Abstract
Underlying the exquisite soft tissue contrast provided by magnetic resonance imaging are the inherent biophysical processes of relaxation. Through the intricate relationships between tissue microstructure and biochemistry and the longitudinal and transverse relaxation rates, quantitative measurement of these relaxation parameters is informative of tissue change associated with disease, neural plasticity, and other biological processes. Quantitative imaging studies can further facilitate more detailed characterizations of tissue, providing a more direct link between modern MR imaging and classic histochemical and histological studies. In this chapter, we briefly review the biophysical basis of relaxation, introducing and focusing specifically on the T 1, T 2, and T 2 * relaxation times and detail some of the more widely used and clinically feasible techniques for their in vivo measurement. Methods for analyzing relaxation data are covered, and a summary of significant results from reported neuroimaging studies is provided. Finally, the combination of relaxation time data with other quantitative imaging data, including diffusion tensor and magnetization transfer, is examined, with the aim of providing more thorough characterization of brain tissue.
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References
Blinkov, S. M., Glezer, I. I. The Human Brain in Figures and Tables. New York, NY: A Quantitative Handbook. Plenum Press; 1968.
Damadian, R. V. Tumor detection by nuclear magnetic resonance. Science 1971;171:1151.
Rabi, I. I., Zacharias, J. R., Millman, S., Kusch, P. A new method of measuring the nuclear magnetic moment. Phys Rev 1938;53:318.
Bloembergen, N., Purcell, E. M., Pound, R. V. Relaxation effects in nuclear magnetic resonance absorption. Phys Rev 1948;73:679–715.
Stanisz, G. J., Odrobina, E. E., Pun, J., Escaravage, M., Graham, S. J. et al. T1,T2 relaxation and magnetization transfer in tissue at 3t. Magn Reson Med 2005;54: 507–512.
Bottomley, P. A., Hardy, C. J., Argersinger, R. E., Allen-Moore, G. A review of 1H nuclear magnetic resonance relaxation in pathology: Are T1 and T2 diagnostic? Med Phys 1987;14:1–37.
Paus, T., Collins, D. L., Evans, A. C., Leonard, G., Pike, B., Zijdenbos, A. Maturation of white matter in the human brain: A review of magnetic resonance studies. Brain Res Bull 2001;54:255–266.
Gelman, N., Ewing, J. R., Gorell, J. M., Spickler, E. M., Solomon, E. G. Interregional variation of longitudinal relaxation rates in human brain at 3.0t: Relation to estimated iron and water contents. Magn Reson Med 2001;45:71–79.
Gelman, N., Gorell, J. M., Barker, P. B., Savage, R. M., Spickler, E. M. et al. MR imaging of the human brain at 3.0t: Preliminary report on transverse relaxation rates and relation to estimated iron content. Radiology 1999;210:759–767.
Naoko, S., Sakai, O., Ozonoff, A., Jara, H. Relaxo-volumetric multispectral quantitative magnetic resonance imaging of the brain over the human lifespan: Global and regional aging patterns. Mag Reson Imaging 2009;27:895–906.
Williams, L. A., Gelman, N., Picot, P. A., Lee, D. S., Ewing, J. R. et al. Neonatal brain: regional variability of in vivo MR imaging relaxation rates at 3.0t – initial experience. Radiology 2005;235:595–603.
Hoque, R., Ledbetter, C., Gonzalez-Toledo, E., Misra, V., Menon, V. et al. The role of quantitative neuroimaging indices in the differentiation of ischemia from demyelination: An analytical study with case presentation. Int Rev Neurobiol 2007;79:491–519.
Li, Y., Srinivasan, R., Ratiney, H., Lu, Y., Chang, S. M., Nelson, S. J. Comparison of T1 and T2 metabolite relaxation times in glioma and normal brain at 3t. J Magn Reson Imaging 2008;28:342–350.
Carr, H. Y., Purcell, E. M. Effects of diffusion on free precession in nuclear magnetic resonance experiments. Phys Rev 1954;94: 630–638.
Meiboom, S., Gill, D. Modified spin-echo method for measuring nuclear relaxation times. Rev Sci Instrum 1958;29:688–691.
Whittall, K. P., MacKay, A. L., Li, D. K. B. Are mono-exponential fits to a few echoes sufficient to determine T2 relaxation for in vivo human brain? Magn Reson Med 1999;43:1255–1257.
Powell, M. J. D. A tolerant algorithm for linearly constrained optimization calculations. Math Programming 1989;45:547–566.
