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Published in: Brain Structure and Function 6/2018

01-07-2018 | Original Article

When tractography meets tracer injections: a systematic study of trends and variation sources of diffusion-based connectivity

Authors: Dogu Baran Aydogan, Russell Jacobs, Stephanie Dulawa, Summer L. Thompson, Maite Christi Francois, Arthur W. Toga, Hongwei Dong, James A. Knowles, Yonggang Shi

Published in: Brain Structure and Function | Issue 6/2018

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Abstract

Tractography is a powerful technique capable of non-invasively reconstructing the structural connections in the brain using diffusion MRI images, but the validation of tractograms is challenging due to lack of ground truth. Owing to recent developments in mapping the mouse brain connectome, high-resolution tracer injection-based axonal projection maps have been created and quickly adopted for the validation of tractography. Previous studies using tracer injections mainly focused on investigating the match in projections and optimal tractography protocols. Being a complicated technique, however, tractography relies on multiple stages of operations and parameters. These factors introduce large variabilities in tractograms, hindering the optimization of protocols and making the interpretation of results difficult. Based on this observation, in contrast to previous studies, in this work we focused on quantifying and ranking the amount of performance variation introduced by these factors. For this purpose, we performed over a million tractography experiments and studied the variability across different subjects, injections, anatomical constraints and tractography parameters. By using N-way ANOVA analysis, we show that all tractography parameters are significant and importantly performance variations with respect to the differences in subjects are comparable to the variations due to tractography parameters, which strongly underlines the importance of fully documenting the tractography protocols in scientific experiments. We also quantitatively show that inclusion of anatomical constraints is the most significant factor for improving tractography performance. Although this critical factor helps reduce false positives, our analysis indicates that anatomy-informed tractography still fails to capture a large portion of axonal projections.
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Literature
go back to reference Aganj I, Lenglet C, Sapiro G, Yacoub E, Ugurbil K, Harel N (2010) Reconstruction of the orientation distribution function in single-and multiple-shell q-ball imaging within constant solid angle. Magn Reson Med 64(2):554–566PubMedPubMedCentral Aganj I, Lenglet C, Sapiro G, Yacoub E, Ugurbil K, Harel N (2010) Reconstruction of the orientation distribution function in single-and multiple-shell q-ball imaging within constant solid angle. Magn Reson Med 64(2):554–566PubMedPubMedCentral
go back to reference Albi A, Meola A, Zhang F, Kahali P, Rigolo L, Tax CMW, Ciris PA, Essayed WI, Unadkat P, Norton I, Rathi Y, Olubiyi O, Golby AJ, O’Donnell LJ (2018) Image registration to compensate for EPI distortion in patients with brain tumors: an evaluation of tract-specific effects. J Neuroimag. https://doi.org/10.1111/jon.12485 CrossRef Albi A, Meola A, Zhang F, Kahali P, Rigolo L, Tax CMW, Ciris PA, Essayed WI, Unadkat P, Norton I, Rathi Y, Olubiyi O, Golby AJ, O’Donnell LJ (2018) Image registration to compensate for EPI distortion in patients with brain tumors: an evaluation of tract-specific effects. J Neuroimag. https://​doi.​org/​10.​1111/​jon.​12485 CrossRef
