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Magnetic Resonance Microscopy: Recent Advances and Applications J Michael Tyszka, Scott E Fraser and Russell E Jacobs

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Magnetic Resonance Microscopy: Recent Advances and Applications J Michael Tyszka, Scott E Fraser and Russell E Jacobs Magnetic resonance microscopy: recent advances and applications J Michael Tyszka, Scott E Fraser and Russell E Jacobs Magnetic resonance microscopy is receiving increased as microscopy, but we will limit this review to organisms attention as more researchers in the biological sciences are and sample sizes less than a few centimeters across. turning to non-invasive imaging to characterize development, perturbations, phenotypes and pathologies in model MRI exploits the nuclear magnetism exhibited by certain organisms ranging from amphibian embryos to adult rodents nuclei such as 1H, 19F, 13C and 31P. By far the most and even plants. The limits of spatial resolution are being common nucleus visualized by MRI is 1H, with close to explored as hardware improvements address the need for 100% natural abundance and high magnetic resonance increased sensitivity. Recent developments include in vivo cell sensitivity. The composition of most biological tissue is tracking, restricted diffusion imaging, functional magnetic dominated by liquid water, and it is the difference in resonance microscopy and three-dimensional mouse atlases. water environment between different tissues that MRI Important applications are also being developed outside visualizes so effectively. biology in the fields of fluid mechanics, geology and chemistry. Both MRI and nuclear magnetic resonance (NMR) rely Addresses on the presence of a strong magnetic field to polarize the Biological Imaging Center, Division of Biology, California Institute of bulk nuclear magnetism in an object. A pulse of radio- Technology, 2Q Broad 114-96, 1200 East California Boulevard, frequency radiation perturbs the nuclear magnetization Pasadena, CA 91125, USA and allows a signal to be induced in a receiver coil. The Corresponding author: Tyszka, J Michael ([email protected]) Larmor relation (v = gB) between NMR precession fre- quency, v, gyromagnetic ratio, g, and magnetic field strength, B, is exploited to spatially resolve the nuclear Current Opinion in Biotechnology 2005, 16:93–99 magnetism within a sample. Pulsed magnetic field gra- This review comes from a themed issue on dients are combined with radiofrequency pulsing to Analytical biotechnology encode spatial position in the frequency and phase of Edited by Keith Wood and Dieter Klaubert the received signal, allowing reconstruction of a magnetic resonance image. See books by Haacke et al. [1] and Available online 8th December 2004 Callaghan [2] amongst others for detailed reviews of 0958-1669/$ – see front matter the principles of MRI. # 2005 Elsevier Ltd. All rights reserved. DOI 10.1016/j.copbio.2004.11.004 Perhaps the most important issue for MRM is the funda- mental limit to spatial resolution. Various authors have estimated the limit to be in the order of 1 mm for liquid Abbreviations water at room or physiological temperatures based on BOLD blood oxygenation level dependent arguments of molecular diffusion, T2 relaxation (an DSI diffusion spectrum imaging NMR signal decay mechanism), microscopic field inho- DTI diffusion tensor imaging fMRI functional magnetic resonance imaging mogeneity and the sensitivity of the NMR experiment to MRI magnetic resonance imaging diminishing numbers of nuclear spins [2]. MRM images are MRM magnetic resonance microscopy only rarely acquired at isotropic spatial resolutions less than NMR nuclear magnetic resonance 10 mm. In practice, the spatial resolution is limited by sensitivity factors, specifically the signal-to-noise ratio Introduction achievable in a given time. For in vivo imaging, the total Magnetic resonance imaging (MRI) is now well estab- imaging time is constrained by physiological tolerance and lished as the premier non-invasive imaging modality for anesthetic constraints. For in vitro and ex vivo samples, the central nervous system in humans. Magnetic reso- more mundane constraints, such as equipment schedules nance microscopy (MRM) has also seen a great deal of and system stability, limit practical imaging times. parallel development, with many of the advances in clinical MRI reapplied at smaller scales. The boundary There is a general consensus within the MRM commu- between MRI and MRM is relatively vague, with imaging nity that high-resolution imaging with spatial resolution at spatial resolutions in the order of 100 mm and smaller of less than 100 mm benefits from the use of high-field typically considered to be microscopy (Figure 1). By this magnets, with field strengths greater than 3 Tesla. The definition, some high-resolution MRI in humans qualifies primary benefit to MRM is an increase in the nuclear www.sciencedirect.com Current