A ranking of diffusion MRI compartment models with in vivo human brain data
Purpose Diffusion magnetic resonance imaging (MRI) microstructure imaging provides a unique noninvasive probe into tissue microstructure. The technique relies on biophysically motivated mathematical models, relating microscopic tissue features to the magnetic resonance (MR) signal. This work aims to...
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| Vydané v: | Magnetic resonance in medicine Ročník 72; číslo 6; s. 1785 - 1792 |
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| Hlavní autori: | , , , , , , |
| Médium: | Journal Article |
| Jazyk: | English |
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United States
Blackwell Publishing Ltd
01.12.2014
Wiley Subscription Services, Inc BlackWell Publishing Ltd |
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| ISSN: | 0740-3194, 1522-2594, 1522-2594 |
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| Abstract | Purpose
Diffusion magnetic resonance imaging (MRI) microstructure imaging provides a unique noninvasive probe into tissue microstructure. The technique relies on biophysically motivated mathematical models, relating microscopic tissue features to the magnetic resonance (MR) signal. This work aims to determine which compartment models of diffusion MRI are best at describing measurements from in vivo human brain white matter.
Methods
Recent work shows that three compartment models, designed to capture intra‐axonal, extracellular, and isotropically restricted diffusion, best explain multi‐b‐value data sets from fixed rat corpus callosum. We extend this investigation to in vivo by using a live human subject on a clinical scanner. The analysis compares models of one, two, and three compartments and ranks their ability to explain the measured data. We enhance the original methodology to further evaluate the stability of the ranking.
Results
As with fixed tissue, three compartment models explain the data best. However, a clearer hierarchical structure and simpler models emerge. We also find that splitting the scanning into shorter sessions has little effect on the ranking of models, and that the results are broadly reproducible across sessions.
Conclusion
Three compartments are required to explain diffusion MR measurements from in vivo corpus callosum, which informs the choice of model for microstructure imaging applications in the brain. Magn Reson Med 72:1785–1792, 2014. © 2013 The authors. Magnetic Resonance in Medicine Published by Wiley Periodicals, Inc. on behalf of International Society of Medicine in Resonance. |
|---|---|
| AbstractList | Diffusion magnetic resonance imaging (MRI) microstructure imaging provides a unique noninvasive probe into tissue microstructure. The technique relies on biophysically motivated mathematical models, relating microscopic tissue features to the magnetic resonance (MR) signal. This work aims to determine which compartment models of diffusion MRI are best at describing measurements from in vivo human brain white matter.
Recent work shows that three compartment models, designed to capture intra-axonal, extracellular, and isotropically restricted diffusion, best explain multi-b-value data sets from fixed rat corpus callosum. We extend this investigation to in vivo by using a live human subject on a clinical scanner. The analysis compares models of one, two, and three compartments and ranks their ability to explain the measured data. We enhance the original methodology to further evaluate the stability of the ranking.
As with fixed tissue, three compartment models explain the data best. However, a clearer hierarchical structure and simpler models emerge. We also find that splitting the scanning into shorter sessions has little effect on the ranking of models, and that the results are broadly reproducible across sessions.
Three compartments are required to explain diffusion MR measurements from in vivo corpus callosum, which informs the choice of model for microstructure imaging applications in the brain. Purpose Diffusion magnetic resonance imaging (MRI) microstructure imaging provides a unique noninvasive probe into tissue microstructure. The technique relies on biophysically motivated mathematical models, relating microscopic tissue features to the magnetic resonance (MR) signal. This work aims to determine which compartment models of diffusion MRI are best at describing measurements from in vivo human brain white matter. Methods Recent work shows that three compartment models, designed to capture intra-axonal, extracellular, and isotropically restricted diffusion, best explain multi-b-value data sets from fixed rat corpus callosum. We extend this investigation to in vivo by using a live human subject on a clinical scanner. The analysis compares