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Copyright © Adam Scott Bernstein 2019
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A Dissertation Submitted to the Faculty of the
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DEPARTMENT OF BIOMEDICAL ENGINEERING
DOCTOR OF PHILOSOPHY
2019
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As members of the Dissertation Committee, we certify that we have read the dissertation
prepared by Adam Scott Bernstein, titled Advanced Diffusion MRI Techniques:
Methodological Development and Clinical Application and recommend that it be
accepted as fulfilling the dissertation requirement for the Degree of Doctor of
Philosophy.
Date: 8 February 2019
'
Theodore P Trouard
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Date: 8 February 2019
Peter J Bassei
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Date: 8 February 2019
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Nan-kuei Chen
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Theodore P'rrouard
Date: 8 February 2019
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B Date: 8 February 2019
ation Directo : Peter
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3
STATEMENT BY AUTHOR
This dissertation has been submitted in partial fulfillment of the requirements for an ad-
vanced degree at the University of Arizona and is deposited in the University Library to
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be made available to borrowers under rules of the Library.
Brief quotations from this dissertation are allowable without special permission, provided
that accurate acknowledgment of the source is made. Requests for permission for ex-
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tended quotation from or reproduction of this manuscript in whole or in part may be
granted by the copyright holder.
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ACKNOWLEDGEMENTS
I would first and foremost like to thank my advisors, Drs. Ted Trouard and Peter Basser.
Dr. Trouard welcomed me into his lab as an undergraduate, and inspired me to remain
curious. Dr. Basser recruited me to spend part of my PhD training with him at the
National Institutes of Health. Dr. Basser took great interest in my personal, professional,
and academic growth, and has been a great source of support and encouragement for me.
I am also grateful to have worked under the mentorship of Dr. Alexandru Avram. Dr.
Avram’s technical proficiency and knowledge of MRI, along with his abounding knowl-
edge of UFC fighting and obscure foreign film made for very insightful and enlightening
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discussions.
Drs. Nan-kuei Chen and Ying-Hui Chou could not have come to Arizona at a better
time, and have been the embodiment of collaboration and inclusion. I am very grateful to
have worked (and to continue to work) with both Drs. Chen and Chou on both technical
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development and clinical applications of advanced imaging techniques.
I would like to thank the clinical collaborators involved in many of my projects, in-
cluding Dr. Duke Duncan, Dr. Craig Weinkauf, Dr. Gloria Guzman, Dr. Wei Zhou, and
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Dr. John Butman, for all of their clinical insights, and for providing the inspiration behind
many of the projects I was involved in.
I would like to thank Chidi Ugonna for his extensive technical support and enthusiasm.
I am grateful that a true computer expert was able to step in and clean up the many IT
issues that I created.
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Lastly, I would like to thank all of my friends and family for their ongoing support all
through this process. Their have been many obstacles, and unforeseen roadblocks, and
they were always there to comfort and support me. A special thanks to Hannah for her
patience, support and love.
5
DEDICATION
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TABLE OF CONTENTS
LIST OF FIGURES . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8
LIST OF TABLES . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 16
ABSTRACT . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 17
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1.1 The Origin of the Magnetic Resonance Signal . . . . . . . . . . . . . . . 20
1.2 The Bloch Equations . . . . . . . . . . . . . . . . . . . . . . . . . . . . 21
1.3 The Hahn Spin-Echo Experiment . . . . . . . . . . . . . . . . . . . . . . 25
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1.4 Diffusion Nuclear Magnetic Resonance . . . . . .