go back to reference Avants BB, Tustison NJ, Song G, Cook PA, Klein A, Gee JC (2011) A reproducible evaluation of ANTs similarity metric performance in brain image registration. Neuroimage 54(3):2033–2044CrossRefPubMed Avants BB, Tustison NJ, Song G, Cook PA, Klein A, Gee JC (2011) A reproducible evaluation of ANTs similarity metric performance in brain image registration. Neuroimage 54(3):2033–2044CrossRefPubMed
go back to reference Aydogan DB, Shi Y (2016) Probabilistic tractography for topographically organized connectomes. In: Ourselin S, Joskowicz L, Sabuncu MR, Unal G, Wells W (eds) Medical image computing and computer-assisted intervention—MICCAI 2016: 19th international conference, Athens, Greece, October 17–21, 2016, Proceedings, Part I. Springer International Publishing, Cham, pp 201–209. https://doi.org/10.1007/978-3-319-46720-7_24 CrossRef Aydogan DB, Shi Y (2016) Probabilistic tractography for topographically organized connectomes. In: Ourselin S, Joskowicz L, Sabuncu MR, Unal G, Wells W (eds) Medical image computing and computer-assisted intervention—MICCAI 2016: 19th international conference, Athens, Greece, October 17–21, 2016, Proceedings, Part I. Springer International Publishing, Cham, pp 201–209. https://​doi.​org/​10.​1007/​978-3-319-46720-7_​24 CrossRef
go back to reference Bach M, Fritzsche KH, Stieltjes B, Laun FB (2014) Investigation of resolution effects using a specialized diffusion tensor phantom. Magn Reson Med 71(3):1108–1116CrossRefPubMed Bach M, Fritzsche KH, Stieltjes B, Laun FB (2014) Investigation of resolution effects using a specialized diffusion tensor phantom. Magn Reson Med 71(3):1108–1116CrossRefPubMed
go back to reference Basser PJ, Pajevic S, Pierpaoli C, Duda J, Aldroubi A (2000) In vivo fiber tractography using DT-MRI data. Magn Reson Med 44(4):625–632CrossRefPubMed Basser PJ, Pajevic S, Pierpaoli C, Duda J, Aldroubi A (2000) In vivo fiber tractography using DT-MRI data. Magn Reson Med 44(4):625–632CrossRefPubMed
go back to reference Besseling RM, Jansen JF, Overvliet GM, Vaessen MJ, Braakman HM, Hofman PA, Aldenkamp AP, Backes WH (2012) Tract specific reproducibility of tractography based morphology and diffusion metrics. PloS one 7(4):e34125CrossRefPubMedPubMedCentral Besseling RM, Jansen JF, Overvliet GM, Vaessen MJ, Braakman HM, Hofman PA, Aldenkamp AP, Backes WH (2012) Tract specific reproducibility of tractography based morphology and diffusion metrics. PloS one 7(4):e34125CrossRefPubMedPubMedCentral
go back to reference Calabrese E, Badea A, Cofer G, Qi Y, Johnson GA (2015) A diffusion MRI tractography connectome of the mouse brain and comparison with neuronal tracer data. Cereb Cortex 25:bhv121CrossRef Calabrese E, Badea A, Cofer G, Qi Y, Johnson GA (2015) A diffusion MRI tractography connectome of the mouse brain and comparison with neuronal tracer data. Cereb Cortex 25:bhv121CrossRef
go back to reference Calamante F, Tournier J-D, Kurniawan ND, Yang Z, Gyengesi E, Galloway GJ, Reutens DC, Connelly A (2012) Super-resolution track-density imaging studies of mouse brain: comparison to histology. Neuroimage 59(1):286–296CrossRefPubMed Calamante F, Tournier J-D, Kurniawan ND, Yang Z, Gyengesi E, Galloway GJ, Reutens DC, Connelly A (2012) Super-resolution track-density imaging studies of mouse brain: comparison to histology. Neuroimage 59(1):286–296CrossRefPubMed