models of one, two, and three compartments and ranks their ability to explain the measured data. We enhance the original methodology to further evaluate the stability of the ranking. Results As with fixed tissue, three compartment models explain the data best. However, a clearer hierarchical structure and simpler models emerge. We also find that splitting the scanning into shorter sessions has little effect on the ranking of models, and that the results are broadly reproducible across sessions. Conclusion Three compartments are required to explain diffusion MR measurements from in vivo corpus callosum, which informs the choice of model for microstructure imaging applications in the brain. Magn Reson Med 72:1785-1792, 2014. copyright 2013 The authors. Magnetic Resonance in Medicine Published by Wiley Periodicals, Inc. on behalf of International Society of Medicine in Resonance. Purpose Diffusion magnetic resonance imaging (MRI) microstructure imaging provides a unique noninvasive probe into tissue microstructure. The technique relies on biophysically motivated mathematical models, relating microscopic tissue features to the magnetic resonance (MR) signal. This work aims to determine which compartment models of diffusion MRI are best at describing measurements from in vivo human brain white matter. Methods Recent work shows that three compartment models, designed to capture intra-axonal, extracellular, and isotropically restricted diffusion, best explain multi-b-value data sets from fixed rat corpus callosum. We extend this investigation to in vivo by using a live human subject on a clinical scanner. The analysis compares models of one, two, and three compartments and ranks their ability to explain the measured data. We enhance the original methodology to further evaluate the stability of the ranking. Results As with fixed tissue, three compartment models explain the data best. However, a clearer hierarchical structure and simpler models emerge. We also find that splitting the scanning into shorter sessions has little effect on the ranking of models, and that the results are broadly reproducible across sessions. Conclusion Three compartments are required to explain diffusion MR measurements from in vivo corpus callosum, which informs the choice of model for microstructure imaging applications in the brain. Magn Reson Med 72:1785-1792, 2014. © 2013 The authors. Magnetic Resonance in Medicine Published by Wiley Periodicals, Inc. on behalf of International Society of Medicine in Resonance. Diffusion magnetic resonance imaging (MRI) microstructure imaging provides a unique noninvasive probe into tissue microstructure. The technique relies on biophysically motivated mathematical models, relating microscopic tissue features to the magnetic resonance (MR) signal. This work aims to determine which compartment models of diffusion MRI are best at describing measurements from in vivo human brain white matter.PURPOSEDiffusion magnetic resonance imaging (MRI) microstructure imaging provides a unique noninvasive probe into tissue microstructure. The technique relies on biophysically motivated mathematical models, relating microscopic tissue features to the magnetic resonance (MR) signal. This work aims to determine which compartment models of diffusion MRI are best at describing measurements from in vivo human brain white matter.Recent work shows that three compartment models, designed to capture intra-axonal, extracellular, and isotropically restricted diffusion, best explain multi-b-value data sets from fixed rat corpus callosum. We extend this investigation to in vivo by using a live human subject on a clinical scanner. The analysis compares models of one, two, and three compartments and ranks their ability to explain the measured data. We enhance the original methodology to further evaluate the stability of the ranking.METHODSRecent work shows that three compartment models, designed to capture intra-axonal, extracellular, and isotropically restricted diffusion, best explain multi-b-value data sets from fixed rat corpus callosum. We extend this investigation to in vivo by using a live human subject on a clinical scanner. The analysis compares models of one, two, and three compartments and ranks their ability to explain the measured data. We enhance the original methodology to further evaluate the stability of the ranking.As with fixed tissue, three compartment models explain the data best. However, a clearer hierarchical structure and simpler models emerge. We also find that splitting the scanning into shorter sessions has little effect on the ranking of models, and that the results are broadly reproducible across sessions.RESULTSAs with fixed tissue, three compartment models explain the data best. However, a clearer hierarchical structure and