Opinion in Biotechnology 2005, 16:93–99 94 Analytical biotechnology Figure 1 (a) (b) Clinical MRI Magnetic resonance microscopy Human brain Mouse brain Frog embryo 75 µm 16 µm 1 mm cubic cubic cubic voxel voxel voxel 3 x 1019 water molecules/voxel 1 x 1016 1 x 1014 7 x 1014 detectable spins 9 x 1011 1 x 1010 Current Opinion in Biotechnology Comparison of (a) clinical MRI with (b) MRM. The key difference is in the spatial resolution, implied by the nominal volume element (voxel) dimension. The total number of nuclear spins available for imaging also decreases with voxel volume, but can be partly restored by increased magnetic field strength, which increases the fraction of spins that contribute to the MRM signal. The estimates of detectable spins in this figure are based on 3 Tesla and 37 8C for human brain, 9.4 Tesla and 37 8C for mouse brain and 11.7 Tesla and 15 8C for frog (Xenopus laevis) embryos. The number of detectable spins per voxel drops by almost five orders of magnitude between human brain MRI and frog embryo MRM, requiring significant hardware sensitivity increases to maintain signal-to-noise ratio. polarization fraction contributing to the image; however, Although this article is not an exhaustive review of the other factors, such as a general increase in the T1 relaxa- current MRM literature, it is intended to give the non- tion time, decrease in T2 and increased susceptibility- specialist reader a useful overview of current activity and based field inhomogeneity, are all confounding factors at key applications in this field. We have divided the review high field strengths. into sections covering what we consider to be the most significant areas of MRM research and development. There is less debate surrounding the use of high perfor- mance imaging gradient sets, where higher amplitude MRM of diffusion (T/m) and faster rate of change of gradient amplitude (slew MRM is capable of detecting and quantifying random rate in T/m/s) are almost always an advantage. Microscopy molecular motion within tissues and the molecular inter- gradient capabilities range upwards to 10 T/m allowing actions with restrictive or hindering boundaries. The high resolution and rapid imaging of small samples. popular diffusion tensor model of restricted diffusion (diffusion tensor imaging or DTI), although limited, As experiments approach the theoretical limits of spatial provides a convenient and often acceptable image of resolution in MRM, the need for increasingly sensitive the predominant structural directionality within a voxel radiofrequency coils becomes apparent. Various groups (i.e. three-dimensional volume element) [7] (Figure 2). have explored the use of microcoils (typically single or DTI has found application in studies of cerebral white multiple turn solenoids with dimensions significantly matter tracts, where axonal bundles and fascicles provide smaller than 1 mm) to increase sensitivity in very small a highly ordered and restrictive environment for water samples. Microcoils have been developed primarily for diffusion. High angular resolution diffusion (HARD) small sample NMR spectroscopy applications [3], but the imaging techniques, such as diffusion spectrum imaging highest resolution magnetic resonance images obtained (DSI), have been proposed to address some of the limita- have employed such designs [4,5,6]. tions of DTI, particularly where axonal fibers cross within Current Opinion in Biotechnology 2005, 16:93–99 www.sciencedirect.com Magnetic resonance microscopy Tyszka, Fraser and Jacobs 95 Figure 2 (a) (b) (c) Current Opinion in Biotechnology Diffusion tensor microscopy of a fixed mouse brain at a nominal 75 mm isotropic resolution demonstrates the high signal-to-noise ratio and tissue contrast capabilities of volumetric MR histology. (a) Isotropic diffusion-weighted images of the mouse brain demonstrate basic anatomical organization. (b) Corresponding map of fractional anisotropy reveals regions of highly directional tissue organization chiefly in the white matter tracts of the brain. (c) Cuboids representing the diffusion tensor are overlaid on an anatomic reference image to visualize the complex tissue organization of the hippocampus, cortex and white matter tracts. a voxel [8]. Taking its lead from human DTI and DSI (Figure 3). Tracking the migration and distribution of studies, diffusion MRM has been applied to brain devel- appropriately labeled progenitor, stem or immune cells opment in mice [9], dysmyelination models [10] and using MRM is also receiving considerable attention myocardial fiber structure [11]. [26,27]. Most MRM cell tracking has been developed using superparamagnetic iron oxide particles as T2* con- Functional MRI trast labels [28 ], although recent work suggests that T1 Functional MRI (fMRI) attempts to infer neuronal activ- agents such as Mn2+ might hold equal promise. The ity from changes in blood oxygenation level dependent evolving
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