Abstract
We have developed a novel method to describe human white matter anatomy using an approach that is both intuitive and simple to use, and which automatically extracts white matter tracts from diffusion MRI volumes. Further, our method simplifies the quantification and statistical analysis of white matter tracts on large diffusion MRI databases. This work reflects the careful syntactical definition of major white matter fiber tracts in the human brain based on a neuroanatomist’s expert knowledge. The framework is based on a novel query language with a near-to-English textual syntax. This query language makes it possible to construct a dictionary of anatomical definitions that describe white matter tracts. The definitions include adjacent gray and white matter regions, and rules for spatial relations. This novel method makes it possible to automatically label white matter anatomy across subjects. After describing this method, we provide an example of its implementation where we encode anatomical knowledge in human white matter for ten association and 15 projection tracts per hemisphere, along with seven commissural tracts. Importantly, this novel method is comparable in accuracy to manual labeling. Finally, we present results applying this method to create a white matter atlas from 77 healthy subjects, and we use this atlas in a small proof-of-concept study to detect changes in association tracts that characterize schizophrenia.
Similar content being viewed by others
Notes
To improve readability, through this paper we will use the term tractography to refer exclusively to streamline tractography.
It has been pointed to us that these procedures have been recently updated to constrained spherical deconvoltion-based tractography approaches in the supplementary material of a recent article by Rojkova et al. (2015). This procedure could be better suited for the dataset and tractography algorithm used in this work. Hence, we think that manual validation against this novel protocol could be an interesting follow-up to this article.
References
Akers D, Sherbondy A, Mackenzie R, Dougherty RF, Wandell B (2005) Exploration of the brain’s white matter pathways with dynamic queries. IEEE Trans Visual Comput Graphics 11:377–384
Asami T, Saito Y, Whitford TJ, Makris N, Niznikiewicz M, McCarley RW, Shenton ME, Kubicki M (2013): Abnormalities of middle longitudinal fascicle and disorganization in patients with schizophrenia. Schizophr Res 143:253–259
Avants B, Epstein CL, Grossman M, Gee JC (2008) Symmetric diffeomorphic image registration with cross-correlation: evaluating automated labeling of elderly and neurodegenerative brain. Med Image Anal 12:26–41
Avants B, Tustison NJ, Song G, Cook PA, Klein A, Gee JC (2011) A reproducible evaluation of ANTs similarity metric performance in brain image registration. Neuroimage 54:2033–2044
Axer H, Klingner CM, Prescher A (2013) Fiber anatomy of dorsal and ventral language streams. Brain Lang 127:192–204
Beaulieu C (2002) The basis of anisotropic water diffusion in the nervous system—a technical review. NMR Biomed 15:435–455
Behrens TEJ, Johansen Berg H, Woolrich MW, Smith SM, Wheeler-Kingshott CAM, Boulby PA, Barker GJ, Sillery EL, Sheehan K, Ciccarelli O (2003) Non-invasive mapping of connections between human thalamus and cortex using diffusion imaging. Nat Neurosci 6:750–757
Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B (Methodol) 57:289–300
Bergen GVD (1997) Efficient collision detection of complex deformable models using AABB trees. J Graph Tools 2:1–13
Bernal B, Ardila A (2009) The role of the arcuate fasciculus in conduction aphasia. Brain 132:2309–2316
Catani M, Thiebaut de Schotten M (2008) A diffusion tensor imaging tractography atlas for virtual in vivo dissections. Cortex 44:1105–1132
Catani M, Howard RJ, Pajevic S, Jones DK (2002) Virtual in vivo interactive dissection of white matter fasciculi in the human brain. Neuroimage 17:77–94
Catani M, Jones DK, Ffytche DH (2005) Perisylvian language networks of the human brain. Ann Neurol 57:8–17