simpler models emerge. We also find that splitting the scanning into shorter sessions has little effect on the ranking of models, and that the results are broadly reproducible across sessions.Three compartments are required to explain diffusion MR measurements from in vivo corpus callosum, which informs the choice of model for microstructure imaging applications in the brain.CONCLUSIONThree compartments are required to explain diffusion MR measurements from in vivo corpus callosum, which informs the choice of model for microstructure imaging applications in the brain. Purpose Diffusion magnetic resonance imaging (MRI) microstructure imaging provides a unique noninvasive probe into tissue microstructure. The technique relies on biophysically motivated mathematical models, relating microscopic tissue features to the magnetic resonance (MR) signal. This work aims to determine which compartment models of diffusion MRI are best at describing measurements from in vivo human brain white matter. Methods Recent work shows that three compartment models, designed to capture intra‐axonal, extracellular, and isotropically restricted diffusion, best explain multi‐b‐value data sets from fixed rat corpus callosum. We extend this investigation to in vivo by using a live human subject on a clinical scanner. The analysis compares models of one, two, and three compartments and ranks their ability to explain the measured data. We enhance the original methodology to further evaluate the stability of the ranking. Results As with fixed tissue, three compartment models explain the data best. However, a clearer hierarchical structure and simpler models emerge. We also find that splitting the scanning into shorter sessions has little effect on the ranking of models, and that the results are broadly reproducible across sessions. Conclusion Three compartments are required to explain diffusion MR measurements from in vivo corpus callosum, which informs the choice of model for microstructure imaging applications in the brain. Magn Reson Med 72:1785–1792, 2014. © 2013 The authors. Magnetic Resonance in Medicine Published by Wiley Periodicals, Inc. on behalf of International Society of Medicine in Resonance. |
| Author | Zhang, Hui Ferizi, Uran Wheeler-Kingshott, Claudia A. M. Schneider, Torben Alexander, Daniel C. Panagiotaki, Eleftheria Nedjati-Gilani, Gemma |
| Author_xml | – sequence: 1 givenname: Uran surname: Ferizi fullname: Ferizi, Uran email: uran.ferizi.10@ucl.ac.uk organization: Department of Computer Science and Centre for Medical Image Computing, University College London, London, UK – sequence: 2 givenname: Torben surname: Schneider fullname: Schneider, Torben organization: NMR Research Unit, Department of Neuroinflammation, Institute of Neurology, University College London, London, UK – sequence: 3 givenname: Eleftheria surname: Panagiotaki fullname: Panagiotaki, Eleftheria organization: Department of Computer Science and Centre for Medical Image Computing, University College London, London, UK – sequence: 4 givenname: Gemma surname: Nedjati-Gilani fullname: Nedjati-Gilani, Gemma organization: Department of Computer Science and Centre for Medical Image Computing, University College London, London, UK – sequence: 5 givenname: Hui surname: Zhang fullname: Zhang, Hui organization: Department of Computer Science and Centre for Medical Image Computing, University College London, London, UK – sequence: 6 givenname: Claudia A. M. surname: Wheeler-Kingshott fullname: Wheeler-Kingshott, Claudia A. M. organization: NMR Research Unit, Department of Neuroinflammation, Institute of Neurology, University College London, London, UK – sequence: 7 givenname: Daniel C. surname: Alexander fullname: Alexander, Daniel C. organization: Department of Computer Science and Centre for Medical Image Computing, University College London, London, UK |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/24347370$$D View this record in MEDLINE/PubMed |
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| Copyright | 2013 The Authors. Magnetic Resonance in Medicine published by Wiley Periodicals, Inc. on behalf of International Society of Medicine in Resonance. 2014 Wiley Periodicals, Inc. 2013 The Authors. Magnetic Resonance in Medicine published by Wiley Periodicals, Inc. on behalf of International Society of Medicine in Resonance. 2013 |
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| Keywords | brain imaging white matter diffusion magnetic resonance imaging microstructure imaging |