1.5 Magnetic Resonance Imaging . . . . . . . . . . . .
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1.6 Diffusion Imaging . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 43
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CHAPTER 2 Developments in Diffusion Data Processing and Analysis . . . . . 65
2.1 The Diffusion MRI Protocol . . . . . . . . . . . . . . . . . . . . . . . . 65
2.2 Diffusion MRI Artifacts and Their Correction . . . . . . . . . . . . . . . 67
2.3 Development of an Artifact Correction Pipeline . . . . . . . . . . . . . . 76
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REFERENCES . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 115
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B.2 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 158
B.3 Materials and Methods . . . . . . . . . . . . . . . . . . . . . . . . . . . 160
B.4 Results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 165
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B.5 Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 171
B.6 Appendix B.A The MAP MRI basis functions . . . . . . . . . . . . . . . 174
B.7 Appendix B.B Jensen-Shannon divergence for MAP propagators . . . . . 175
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APPENDIX C A diffusion-matched principal component analysis (DM-PCA) based
two-channel denoising procedure for high-resolution diffusion-weighted MRI . 178
C.1 Abstract . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 178
C.2 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 179
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LIST OF FIGURES
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along the x-axis, M ~ begins to nutate about the x-axis (B). If B ~ 1 is ap-
plied at exactly the Larmor frequency of the spins making up M ~,M ~ will
~
continue to nutate about the rotating B1 field until it is turned off. . . . . . 23
1.3 Graphical representation of the net magnetization, M
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nutating down into the x-y plane, represented in the rotating frame of
reference. In the rotating frame of reference, B~ 1 remains aligned with the
0
x axis, and M~ will lay along the y axis. . . . . . . . . . . . . . . . . . .
0
24
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1.4 Graphical representation of signal generation and reception in a typical
MRI experiment. In panel A, the net magnetization, M ~ , precesses in the
x-y plane after excitation, and generates a voltage (C) in a receiver coil (B). 24
1.5 Dephasing of spins due to magnetic field inhomogeneities shown in the
rotating frame of reference. The net transverse magnetization is depicted
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a single echo formation (bottom) over the same total experimental time.
The signal from the single echo experiment is significantly decreased due
to diffusion. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
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1.13 Pulse sequence diagram of the PGSE experiment. . . . . . . . . . . . . . 37
1.14 The expected signal modulation due to diffusion (top), expected root
mean square of the phase evolution (middle), and the pulsed diffusion
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encoding wave forms (bottom) for a standard PGSE NMR experiment. . . 38
1.15 Idealized gradient waveforms (left), and the k-space trajectory (right) for
a standard EPI readout. . . . . . . . . . . . . . . . . . . . . . . . . . . . 42
1.16 A full diffusion weighted imaging pulse sequence. The first section de-
picts a slice-selective excitation. Next, the excited magnetization is dif-
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fusion weighted using the PGSE scheme. Finally, the signal is spatially
encoded, and an image acquired using the EPI readout. . . . . . . . . . . 45
1.17 A simple in vivo example of fitting the diffusion coefficient, D, across an
entire image with several b-values collected. . . . . . . . . . . . . . . . . 46
1.18 Graphical representation of a diffusion tensor, with primary axes λ1 , λ2 ,
and λ3 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 47
1.19 Diffusion tensor shape as a function of increasing FA (left-right) and in-
creasing diffusivity (top-bottom). . . . . . . . . . . . . . . . . . . . . . . 49
1.20 DTI derived parameter maps. The directionally encoded color map (DEC)
(E) is red when water diffuses primarily along the x-axis, green when
water diffuses primarly along the y-axis, and blue primarily along the z-
axis, as indicated by the legend on the bottomr right. . . . . . . . . . . . 50
1.21 MAP basis functions in 2-dimensions in diffusion space. Red indicates
positive values, and blue indicates negative values. . . . . . . . . . . . . 54
1.22 Example parameter maps derived from MAP MRI. . . . . . . . . . . . . 56
1.23 Diffusion orientation distribution functions for each of the MAP-MRI ba-
sis functions up to order 4. . . . . . . . . . . . . . . . . . . . . . . . . . 57
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1.24 Fiber orientation distribution functions fit for every voxel in a brain. . . . 59