Nelder, J. A., Mead, R. A simplex method for function minimization. Comput J 1965;7:308–313.
Levenberg, K. A method for the solution of certain non-linear problems in least squares. Appl Math 1944;2:164–168.
Holland, J. H. Adaptation in Natural and Artificial Systems. Ann Arbor, MI: The University of Michigan Press; 1975.
Kirkpatrick, S., Gelatt, C. D., Vecchi, M. P. Optimization by simulated annealing. Science 1983;220:671–680.
Clerc, M., Kennedy, J. The particle swarm-explosion, stability, and convergence in a multidimensional complex space. IEEE Trans Evol Comput 2002;6:58–73.
Berger, M. F., Silverman, H. F. Microphone array optimization by stochastic region contraction. IEEE Trans Signal Proc 1991;38:2377–2386.
Look, D. C., Locker, D. R. Time saving in measurement of NMR and EPR relaxation times. Rev Sci Instrum 1970;41: 250–251.
Brix, G., Schad, L. R., Deimling, M., Lorenz, W. J. Fast and precise T1 imaging using a TOMROP sequence. Magn Reson Imaging 1990;8:351–356.
Henderson, E., McKinnon, G., Lee, T. Y., Rutt, B. K. A fast 3d look-locker method for volumetric T1 mapping. Magn Reson Imaging 1999;17:1163–1171.
Gai, N. D., Butman, J. A. Modulated repetition time look-locker (MORTLL): A method for rapid high resolution three-dimensional T1 mapping. J Magn Reson Imaging 2009;30:640–648.
Freeman, A. J., Gowland, P. A., Mansfield, P. Optimization of the ultrafast look-locker echo-planar imaging T1 mapping sequence. Magn Reson Med 1998;16:765–772.
Christensen, K. A., Grand, D. M., Schulman, E. M., Walling, C. Optimal determination of relaxation times of Fourier transform nuclear magnetic resonance. Determination of spin-lattive relaxation times in chemically polarized species. J Phys Chem 1974;78:1971–1977.
Homer, J., Beevers, M. S. A re-evaluation of a rapid ‘new’ method for determining NMR spin-lattice relaxation times. J Magn Reson 1985;63:287–297.
Wang, H. Z., Riederer, S. J., Lee, J. N. Optimizing the precision in T1 relaxation estimation using limited flip angles. Magn Reson Med 1987;5:399–416.
Homer, J., Roberts, J. K. Routine evaluation of mo ratios and T1 values from driven equilibrium NMR specta. J Magn Reson 1990;87:265–272.
Deoni, S. C. L., Rutt, B. K., Peters, T. M. Rapid combined T1 and T2 mapping using gradient recalled acquisition in the steady state. Magn Reson Med 2003;49: 515–526.
Deoni, S. C. L., Peters, T. M., Rutt, B. K. Determination of optimal angles for variable nutation proton magnetic spin-lattice, T1, and spin-spin, T2, relaxation times measurement. Magn Reson Med 2004;51: 194–199.
Chang, L. C., Koay, C. G., Basser, P. J., Pierpaoli, C. Linear least-squares method for unbiased estimation of T1 from SPGR signals. Magn Reson Med 2008;60:496–501.
Carr, H. Y. Steady-state free precession in nuclear magnetic resonance. Phys Rev 1958;112:1693–1701.
Hinshaw, W. S. Spin mapping: The application of moving gradients to NMR. Phys Lett A 1974;48:87–88.
Scheffler, K., Hennig, J. T1 quantification with inversion recovery truefisp. Magn Reson Med 2001;45:720–723.
Deimling, M., Heid, O. (1994). Magnetization Prepared True FISP Imaging. In: Proceedings of the 2nd annual meeting of the ISMRM. San Fransico, p. 495.
Schmitt, P., Griswold, M. A., Jakob, P. M., Kotas, M., Gulani, V. et al. Inversion recovery truefisp: Quantification of T1, T2 and spin density. Magn Reson Med 2004;51: 661–667.
Parker, G. J., Barker, G. J., Tofts, P. S. Accurate multislice gradient echo T1 measurement in the presence of non-ideal RF pulse shape and RF field nonuniformity. Magn Reson Med 2001;45:838–845.
Pauly, P., Le Roux, P., Nishimura, D., Macovski, A. Parameter relations for the shinnar-le roux selective excitation pulse design algorithm. IEEE Trans Med Imaging 1991;10:53–65.
Madhuranthakam, A. J., Busse, R. F., Brittain, J. H., Rofsky, N. M., Alsop, D. C. B1-insensitive fast spin-echo using adiabatic square wave enabling of the echo train (SWEET) excitation. Magn Reson Med 2008;59:1386–1393.