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| References_xml | – reference: Assaf Y, Blumenfeld-Katzir T, Yovel Y, Basser PJ. AxCaliber: a method for measuring axon diameter distribution from diffusion MRI. Magn Reson Med 2008;59:1347-1354. – reference: Stanisz GJ, Szafer A, Wright GA, Henkelman M. An analytical model of restricted diffusion in bovine optic nerve. Magn Reson Med 1997;37:103-111. – reference: Schwarz G. Estimating the dimension of a model. Ann Stat 1978;6:461-464. – reference: Sotiropoulos S, Behrens TE, Jbabdi S. Ball and rackets: inferring fibre fanning from diffusion-weighted MRI. Neuroimage 2012;60:1412-1425. – reference: Jones DK, Basser PJ. Squashing peanuts and smashing pumpkins: how noise distorts diffusion-weighted MR data. Magn Reson Med 2004;52:979-993. – reference: Zhang H, Schneider T, Wheeler-Kingshott CA, Alexander DC. NODDI: practical in vivo neurite orientation dispersion and density imaging of the human brain. Neuroimage 2012;61:1000-1016. – reference: Basser PJ, Mattiello J, LeBihan D. Estimation of the effective self-diffusion tensor from the NMR spin echo. J Magn Reson 1994;103:247-254. – reference: Barazany D, Basser PJ, Assaf Y. In vivo measurement of axon diameter distribution in the corpus callosum of rat brain. Brain 2009;132:1210-1220. – reference: Assaf Y, Freidlin RZ, Rohde GK, Basser PJ. New modeling and experimental framework to characterize hindered and restricted water diffusion in brain white matter. Magn Reson Med 2004;52:965-978. – reference: Dyrby TB, Soegaard LV, Hall MG, Ptito M, Alexander DC. Contrast and stability of the axon diameter index from microstructure imaging with diffusion MRI. Magn Reson Med 2012;10:1522-2594. – reference: Wilm BJ, Svensson J, Henning A, Pruessmann KP, Boesiger P, Kollias SS. Reduced field-of-view MRI using outer volume suppression for spinal cord diffusion imaging. Magn Reson Med 2007;57:625-630. – reference: Alexander DC. A general framework for experiment design in diffusion MRI and its application in measuring direct tissue-microstructure features. Magn Reson Med 2008;60:439-448. – reference: Behrens TE, Woolrich MW, Jenkinson M, Johansen-Berg H, Nunes RG, Clare S, Matthews PM, Brady JM, Smith SM. Characterization and propagation of uncertainty in diffusion-weighted MR imaging. Magn Reson Med 2003;50:1077-1088. – reference: Zhang H, Hubbard PL, Parker GJM, Alexander DC. Axon diameter mapping in the presence of orientation dispersion with diffusion MRI. Neuroimage 2011;56:1301-1315. – reference: Tanner JE, Stejskal EO. Restricted self-diffusion of protons in colloidal systems by pulsed-gradient spin echo method. J Chem Phys 1968;49:1768. – reference: Alexander DC, Hubbard PL, Hall MG, Moore EA, Ptito M, Parker GJM, Dyrby TB. Orientationally invariant indices of axon diameter and density from diffusion MRI. Neuroimage 2010;52:1374-1389. – reference: Nilsson M, Lätt J, Ståhlberg F, van Westen D, Hagslätt H. The importance of axonal undulation in diffusion MR measurements: a Monte Carlo simulation study. NMR Biomed 2012;25:795-805. – reference: Panagiotaki E, Schneider T, Siow B, Hall MG, Lythgoe MF, Alexander DC. Compartment models of the diffusion MR signal in brain white matter: a taxonomy and comparison. Neuroimage 2012;59:2241-2254. – reference: Sotak CH. The role of diffusion tensor imaging in the evaluation of ischaemic brain injury: a review. NMR Biomed 2002;15:561-569. – reference: Efron B. Bootstrap methods: another look at the jackknife. Ann Stat 1979;7:1-26. – reference: Beaulieu C. The basis of anisotropic water diffusion in the nervous system-a technical review. NMR Biomed 2002;15:435-455. – reference: Shepherd TM, Thelwall PE, Stanisz GJ, Blackband SJ. Aldehyde fixative solutions alter the water relaxation and diffusion properties of nervous tissue. Magn Reson Med 2009;62:26-34. – volume: 61 start-page: 1000 year: 2012 end-page: 1016 article-title: NODDI: practical in vivo neurite orientation dispersion and density imaging of the human brain publication-title: Neuroimage – volume: 25 start-page: 795 year: 2012 end-page: 805 article-title: The importance of axonal undulation in diffusion MR measurements: a Monte Carlo simulation study publication-title: NMR Biomed – volume: 15 start-page: 435 year: 2002 end-page: 455 article-title: The basis of anisotropic water diffusion in the nervous system—a technical review publication-title: NMR Biomed – volume: 10 start-page: 1522 year: 2012 end-page: 2594 article-title: Contrast and stability of the axon diameter index from microstructure imaging with diffusion MRI publication-title: Magn Reson Med – volume: 59 start-page: 2241 year: 2012 end-page: 2254 article-title: Compartment models of the diffusion MR signal in brain white matter: a taxonomy and comparison publication-title: Neuroimage – volume: 52 start-page: 1374 year: 2010 end-page: 1389 article-title: Orientationally invariant indices of axon diameter and density from diffusion MRI publication-title: Neuroimage – volume: 7 start-page: 1 year: 1979 end-page: 26 article-title: Bootstrap methods: another look at the jackknife