1.25 Spherical harmonic basis up to order four. The sphere is modulated by
the spherical harmonic amplitude for every θ and φ. Positive values are
shown in red, and negative values in blue. . . . . . . . . . . . . . . . . . 59
1.26 Apparent fiber density calculated for every lobe of the fODFs computed
previously. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 61
2.1 The effects of eddy currents are shown for a single line of data (red line in
image A) in B. As can be seen the edge of the brain appears to shift by 1-2
voxels for each diffusion image collected. After eddy current correction,
the edge of the brain is stable throughout the entire set of diffusion images
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(C), providing the required alignment for further processing. . . . . . . . 71
2.2 The effects of EPI distortion are shown in A and B above, where the phase
encoding direction has been reversed between the two images. In A, the
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PE direction is anterior to posterior, and leads to a compression of the
brain near the frontal sinuses. When the PE direction is reversed (B), the
brain is streched near the frontal sinuses. In C, the distortions have been
corrected by finding the midway point of images A and B. In panels D
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and E, the same brains from A and B are overlayed on an undistorted T1 -
weighted image. The white arrows point out regions where the brain is
obviously distorted relative to the anatomical reference, and in panel F,
the distortions are shown to be largely removed, leading to much better
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diffusion parameters within each of the ROIs defined in the ICBM DTI
atlas when measured prior to carotid endarcterectomy. The blue box and
whisker plots show the same information for the parameters measured 4-6
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months following the procedure. . . . . . . . . . . . . . . . . . . . . . . 94
3.6 Connectome edges that demonstrated statistically significant increases in
connectivity prior to multiple comparisons correction are highlighted in
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the images above. The left putamen (top row, red arrow) showed signif-
icant increases in structural connectivity with several regions. The right
superior temporal gyrus (bottoms row, red arrow) also demonstrated in-
creased connectivity with several regions nearby. . . . . . . . . . . . . . 95
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4.1 Crossover study design where group one receives the standard of care
therapy for 36 weeks followed by 12 weeks of intense therapy. Group
two receives 12 weeks of intense therapy first, followed by the standard
of care therapy. Imaging is performed at zero and 36 weeks, before group
one has undergone intense therapy. . . . . . . . . . . . . . . . . . . . . . 99
4.2 Schematic of the generation of along-tract DTI parameter profiles. First,
ROIs are drawn on the cerebral peduncle (top of step 1) and the internal
capsule (bottom of step 2). Then deterministic CSD-based tractography is
performed to identify the CSTs (2). Then maps of FA and RD are sampled
at 100 evenly spaced points along the length of the generated tractograms
(3). Finally the FA and RD are averaged across the width of the CST at
every sampled point to generate an along track profile (4). . . . . . . . . . 101
4.3 Line plots showing the change in GMFM scores at baseline and 36 week
followup. Subjects 3 and 5 are in group one, and subjects 1, 2, and 4 are
in group two. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 102
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prior to treatment (solid line) is shown in blue (dashed line is standard
deviation), and the along track FA following 36 weeks of treatment is
shown in red. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
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4.8 Along track RD measurements for all 5 enrolled subjects. Along track RD
prior to treatment (solid line) is shown in blue (dashed line is standard
deviation), and the along track RD following 36 weeks of treatment is
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shown in red. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 110
A.1 Visualization of the average parameter maps derived from DTI and MAP-
MRI for three different collection schemes. The top row are the maps de-
rived from the minimum TR (i.e. 3.7s) 3x MB sequence, followed by the
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A.3 Maps of the coefficient of variation of the parameter maps derived from
both DTI and MAP for all 3 collection schemes. The top row are the
maps derived from the minimum TR SMS sequence, followed by the 10
second TR SMS sequence, and finally the parameter maps derived from
the standard single band sequence with minimum TR for full brain coverage.152
A.4 Difference maps between the CVs of parameters derived from MB and SB