go back to reference Campbell JS, Savadjiev P, Siddiqi K, Pike GB (2006) Validation and regularization in diffusion MRI tractography. In: 3rd IEEE International Symposium on Biomedical Imaging: Nano to Macro, 2006. IEEE, pp 351–354 Campbell JS, Savadjiev P, Siddiqi K, Pike GB (2006) Validation and regularization in diffusion MRI tractography. In: 3rd IEEE International Symposium on Biomedical Imaging: Nano to Macro, 2006. IEEE, pp 351–354
go back to reference Chen H, Liu T, Zhao Y, Zhang T, Li Y, Li M, Zhang H, Kuang H, Guo L, Tsien JZ (2015a) Optimization of large-scale mouse brain connectome via joint evaluation of DTI and neuron tracing data. NeuroImage 115:202–213CrossRefPubMed Chen H, Liu T, Zhao Y, Zhang T, Li Y, Li M, Zhang H, Kuang H, Guo L, Tsien JZ (2015a) Optimization of large-scale mouse brain connectome via joint evaluation of DTI and neuron tracing data. NeuroImage 115:202–213CrossRefPubMed
go back to reference Daducci A, Dal Palù A, Lemkaddem A, Thiran J-P (2015) COMMIT: convex optimization modeling for microstructure informed tractography. IEEE Trans Med Imaging 34(1):246–257CrossRefPubMed Daducci A, Dal Palù A, Lemkaddem A, Thiran J-P (2015) COMMIT: convex optimization modeling for microstructure informed tractography. IEEE Trans Med Imaging 34(1):246–257CrossRefPubMed
go back to reference Daianu M, Jahanshad N, Villalon-Reina JE, Prasad G, Jacobs RE, Barnes S, Zlokovic BV, Montagne A, Thompson PM (2015) 7T multi-shell hybrid diffusion imaging (HYDI) for mapping brain connectivity in mice. Proc SPIE Int Soc Opt Eng 9413. https://doi.org/10.1117/12.2081491 Daianu M, Jahanshad N, Villalon-Reina JE, Prasad G, Jacobs RE, Barnes S, Zlokovic BV, Montagne A, Thompson PM (2015) 7T multi-shell hybrid diffusion imaging (HYDI) for mapping brain connectivity in mice. Proc SPIE Int Soc Opt Eng 9413. https://​doi.​org/​10.​1117/​12.​2081491
go back to reference Dauguet J, Peled S, Berezovskii V, Delzescaux T, Warfield SK, Born R, Westin C-F (2007) Comparison of fiber tracts derived from in-vivo DTI tractography with 3D histological neural tract tracer reconstruction on a macaque brain. Neuroimage 37(2):530–538CrossRefPubMed Dauguet J, Peled S, Berezovskii V, Delzescaux T, Warfield SK, Born R, Westin C-F (2007) Comparison of fiber tracts derived from in-vivo DTI tractography with 3D histological neural tract tracer reconstruction on a macaque brain. Neuroimage 37(2):530–538CrossRefPubMed
go back to reference Dong HW (2007) Allen reference atlas: a digital color brain atlas of the C57BL/6J male mouse. Wiley, New York Dong HW (2007) Allen reference atlas: a digital color brain atlas of the C57BL/6J male mouse. Wiley, New York
go back to reference Dyrby TB, Søgaard LV, Parker GJ, Alexander DC, Lind NM, Baaré WF, Hay-Schmidt A, Eriksen N, Pakkenberg B, Paulson OB (2007) Validation of in vitro probabilistic tractography. Neuroimage 37(4):1267–1277CrossRefPubMed Dyrby TB, Søgaard LV, Parker GJ, Alexander DC, Lind NM, Baaré WF, Hay-Schmidt A, Eriksen N, Pakkenberg B, Paulson OB (2007) Validation of in vitro probabilistic tractography. Neuroimage 37(4):1267–1277CrossRefPubMed