publication-title: Ann Stat – volume: 59 start-page: 1347 year: 2008 end-page: 1354 article-title: AxCaliber: a method for measuring axon diameter distribution from diffusion MRI publication-title: Magn Reson Med – volume: 60 start-page: 439 year: 2008 end-page: 448 article-title: A general framework for experiment design in diffusion MRI and its application in measuring direct tissue‐microstructure features publication-title: Magn Reson Med – volume: 50 start-page: 1077 year: 2003 end-page: 1088 article-title: Characterization and propagation of uncertainty in diffusion‐weighted MR imaging publication-title: Magn Reson Med – volume: 132 start-page: 1210 year: 2009 end-page: 1220 article-title: In vivo measurement of axon diameter distribution in the corpus callosum of rat brain publication-title: Brain – volume: 49 start-page: 1768 year: 1968 article-title: Restricted self‐diffusion of protons in colloidal systems by pulsed‐gradient spin echo method publication-title: J Chem Phys – start-page: 3 year: 2009 end-page: 20 – volume: 15 start-page: 561 year: 2002 end-page: 569 article-title: The role of diffusion tensor imaging in the evaluation of ischaemic brain injury: a review publication-title: NMR Biomed – volume: 60 start-page: 1412 year: 2012 end-page: 1425 article-title: Ball and rackets: inferring fibre fanning from diffusion‐weighted MRI publication-title: Neuroimage – volume: 62 start-page: 26 year: 2009 end-page: 34 article-title: Aldehyde fixative solutions alter the water relaxation and diffusion properties of nervous tissue publication-title: Magn Reson Med – volume: 37 start-page: 103 year: 1997 end-page: 111 article-title: An analytical model of restricted diffusion in bovine optic nerve publication-title: Magn Reson Med – volume: 57 start-page: 625 year: 2007 end-page: 630 article-title: Reduced field‐of‐view MRI using outer volume suppression for spinal cord diffusion imaging publication-title: Magn Reson Med – volume: 103 start-page: 247 year: 1994 end-page: 254 article-title: Estimation of the effective self‐diffusion tensor from the NMR spin echo publication-title: J Magn Reson – volume: 52 start-page: 965 year: 2004 end-page: 978 article-title: New modeling and experimental framework to characterize hindered and restricted water diffusion in brain white matter publication-title: Magn Reson Med – volume: 52 start-page: 979 year: 2004 end-page: 993 article-title: Squashing peanuts and smashing pumpkins: how noise distorts diffusion‐weighted MR data publication-title: Magn Reson Med – volume: 6 start-page: 461 year: 1978 end-page: 464 article-title: Estimating the dimension of a model publication-title: Ann Stat – volume: 56 start-page: 1301 year: 2011 end-page: 1315 article-title: Axon diameter mapping in the presence of orientation dispersion with diffusion MRI publication-title: Neuroimage – ident: e_1_2_5_3_1 doi: 10.1002/nbm.786 – ident: e_1_2_5_5_1 doi: 10.1002/mrm.10609 – ident: e_1_2_5_20_1 doi: 10.1016/j.neuroimage.2012.03.072 – ident: e_1_2_5_2_1 doi: 10.1006/jmrb.1994.1037 – ident: e_1_2_5_25_1 doi: 10.1063/1.1670306 – ident: e_1_2_5_12_1 doi: 10.1016/j.neuroimage.2011.09.081 – ident: e_1_2_5_17_1 doi: 10.1002/mrm.20283 – ident: e_1_2_5_6_1 doi: 10.1002/mrm.20274 – ident: e_1_2_5_11_1 doi: 10.1016/j.neuroimage.2011.01.084 – ident: e_1_2_5_24_1 doi: 10.1002/mrm.21646 – ident: e_1_2_5_8_1 doi: 10.1093/brain/awp042 – ident: e_1_2_5_22_1 doi: 10.1002/nbm.782 – ident: e_1_2_5_4_1 doi: 10.1002/mrm.1910370115 – ident: e_1_2_5_18_1 doi: 10.1214/aos/1176344136 – ident: e_1_2_5_9_1 doi: 10.1016/j.neuroimage.2010.05.043 – ident: e_1_2_5_15_1 doi: 10.1002/mrm.21167 – ident: e_1_2_5_19_1 doi: 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Diffusion magnetic resonance imaging (MRI) microstructure imaging provides a unique noninvasive probe into tissue microstructure. The technique relies... Diffusion magnetic resonance imaging (MRI) microstructure imaging provides a unique noninvasive probe into tissue microstructure. The technique relies on... Purpose Diffusion magnetic resonance imaging (MRI) microstructure imaging provides a unique noninvasive probe into tissue microstructure. The technique relies... |
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| SubjectTerms | Body Water - metabolism Brain - anatomy & histology Brain - metabolism brain imaging Computer Processing and Modeling—Note Computer Simulation Diffusion diffusion magnetic resonance imaging Diffusion Magnetic Resonance Imaging - methods Humans Image Interpretation, Computer-Assisted - methods microstructure imaging Models, Neurological Reproducibility of Results Sensitivity and Specificity white matter |
| Title | A ranking of diffusion MRI compartment models with in vivo human brain data |
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