Garwood, M., Ugurbil, K., Rath, A. R., Bendall, M. R., Ross, B. D., Mitchell, S. L., Merkle, H. Magnetic resonance imaging with adiabatic pulses using a single surface coil for RF transmission and signal detection. Magn Reson Med 1989;9:25–34.
Insko, E. K., Bolinger, L. Mapping of the radiofrequency field. J Magn Reson Ser A 1993;103:82–85.
Jiru, F., Klose, U. Fast 3D radiofrequency field mapping using echo-planar imaging. Magn Reson Med 2006;56:1375–1379.
Morrell, G. R. A phase-sensitive method of flip angle mapping. Magn Reson Med 2008;60:889–894.
Cunningham, C. H., Pauly, J. M., Nayak, K. S. Saturated double-angle method for rapid B1+ mapping. Magn Reson Med 2006;55:1326–1333.
Deoni, S. C. L. High resolution T1 mapping of the brain at 3T with driven equilibrium single pulse observation of T1 with high-speed incorporation of RF field inhomogeneities (DESPOT1-HIFI). J Magn Reson Imaging 2007;26:1106–1111.
Katscher, U., Bornert, P. Parallel RF transmission in MRI. Nmr Biomed 2006;19:393–400.
Preibisch, C., Deichmann, R. Influence of RF spoiling on the stability and accuracy of T1 mapping based on spoiled FLASH with varying flip angles. Magn Reson Med 2009;61:125–135.
Freeman, R., Hill, H. D. W. Phase and intensity anomalies in Fourier transform NMR. J Magn Reson 1971;4:366–383.
Zur, Y., Wood, M. L., Neuringer, L. J. Motion-insensitive steady-state free precession imaging. Magn Reson Med 1990;16:444–459.
Deoni, S. C. L. Transverse relaxation time (T2) mapping in the brain with off-resonance correction using phase-cycled steady-state free precession imaging. J Magn Reson Imaging 2009;30:411–417.
MacKay, A., Laule, C., Vavasour, I., Bjarnason, T., Kolind, S., Madler, B. Insights into brain microstructure from the T2 distribution. Magn Reson Imaging 2006;24:515–525.
Kroeker, R. M., Henkelman, R. M. Analysis of biological NMR relaxation data with continuous distributions of relaxation times. J Magn Reson 1986;69:218–235.
Menon, R. S., Rusinko, M. S., Allen, P. S. Multiexponential proton relaxation in model cellular systems. Magn Reson Med 1991;20:196–213.
Whittal, K. P., MacKay, A. L., Graeb, D. A., Nugent, R. A., Li, D. K., Paty, D. W. In vivo measurement of T2 distributions and water contents in normal human brain. Magn Reson Med 1997;37:34–43.
Cheng, K. H. In vivo tissue characterization of human brain by chisquares parameter maps: Multiparameter proton T2-relaxation analysis. Magn Reson Imaging 1994;12:1099–1109.
Laule, C., Leung, E., Lis, D. K., Traboulsee, A. L., Paty, D. W. et al. Myelin water imaging in multiple sclerosis: Quantitative comparison with histopathology. Mult Scler 2006;12:747–753.
Flynn, S. W., Lang, D. J., MacKay, A. L., Goghari, V., Vavasoir, I. M. et al. Abnormalities of myelination in schizophrenia detected in vivo with MRI, and post-mortem with analysis of oligodendrocyte proteins. Mol Psychiatry 2003;8:811–820.
Zimmerman, J. R., Britten, W. E. Nuclear magnetic resonance studies in multiple phase systems: Lifetime of a water molecule in an adsorbing phase on a silica gel. J Phys Chem 1957;61:1328–1333.
Poon, C. S., Henkelman, R. M. Practical T2 quantitation for clinical applications. J Magn Reson Imaging 1992;2:541–553.
Du, Y. P., Chu, R., Hwang, D., Brown, M. S., Kleinschmidt-DeMasters, B. K. et al. Fast multislice mapping of the myelin water fraction using multicomponent analysis of T2* decay at 3t: A preliminary postmortem study. Magn Reson Med 2007;58:865–870.
Kreis, R., Fusch, C., Boesch, C. (1992). In vivo characterization of three water compartments in human white matter using a single voxel technique with short TE. In: Proceedings of the 11th Annual Meeting of SMRM, Berlin, Germany, p. 1963.