acquisitions. The top row shows the CV of the short TR MB (TR=3.7s)
derived parameter values subtracted from the CV of the SB derived pa-
rameter values. The bottom row shows the CV of the TR-matched MB
(TR=10.7s) derived parameter values subtracted from the CV of the SB
derived parameter values. All CV maps are plotted on the same scale,
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where red and yellow indicate that the MB CV is lower than the SB CV,
and blue indicates that the MB CV is larger than the SB CV. . . . . . . . 153
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B.1 A flowchart for spatial standardization of MAP MRI data and for con-
structing a population template of MAP MRI 3D diffusion propagators. . 160
B.2 Microstructural MAP MRI parameters computed from the template of 3D
diffusion propagators measured in a healthy population: DTI-parameters:
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mean diffusivity (MD), fractional anisotropy (FA), and direction encoded
color (DEC) map; along with MAP MRI microstructural parameters: the
Return-to-origin probability (RTOP), Propagator Anisotropy (PA), and
Non-Gaussianity (NG). . . . . . . . . . . . . . . . . . . . . . . . . . . . 167
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C.1 The schematic diagram of the new complex-domain DM-PCA based two-
channel denoising procedure. . . . . . . . . . . . . . . . . . . . . . . . . 183
C.2 Comparison of DWI denoising through filtering signals across nearest
neighboring voxels and diffusion-matched voxels: The red dot in (a)
shows a target voxel (displayed on top of mean DWI map), whose sig-
nals in 6-direction DWI scans are to be denoised. In many existing de-
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noising methods, signals of nearest neighboring voxels in a patch (see b)
are the input of a filtering procedure. In contrast, we identify a group
of voxels that demonstrate very similar signal variation patterns along
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the diffusion dimension but are not necessarily neighboring (see c) for
subsequent filtering procedures. Panels d, e and f show an input image,
nearest-neighboring PCA produced image, and DM-PCA produced im-
age, respectively. Residual maps obtained with nearest-neighboring PCA
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and DM-PCA methods are shown in panels g and h, respectively. . . . . . 184
C.3 A simulation study for comparing magnitude-domain DM-PCA and two-
channel complex-domain DM-PCA in terms of the accuracy in ADC
fitting: (a) Noise-free DWI data corresponding to b = 0, 200, 400 ...
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2200 (s/mm2). (b) DWI data affected by Rician noise. (c) DWI data
denoised by magnitude-domain DM-PCA. (d) DWI data denoised by a
two-channel complex-domain DM-PCA procedure. (e) Signal intensities
of noisy DWI data (solid curve in orange) and the ground truth (dashed
curve in blue). (f) Signal intensities of magnitude-domain DM-PCA pro-
duced data (solid curve in orange) and the ground truth (dashed curve in
blue). (g) Signal intensities of complex-domain DM-PCA produced data
(solid curve in orange) and the ground truth (dashed curve in blue). (h)
Errors in ADC fitting for data with different SNR levels. . . . . . . . . . 188
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curve in orange) and the ground truth (dashed curve in blue). (g) Signal
intensities of complex-domain DM-PCA produced data (solid curve in
orange) and the ground truth (dashed curve in blue). (h) Errors in ADC
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fitting for data with different SNR levels. . . . . . . . . . . . . . . . . . . 190
C.5 FA maps obtained from high-resolution DWI images (0.85 mm3 voxel
size), before and after DM-PCA based denoising, corresponding to dif-
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ferent SNR levels in input data. . . . . . . . . . . . . . . . . . . . . . . . 194
C.6 (a) and (b) show coronal-plane mean DWI and FA maps, respectively, de-
rived from high-resolution data after DM-PCA based denoising, with ar-
rows indicating the left hippocampus. The corresponding zoom-in images
shown in (c) and (d), respectively. The FA map derived from images with-
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LIST OF TABLES
B.1 The average standard deviation of PA (top row), NG (middle row) and
RTOP (bottom row) across all 50 WM ROIs and all 5 subjects in subject
space (left) and template space (middle). The difference is shown in the
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last column. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 168
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ABSTRACT
Diffusion magnetic resonance imaging (dMRI) has become a mainstay for better under-
standing the structure of the normal human brain, as well as for understanding the changes
that occur in disease. Using the motion of water as a probe for the microscopic environ-
ment of tissues, dMRI provides insight into the structure and organization of the brain.