go back to reference Fieremans E, De Deene Y, Delputte S, Özdemir MS, Achten E, Lemahieu I (2008) The design of anisotropic diffusion phantoms for the validation of diffusion weighted magnetic resonance imaging. Phys Med Biol 53(19):5405CrossRefPubMed Fieremans E, De Deene Y, Delputte S, Özdemir MS, Achten E, Lemahieu I (2008) The design of anisotropic diffusion phantoms for the validation of diffusion weighted magnetic resonance imaging. Phys Med Biol 53(19):5405CrossRefPubMed
go back to reference Fillard P, Descoteaux M, Goh A, Gouttard S, Jeurissen B, Malcolm J, Ramirez-Manzanares A, Reisert M, Sakaie K, Tensaouti F (2011) Quantitative evaluation of 10 tractography algorithms on a realistic diffusion MR phantom. Neuroimage 56(1):220–234CrossRefPubMed Fillard P, Descoteaux M, Goh A, Gouttard S, Jeurissen B, Malcolm J, Ramirez-Manzanares A, Reisert M, Sakaie K, Tensaouti F (2011) Quantitative evaluation of 10 tractography algorithms on a realistic diffusion MR phantom. Neuroimage 56(1):220–234CrossRefPubMed
go back to reference Girard G, Whittingstall K, Deriche R, Descoteaux M (2014) Towards quantitative connectivity analysis: reducing tractography biases. Neuroimage 98:266–278CrossRefPubMed Girard G, Whittingstall K, Deriche R, Descoteaux M (2014) Towards quantitative connectivity analysis: reducing tractography biases. Neuroimage 98:266–278CrossRefPubMed
go back to reference Gyengesi E, Calabrese E, Sherrier MC, Johnson GA, Paxinos G, Watson C (2014) Semi-automated 3D segmentation of major tracts in the rat brain: comparing DTI with standard histological methods. Brain Struct Funct 219(2):539–550CrossRefPubMed Gyengesi E, Calabrese E, Sherrier MC, Johnson GA, Paxinos G, Watson C (2014) Semi-automated 3D segmentation of major tracts in the rat brain: comparing DTI with standard histological methods. Brain Struct Funct 219(2):539–550CrossRefPubMed
go back to reference Heiervang E, Behrens T, Mackay C, Robson M, Johansen-Berg H (2006) Between session reproducibility and between subject variability of diffusion MR and tractography measures. Neuroimage 33(3):867–877CrossRefPubMed Heiervang E, Behrens T, Mackay C, Robson M, Johansen-Berg H (2006) Between session reproducibility and between subject variability of diffusion MR and tractography measures. Neuroimage 33(3):867–877CrossRefPubMed
go back to reference Jbabdi S, Lehman JF, Haber SN, Behrens TE (2013) Human and monkey ventral prefrontal fibers use the same organizational principles to reach their targets: tracing versus tractography. J Neurosci 33(7):3190–3201CrossRefPubMedPubMedCentral Jbabdi S, Lehman JF, Haber SN, Behrens TE (2013) Human and monkey ventral prefrontal fibers use the same organizational principles to reach their targets: tracing versus tractography. J Neurosci 33(7):3190–3201CrossRefPubMedPubMedCentral
go back to reference Keifer OP, Gutman DA, Hecht EE, Keilholz SD, Ressler KJ (2015) A comparative analysis of mouse and human medial geniculate nucleus connectivity: a DTI and anterograde tracing study. NeuroImage 105:53–66CrossRefPubMed Keifer OP, Gutman DA, Hecht EE, Keilholz SD, Ressler KJ (2015) A comparative analysis of mouse and human medial geniculate nucleus connectivity: a DTI and anterograde tracing study. NeuroImage 105:53–66CrossRefPubMed
go back to reference Knösche TR, Anwander A, Liptrot M, Dyrby TB (2015) Validation of tractography: comparison with manganese tracing. Hum Brain Map 36(10):4116–4134CrossRef Knösche TR, Anwander A, Liptrot M, Dyrby TB (2015) Validation of tractography: comparison with manganese tracing. Hum Brain Map 36(10):4116–4134CrossRef