Spencer, R. G. S., Fishbein, K. W. Measurement of spin-lattice relaxation times and concentrations in systems with chemical exchange using the one-pulse sequence: Breakdown of the Ernst model for partial saturation in nuclear magnetic resonance spectroscopy. J Magn Reson 2000;142:120–135.
Deoni, S. C. L., Rutt, B. K., Arun, T., Pierpaoli, C., Jones, D. K. Gleaning multicomponent T1 and T2 information from steady-state imaging data. Magn Reson Med 2008;60:1372–1387.
Ashburner, J., Friston, K. J. Voxel-based morphometry – the methods. Neuroimage 2000;11:805–821.
Tosun, D., Rettmann, M. E., Han, X., Tao, X., Xu, C. et al. Cortical surface segmentation and mapping. Neuroimage 2004;23(S1):S108–S118.
Deoni, S. C. L., Williams, S. C. R., Jezzard, P., Suckling, J., Murphy, D. G., Jones, D. K. Standardized structural magnetic resonance imaging in multicentre studies using quantitative T1 and T2 imaging at 1.5T. Neuroimage 2008;40:662–671.
van Buchem, M. A., McGowan, J. C., Grossman, R. I. Magnetization transfer histogram methodology: Its clinical and neuropsychological correlates. Neurology 1999;53: S23–S28.
Jenkinson, M., Bannister, P. R., Brady, J. M. Improved optimization for the robust and fast linear registration and motion correction of brain images. Neuroimage 2002;17: 825–841.
Voormolem, E. H., Wei, C., Chow, E. W., Bassett, A. S., Mikulis, D. J., Crawley, A. P. Voxel-based morphometry and automated lobar volumetry: The trade-off between spatial scale and statistical correction. Neuroimage 2009;18 (ahead of print).
Catani, M., ffytche, D. H. The rises and falls of disconnection syndromes. Brain 2005;128:2224–2239.
Kanaan, R. A., Shergill, S. S., Barker, G. K., Catani, M., Ng, V. W. et al. Tract-specific anisotropy measurements in diffusion tensor imaging. Psychiatry Res 2006;146:73–82.
More, S., Oishi, K., Jiang, L., Li, X., Akhter, K. et al. Stereotactic white matter atlas based on diffusion tensor imaging in an ICBM template. Neuroimage 2008;40:570–582.
Catani, M., Thiebaut de Schotten, M. A diffusion tensor imaging tractography atlas for virtual in vivo dissections. Cortex 2009;44:1105–1132.
Basser, P. J. Inferring microstructural features and the physiological state of tissues from diffusion-weighted images. Nmr Biomed 1995;8:333–344.
Jones, D. K., Simmons, A., Williams, S. C., Horsfield, M. A. Non-invasive assessment of axonal fiber connectivity in the human brain via diffusion tensor MRI. Magn Reson Med 1999;42:37–41.
Bakshi, R., Thompson, A. J., Rocca, M. A., Pelletier, D., Dousset, V. et al. MRI in multiple sclerosis: Current status and future prospects. Lancet Neurol 2008;7:615–625.
Manfredonia, F., Ciccarelli, O., Khaleeli, Z., Tozer, D. J., Saste-Garriga, J. et al. Normal appearing brain T1 relaxation time predicts disability in early primary progressive multiple sclerosis. Arch Neurol 2007;64: 411–415.
Wang, Yi. Description of parallel imaging in MRI using multiple coils. Magn Reson Med 2000;44:495–499.
Deoni, S. C. L., Catani, M. Visualization of the deep cerebellar nuclei using quantitative T1 and rho magnetic resonance imaging at 3 Tesla. Neuroimage 2007;37:1260–1266.
Ffrench-Constant, C. Pathogenesis of multiple sclerosis. Lancet 1994;29:271–275.
Be, L. The histopathology of grey matter demyelination in multiple sclerosis. Acta Neurol Scand Suppl 2009;189:51–57.
Gasperini, C., Horsfield, M. A., Thorpe, J. W., Kidd, D., Barkr, G. J. et al. Macroscopic and microscopic assessments of disease burden by MRI in multiple sclerosis: Relationship to clinical parameters. J Magn Reson Imaging 1996;6:580–584.
Ropele, S., Strasser-Fuchs, S., Augustin, M. et al. A comparison of magnetization transfer ratio, magnetization transfer rate, and the native relaxation time of water protons related to relapsing-remit- ting multiple sclerosis. AJNR Am J Neuroradiol 2000;21:1885–1889.