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Diffusion tensor imaging (DTI), a dMRI provided the neuroimaging community with a
means of further characterizing the microstructure of the brain. Further, the macroscopic
structure of the brain can be characterized by means of tractography using DTI. While
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DTI provides a wealth of valuable information, measures of anisotropy and diffusivity
derived from DTI are often obscured by partial volume effects and complex neuronal
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fiber geometries. DTI further assumes that diffusion is gaussian, which is not the case in
the presence of barriers to diffusion, such as cell membranes and the extracellular matrix,
resulting in small errors and a diffusion time-dependence to the measures of anisotropy
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and diffusivity. More advanced frameworks for diffusion imaging, including mean appar-
ent propagator- (MAP) MRI, and constrained spherical deconvolution (CSD) are capable
of both resolving complex crossing fiber architectures, as well as better characterizing the
true, nongaussian nature of diffusion in tissue. In the following work, DTI, MAP-MRI,
and CSD are applied to cerebral palsy (CP) and carotid artery disease (CAD) in order to
better characterize the effects of intervention in children with CP and adults with CAD.
In the children with CP, we find that there are general structural changes in the corti-
cospinal tracts following 36 weeks of physical therapy, as well as a correlation between
the gross motor function measure (GMFM) and both FA and RD that may be trending
towards significance. In subjects with CAD, we find that 6 months following carotid en-
darcterectomy, a surgical procedure to remove the accumulated atherosclerotic placque
from the lining of the carotid artery, there are significant increases in the apparent fiber
density and structural connectivity largely in the ipsilateral hemisphere of the occluded
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artery. These works are preliminary, and require the inclusion of more subjects before
any major conlusions are drawn, but the results are compelling nonetheless.
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CHAPTER 1
Magnetic resonance imaging (MRI) has become a mainstay diagnostic tool in radiol-
ogy. The nuclear magnetic resonance (NMR) phenomenon was first observed in 1938 by
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Rabi et al. [1]. In 1946, Felix Bloch and Edward Purcell independently published works
demonstrating the measurement of the NMR phenomenon [2, 3], and Bloch’s 1946 arti-
cle introduced the Bloch equations that describe the NMR process. With the discovery of
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spin-echoes by Erwin Hahn in 1950 [4], the deleterious effects of diffusion on the NMR
signal were noted, and thus the field of diffusion NMR was born. The ability to measure
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the random diffusive motion of water proved to be a valuable tool for characterizing the
local microstructure that water is diffusing in. After contributions from Hahn Hahn [4],
Carr and Purcell Carr and Purcell [5], and others, the pulsed gradient spin-echo diffu-
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sion experiment was introduced by Stejskal and Tanner in 1965 [6]. In the mid 1980s,
Le Bihan and others proposed a method for imaging diffusion in humans as a means to
better understand the microscopic environment of tissue [7]. In the late 80s and early
90s, researchers began to suggest that anisotropic diffusion in the brain could be used
to better understand the general alignment of tissues. And finally, in 1994, Peter Basser
[8, 9] introduced the diffusion tensor as a means of mathematically characterizing the 3D
microstructure of tissue. While diffusion tensor imaging (DTI) remains the most popular
diffusion imaging technique in clinical research [10], new, more sophisticated techniques
such as q-ball imaging [11], constrained spherical deconvolution [12, 13], diffusion spec-
trum imaging [14], and mean apparent propagator MRI [15, 16] can provide additional
microstructural information. In this chapter, the physics of diffusion and MRI will be
introduced as a primer for the clinical applications of diffusion imaging presented in the
following chapters.
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All atomic and subatomic particles possess a property called spin. While the term spin
is somewhat misleading, as these particles are not actually spinning, a simple, classi-
cal physics representation provides a very straightforward description of the NMR phe-
nomenon. If a proton is represented as a spinning ball of charge (figure 1.1)[17, 18], then
one could expect that a tiny magnetic moment would be generated along its axis of rota-
tion. If this tiny magnetic moment is then placed in a much larger external magnetic field,
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it tends to align with the external magnetic field and begins precessing about the axis of
that field. The rate of precession is given by:
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ω0 = γB0 (1.1)
Placing many protons in this external field can generate a combined magnetic moment
large enough to produce a detectable signal. The magnitude of this measurable magnetic
moment, M ~ , is given by [19]:
2 2
|M~ |= ρ0 γ h̄ B0 (1.2)
4kB T
where ρ0 is the proton density, h̄ is Planck’s constant, kB is Boltzmann’s constant and T
is the temperature in Kelvin. From equation 1.2, the magnitude of the magnetic moment,
and therefore the measured signal, is proportional to B0 . Surprisingly, thermal energy,
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as measured by kB T , also acts to randomize spins in a static magnetic field, so a large
B0 is needed to align them. This explains why clinical MRI scanners use such high field
strengths, ranging from 1T - 7T, several tens of thousands of times stronger than the earths
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magnetic field.
