]  M. Raichle,et al.  Focal physiological uncoupling of cerebral blood flow and oxidative metabolism during somatosensory stimulation in human subjects. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[38]  Seong-Gi Kim Quantification of relative cerebral blood flow change by flow‐sensitive alternating inversion recovery (FAIR) technique: Application to functional mapping , 1995, Magnetic resonance in medicine.

[39]  E C Wong,et al.  Comparison of simultaneously measured perfusion and BOLD signal increases during brain activation with T1‐based tissue identification , 2000, Magnetic resonance in medicine.

[40]  M E Raichle,et al.  Coupling between changes in human brain temperature and oxidative metabolism during prolonged visual stimulation. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[41]  K. Uğurbil,et al.  Effect of Basal Conditions on the Magnitude and Dynamics of the Blood Oxygenation Level-Dependent fMRI Response , 2002, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[42]  Jeroen van der Grond,et al.  Measurements of cerebral perfusion and arterial hemodynamics during visual stimulation using TURBO‐TILT , 2003, Magnetic resonance in medicine.

[43]  T. Foster,et al.  A review of normal tissue hydrogen NMR relaxation times and relaxation mechanisms from 1-100 MHz: dependence on tissue type, NMR frequency, temperature, species, excision, and age. , 1984, Medical physics.

[44]  Weili Lin,et al.  Cerebral oxygen extraction fraction and cerebral venous blood volume measurements using MRI: Effects of magnetic field variation , 2002, Magnetic resonance in medicine.

[45]  Wen-Ming Luh,et al.  Turbo ASL: Arterial spin labeling with higher SNR and temporal resolution , 2000 .