Laule, C., Vavasour, I. M., Moore, G. R., Oger, J., Li, D. K., Paty, D. W., MacKay, A. L. Water content and myelin water fraction in multiple sclerosis. A T2 relaxation study. J Neurol 2004;251:284–293.
Laule, C., Vavasour, I. M., Kolind, S. H., Traboulsee, A. L., Moore, G. R. et al. Long T2 water in multiple sclerosis: What else can we learn from multi-echo T2 relaxation? J Neurol 2007;254:1579–1587.
Kolind, S. H., Laule, C., Vavasour, I. M., Li, D. K., Traboulsee, A. L. et al. Complementary information from multi-exponential T2 relaxation and diffusion tensor imaging reveals differences between multiple sclerosis lesions. Neuroimage 2008;40:77–85.
DeWitt, L. D., Kistler, J. P., Miller, D. C., Richardson, E. P., Buonanno, F. S. NMR-neuropathologic correlation in stroke. Stroke 1987;18:342–351.
Kaur, J., Tuor, U. I., Zhao, Z., Peterson, J., Jin, A. Y., Baber, P. A. Quantified T1 as an adjunct to apparent diffusion coefficient for early infarct detection: A high-field magnetic resonance study in a rat stroke model. Int J Stroke 2009;4:159–168.
Bernarding, J., Braud, J., Hohmann, J., Mansmann, U., Hoehn-Berlage, M. et al. Histogram-based characterization of healthy and ischemic brain tissues using multiparametric MR imaging including apparent diffusion coefficient maps and relaxometry. Magn Reson Med 2000;43:52–61.
Reutens, D. C., Stevens, J. M., Kingsley, D., Kendall, B., Mose- ley, I. et al. Reliability of visual inspection for the detection of volumetric hippocampal asymmetry. Neuroradiology 1996;38:221–225.
Jackson, G. D., Connelly, A., Duncan, J. S., Gruenewald, R. A., Gadian, D. G. Detection of hippocampal pathology in intractable partial epilepsy: Increased sensitivity with qualitative magnetic resonance T2 relaxometry. Neurology 1993;43:1793–1799.
Conlon, P., Trimble, M. R., Rogers, D., Callicot, C. Magnetic resonance imaging in epilepsy: A controlled study. Epilepsy Reson 1988;2:37–43.
Jack, C. R., Jr., Wengenack, T. M., Reyes, D. A., Garwood, M., Curran, G. L. et al. In vivo magnetic resonance microimaging of individual amyloid plaques in Alzheimer’s transgenic mice. J Neurosci 2005;25:10041–10048.
Schenck, J. F., Zimmerman, E. A. High-field magnetic resonance imaging of brain iron: Birth of a biomarker? NMR Biomed 2004;17:433–445.
Duan, J. H., Wang, H. Q., Xu, J., Lin, X., Chen, S. Q. et al. White matter damage of patients with Alzheimer’s disease correlated with decreased cognitive function. Surg Radiol Anat 2006;28:150–156.
Barkzokis, G., Lu, P. H., Mintz, J. Human brain myelination and amyloid beta deposition in Alzheimer’s disease. Alzheimers Dement 2007;3:122–125.
House, M. J., St. Pierre, T. G., Foster, J. K., Matrins, R. N., Clarnette, R. Quantitative MR imaging R2 relaxometry in elderly participants reporting memory loss. AJNR 2006;27:430–439.
Akshoomoff, N., Pierce, K., Courchesne, E. The neurobiological basis of autism from a developmental perspective. Dev Psychol 2002;14:613–634.
Saito, N., Sakai, O., Ozonoff, A., Jara, H. Relaxo-volumetric multispectral quantitative magnetic resonance imaging of the brain over the human lifespan: Global and regional aging patterns. Magn Reson Imaging 2009;27:895–906.
Acknowledgments
A special thanks is extended to those who provided clinical examples and imaging data used herein: Prof. Derek Jones, Dr. Shannon Kolind, Dr. Janneke Zinkstok, Dr. Marco Catani, Dr. Emma Burkus, Dr. Mark Richardson, Katrina McMullin, Catherine Traynor, and Sarah Kwan. A debt of gratitude is owed to Dr. David Lythgoe, Dr. Fernando Zelya, Astrid Pauls, and Katrina McMullen for proof reading and comments.
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Deoni, S.C. (2011). Magnetic Resonance Relaxation and Quantitative Measurement in the Brain. In: Modo, M., Bulte, J. (eds) Magnetic Resonance Neuroimaging. Methods in Molecular Biology, vol 711. Humana Press. https://doi.org/10.1007/978-1-61737-992-5_4
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