go back to reference Kuan L, Li Y, Lau C, Feng D, Bernard A, Sunkin SM, Zeng H, Dang C, Hawrylycz M, Ng L (2015) Neuroinformatics of the allen mouse brain connectivity atlas. Methods 73:4–17CrossRefPubMed Kuan L, Li Y, Lau C, Feng D, Bernard A, Sunkin SM, Zeng H, Dang C, Hawrylycz M, Ng L (2015) Neuroinformatics of the allen mouse brain connectivity atlas. Methods 73:4–17CrossRefPubMed
go back to reference Leemans A, Sijbers J, Verhoye M, Van der Linden A, Van Dyck D (2005) Mathematical framework for simulating diffusion tensor MR neural fiber bundles. Magn Reson Med 53(4):944–953CrossRefPubMed Leemans A, Sijbers J, Verhoye M, Van der Linden A, Van Dyck D (2005) Mathematical framework for simulating diffusion tensor MR neural fiber bundles. Magn Reson Med 53(4):944–953CrossRefPubMed
go back to reference Mangin J-F, Fillard P, Cointepas Y, Le Bihan D, Frouin V, Poupon C (2013) Toward global tractography. NeuroImage 80:290–296CrossRefPubMed Mangin J-F, Fillard P, Cointepas Y, Le Bihan D, Frouin V, Poupon C (2013) Toward global tractography. NeuroImage 80:290–296CrossRefPubMed
go back to reference MathWorks I (2012) MATLAB and statistics toolbox release 2012. The MathWorks. Inc, Natick MathWorks I (2012) MATLAB and statistics toolbox release 2012. The MathWorks. Inc, Natick
go back to reference Mori S, Crain BJ, Chacko VP, van Zijl PC (1999) Three-dimensional tracking of axonal projections in the brain by magnetic resonance imaging. Ann Neurol 45(2):265–269CrossRefPubMed Mori S, Crain BJ, Chacko VP, van Zijl PC (1999) Three-dimensional tracking of axonal projections in the brain by magnetic resonance imaging. Ann Neurol 45(2):265–269CrossRefPubMed
go back to reference Neher PF, Laun FB, Stieltjes B, Maier-Hein KH (2014) Fiberfox: facilitating the creation of realistic white matter software phantoms. Magn Reson Med 72(5):1460–1470CrossRefPubMed Neher PF, Laun FB, Stieltjes B, Maier-Hein KH (2014) Fiberfox: facilitating the creation of realistic white matter software phantoms. Magn Reson Med 72(5):1460–1470CrossRefPubMed
go back to reference Nolte J (2009) The human brain: an introduction to its functional anatomy, 6th edn. Mosby/Elsevier, Philadelphia Nolte J (2009) The human brain: an introduction to its functional anatomy, 6th edn. Mosby/Elsevier, Philadelphia
go back to reference Novikov DS, Jespersen SN, Kiselev VG, Fieremans E (2016) Quantifying brain microstructure with diffusion MRI: Theory and parameter estimation (ArXiv e-prints 1612) Novikov DS, Jespersen SN, Kiselev VG, Fieremans E (2016) Quantifying brain microstructure with diffusion MRI: Theory and parameter estimation (ArXiv e-prints 1612)
go back to reference Oh SW, Harris JA, Ng L, Winslow B, Cain N, Mihalas S, Wang Q, Lau C, Kuan L, Henry AM, Mortrud MT, Ouellette B, Nguyen TN, Sorensen SA, Slaughterbeck CR, Wakeman W, Li Y, Feng D, Ho A, Nicholas E, Hirokawa KE, Bohn P, Joines KM, Peng H, Hawrylycz MJ, Phillips JW, Hohmann JG, Wohnoutka P, Gerfen CR, Koch C, Bernard A, Dang C, Jones AR, Zeng H (2014) A mesoscale connectome of the mouse brain. Nature 508(7495):207–214. https://doi.org/10.1038/nature13186 CrossRefPubMedPubMedCentral Oh SW, Harris JA, Ng L, Winslow B, Cain N, Mihalas S, Wang Q, Lau C, Kuan L, Henry AM, Mortrud MT, Ouellette B, Nguyen TN, Sorensen SA, Slaughterbeck CR, Wakeman W, Li Y, Feng D, Ho A, Nicholas E, Hirokawa KE, Bohn P, Joines KM, Peng H, Hawrylycz MJ, Phillips JW, Hohmann JG, Wohnoutka P, Gerfen CR, Koch C, Bernard A, Dang C, Jones AR, Zeng H (2014) A mesoscale connectome of the mouse brain. Nature 508(7495):207–214. https://​doi.​org/​10.​1038/​nature13186 CrossRefPubMedPubMedCentral