The above description provides a simplified overview of a much more complicated
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quantum mechanical phenomenon that will not be discussed in this work for brevity.
While spin is a quantum mechanical property of atomic and subatomic particles, and the
interaction of individual particles with an external magnetic field is complex, the com-
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bined effect of a large ensemble of particles (e.g. 1018 hydrogen protons in 1 mm3 of
average tissue) results in a macroscopic magnetization that can be accurately and com-
pletely described using classical physics, first elucidated by Felix Bloch and described by
the famous Bloch equations.
In 1946, Felix Bloch introduced the equations of motion of nuclear magnetization, now
typically referred to as the Bloch equations [2]. These equations, shown below, are the
~ , with
basis of all MR techniques, and describe the interaction of the net magnetization, M
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~
an external magnetic field, B.
Mx − T12 γBz −γBy Mx 0
d
M = −γBz − 1
γBx My + 0 (1.3)
dt y T2
M0
Mz γBy −γBx − T11 Mz T1
The system of differential equations in 1.3 describe the evolution of the magnetization
~ in the presence of any external magnetic field as a result of exciting the system.
vector M
~ as spins
The relaxation time constants T1 and T2 are used to describe the change in M
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interact with their surroundings and release thermal energy (T1 or spin-lattice relaxation)
and as spins interact with one another, leading to an irreversible dephasing, or loss of co-
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herence among the excited spins (T2 or spin-spin relaxation). These relaxation processes
are fundamental to understanding and designing MR experiments, and play an important
role in the signal to noise ratio of diffusion NMR data, and are discussed in great detail in
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many other sources [19, 2, 18, 17].
Figure 1.2A illustrates the initial state of an NMR experiment, where a sample is placed
in an external magnetic field, B0 , oriented along the z-axis. At rest, the net magnetization,
M~ , is aligned with B0 . If an additional excitation field, B~1 , is introduced to the system,
initially aligned with the x-axis (Bx and By in equation 1.3 are made nonzero), a torque is
applied to M ~ , such that M
~ will nutate about the x-axis towards the x - y plane as shown
in figure 1.2B. If B~1 is applied at the resonant frequency of the system, ω0 , such that it is
circularly polarized, M ~ will continue to nutate, following a spiral trajectory as illustrated
in figure 1.2C.
~ with the net external magnetic field can be greatly
The analysis of the interaction of M
simplified by ignoring the effects of the static B0 field. This can be achieved by selecting
a frame of reference that rotates at the Larmor frequency, often called the rotating frame
of reference, whose coordinate axes are denoted as x0 , y 0 , and z 0 . In the rotating frame of
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~
circularly polarized RF excitation pulse. At rest, M is parallel to B0 (A). Immediately
after the application of a small magnetic field, B ~ 1 initially along the x-axis, M ~ begins to
~ 1 is applied at exactly the Larmor frequency of the spins
nutate about the x-axis (B). If B IE
~ ~
making up M , M will continue to nutate about the rotating B ~ 1 field until it is turned off.
only. The same excitation process is shown in figure 1.3, with the rotating frame of
reference. Here, the analysis of small deviations from the Larmor frequency are much
more apparent, and the math is simplified greatly. The duration and amplitude of the B~ 1
RF pulse determines the angle through which M0 is tipped, also called the flip angle (α):
Z τ
α=γ B1 (t)dt (1.5)
0
where τ is the duration of the RF pulse. For the majority of diffusion MRI experiments,
B~1 (t) is designed such that α = 90° .
~ now precessing about B0 in the x-y plane, there is a time-varying magnetic field,
With M
which can induce a voltage in a receiver coil (pick-up coil) according to Faraday’s law of