go back to reference Pullens P, Roebroeck A, Goebel R (2010) Ground truth hardware phantoms for validation of diffusion-weighted MRI applications. J Magn Reson Imaging 32(2):482–488CrossRefPubMed Pullens P, Roebroeck A, Goebel R (2010) Ground truth hardware phantoms for validation of diffusion-weighted MRI applications. J Magn Reson Imaging 32(2):482–488CrossRefPubMed
go back to reference Reisert M, Kiselev VG, Dihtal B, Kellner E, Novikov DS (2014) MesoFT: unifying diffusion modelling and fiber tracking. Med Image Comput Comput Assist Interv 17(Pt 3):201–208PubMedPubMedCentral Reisert M, Kiselev VG, Dihtal B, Kellner E, Novikov DS (2014) MesoFT: unifying diffusion modelling and fiber tracking. Med Image Comput Comput Assist Interv 17(Pt 3):201–208PubMedPubMedCentral
go back to reference Rojkova K, Volle E, Urbanski M, Humbert F, Dell’Acqua F, de Schotten MT (2016) Atlasing the frontal lobe connections and their variability due to age and education: a spherical deconvolution tractography study. Brain Struct Funct 221(3):1751–1766CrossRefPubMed Rojkova K, Volle E, Urbanski M, Humbert F, Dell’Acqua F, de Schotten MT (2016) Atlasing the frontal lobe connections and their variability due to age and education: a spherical deconvolution tractography study. Brain Struct Funct 221(3):1751–1766CrossRefPubMed
go back to reference Schmahmann JD, Pandya DN, Wang R, Dai G, D’Arceuil HE, de Crespigny AJ, Wedeen VJ (2007) Association fibre pathways of the brain: parallel observations from diffusion spectrum imaging and autoradiography. Brain 130(3):630–653CrossRefPubMed Schmahmann JD, Pandya DN, Wang R, Dai G, D’Arceuil HE, de Crespigny AJ, Wedeen VJ (2007) Association fibre pathways of the brain: parallel observations from diffusion spectrum imaging and autoradiography. Brain 130(3):630–653CrossRefPubMed
go back to reference Seehaus AK, Roebroeck A, Chiry O, Kim D-S, Ronen I, Bratzke H, Goebel R, Galuske RA (2012) Histological validation of DW-MRI tractography in human postmortem tissue. Cereb Cortex 23:bhs036 Seehaus AK, Roebroeck A, Chiry O, Kim D-S, Ronen I, Bratzke H, Goebel R, Galuske RA (2012) Histological validation of DW-MRI tractography in human postmortem tissue. Cereb Cortex 23:bhs036
go back to reference Shattuck DW, Leahy RM (2002) BrainSuite: an automated cortical surface identification tool. Med Image Anal 6(2):129–142CrossRefPubMed Shattuck DW, Leahy RM (2002) BrainSuite: an automated cortical surface identification tool. Med Image Anal 6(2):129–142CrossRefPubMed
go back to reference Smith RE, Tournier J-D, Calamante F, Connelly A (2012) Anatomically-constrained tractography: improved diffusion MRI streamlines tractography through effective use of anatomical information. Neuroimage 62(3):1924–1938CrossRefPubMed Smith RE, Tournier J-D, Calamante F, Connelly A (2012) Anatomically-constrained tractography: improved diffusion MRI streamlines tractography through effective use of anatomical information. Neuroimage 62(3):1924–1938CrossRefPubMed
go back to reference Smith RE, Tournier J-D, Calamante F, Connelly A (2015) SIFT2: Enabling dense quantitative assessment of brain white matter connectivity using streamlines tractography. Neuroimage 119:338–351CrossRefPubMed Smith RE, Tournier J-D, Calamante F, Connelly A (2015) SIFT2: Enabling dense quantitative assessment of brain white matter connectivity using streamlines tractography. Neuroimage 119:338–351CrossRefPubMed
go back to reference Thomas C, Frank QY, Irfanoglu MO, Modi P, Saleem KS, Leopold DA, Pierpaoli C (2014) Anatomical accuracy of brain connections derived from diffusion MRI tractography is inherently limited. Proc Natl Acad Sci 111(46):16574–16579CrossRef Thomas C, Frank QY, Irfanoglu MO, Modi P, Saleem KS, Leopold DA, Pierpaoli C (2014) Anatomical accuracy of brain connections derived from diffusion MRI tractography is inherently limited. Proc Natl Acad Sci 111(46):16574–16579CrossRef
go back to reference Tournier J-D, Calamante F, Gadian DG, Connelly A (2004) Direct estimation of the fiber orientation density function from diffusion-weighted MRI data using spherical deconvolution. NeuroImage 23(3):1176–1185CrossRefPubMed Tournier J-D, Calamante F, Gadian DG, Connelly A (2004) Direct estimation of the fiber orientation density function from diffusion-weighted MRI data using spherical deconvolution. NeuroImage 23(3):1176–1185CrossRefPubMed
go back to reference Tournier J, Calamante F, Connelly A (2010) Improved probabilistic streamlines tractography by 2nd order integration over fibre orientation distributions. In: Proc. 18th annual meeting of the Intl. Soc. Mag. Reson. Med.(ISMRM), p 1670 Tournier J, Calamante F, Connelly A (2010) Improved probabilistic streamlines tractography by 2nd order integration over fibre orientation distributions. In: Proc. 18th annual meeting of the Intl. Soc. Mag. Reson. Med.(ISMRM), p 1670
go back to reference Tran G, Shi Y (2015) Fiber orientation and compartment parameter estimation from multi-shell diffusion imaging. IEEE Trans Med Imaging 34(11):2320–2332CrossRefPubMedPubMedCentral Tran G, Shi Y (2015) Fiber orientation and compartment parameter estimation from multi-shell diffusion imaging. IEEE Trans Med Imaging 34(11):2320–2332CrossRefPubMedPubMedCentral
go back to reference Wedeen VJ, Hagmann P, Tseng WYI, Reese TG, Weisskoff RM (2005) Mapping complex tissue architecture with diffusion spectrum magnetic resonance imaging. Magn Reson Med 54(6):1377–1386CrossRefPubMed Wedeen VJ, Hagmann P, Tseng WYI, Reese TG, Weisskoff RM (2005) Mapping complex tissue architecture with diffusion spectrum magnetic resonance imaging. Magn Reson Med 54(6):1377–1386CrossRefPubMed
go back to reference Yamada K, Sakai K, Akazawa K, Yuen S, Nishimura T (2009) MR tractography: a review of its clinical applications. Magn Reson Med Sci 8(4):165–174CrossRefPubMed Yamada K, Sakai K, Akazawa K, Yuen S, Nishimura T (2009) MR tractography: a review of its clinical applications. Magn Reson Med Sci 8(4):165–174CrossRefPubMed
Metadata
Title
When tractography meets tracer injections: a systematic study of trends and variation sources of diffusion-based connectivity
Authors
Dogu Baran Aydogan
Russell Jacobs
Stephanie Dulawa
Summer L. Thompson
Maite Christi Francois
Arthur W. Toga
Hongwei Dong
James A. Knowles
Yonggang Shi
Publication date
01-07-2018
Publisher
Springer Berlin Heidelberg
Published in
Brain Structure and Function / Issue 6/2018
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-018-1663-8

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