Cohen J (1960) A coefficient of agreement for nominal scales. Educ Psychol Meas 20:37–46. doi:10.1177/001316446002000104
Cormen TH, Leiserson CE, Rivest RL, Stein C (2009) Introduction to algorithms. MIT Press, Cambridge
Crosby EC, Schnitzlein HN (1982) Comparative correlative neuroanatomy of the vertebrate telencephalon. MacMillan, Michigan
Dejerine JJ, Dejerine-Klumpke A (1895) Anatomie des centres nerveux. Rueff, Paris
Desikan RS, Ségonne F, Fischl B, Quinn BT, Dickerson BC, Blacker D, Buckner RL, Dale AM, Maguire RP, Hyman BT, Albert M, Killiany RJ (2006) An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage 31:968–980
Duffau H (2008) The anatomo-functional connectivity of language revisited. Neuropsychologia 46:927–934
Fernandez-Miranda JC, Albert L Rhoton Jr, Yukinari Kakizawa, Chanyoung Choi, Juan Álvarez-Linera (2008a) The claustrum and its projection system in the human brain: a microsurgical and tractographic anatomical study. J Neurosurg 108:764–774
Fernandez-Miranda JC, Rhoton AL, Álvarez-Linera J, Kakizawa Y, Choi C, de Oliveira EP (2008b) Three-dimensional microsurgical and tractographic anatomy of the white matter of the human brain. Neurosurgery 62:989–1026
Fischl B, Salat DH, Busa E, Albert M, Dieterich M, Haselgrove C, van der Kouwe AJW, Killiany R, Kennedy D, Klaveness S, Montillo A, Makris N, Rosen B, Dale AM (2002) Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron 33:341–355
Geschwind N, Quadfasel FA, Segarra JM (1968) Isolation of the speech area. Neuropsychologia 6:327–340
Goñi J, van den Heuvel MP, Avena-Koenigsberger A, de Mendizabal NV, Betzel RF, Griffa A, Hagmann P, Corominas-Murtra B, Thiran J-P, Sporns O (2014) Resting-brain functional connectivity predicted by analytic measures of network communication. Proc Natl Acad Sci 111:833–838. doi:10.1073/pnas.1315529111
Hua K, Zhang J, Wakana S, Jiang H, Li X, Reich DS, Calabresi PA, Pekar JJ, van Zijl PCM, Mori S (2008) Tract probability maps in stereotaxic spaces: analyses of white matter anatomy and tract-specific quantification. Neuroimage 39:336–347
Iglesias JE, Sabuncu MR (2015) Multi-atlas segmentation of biomedical images: a survey. MIA 24:205–219. doi:10.1016/j.media.2015.06.012
Johansen Berg H, Behrens TEJ, Sillery E, Ciccarelli O, Thompson AJ, Smith SM, Matthews PM (2005) Functional-anatomical validation and individual variation of diffusion tractography-based segmentation of the human thalamus. Cereb Cortex 15:31–39
Jones DK, Catani M, Pierpaoli C, Reeves SJC, Shergill SS, O’Sullivan M, Golesworthy P, McGuire P, Horsfield MA, Simmons A, Williams SCR, Howard RJ (2006) Age effects on diffusion tensor magnetic resonance imaging tractography measures of frontal cortex connections in schizophrenia. Hum Brain Mapp 27:230–238
Karlsgodt KH, van Erp TGM, Poldrack RA, Bearden CE, Nuechterlein KH, Cannon TD (2008) Diffusion tensor imaging of the superior longitudinal fasciculus and working memory in recent-onset schizophrenia. Biol Psychiatry 63:512–518
Kubicki M, McCarley R, Westin C-F, Park H-J, Maier SE, Kikinis R, Jolesz FA, Shenton ME (2007) A review of diffusion tensor imaging studies in schizophrenia. J Psychol Res 41:15–30
Landis JR, Koch GG (1977) The measurement of observer agreement for categorical data. Biometrics 33:159–174
Lawes INC, Barrick TR, Murugam V, Spierings N, Evans DR, Song M, Clark CA (2008) Atlas-based segmentation of white matter tracts of the human brain using diffusion tensor tractography and comparison with classical dissection. Neuroimage 39:62–79
Lazar M, Alexander AL (2003) An error analysis of white matter tractography methods: synthetic diffusion tensor field simulations. Neuroimage 20:1140–1153
Lebel C, Gee M, Camicioli R, Wieler M, Martin W, Beaulieu C (2012) Diffusion tensor imaging of white matter tract evolution over the lifespan. Neuroimage 60:340–352
Ludwig E, Klinger L (1956) Atlas cerebri humani. Karger, Basel
Makris N, Pandya D (2009) The extreme capsule in humans and rethinking of the language circuitry. Brain Struct Funct 213:343–358
Makris N, Worth AJ, Papadimitriou GM, Stakes JW, Caviness VS, Kennedy DN, Pandya D, Kaplan E, Sorensen AG, Wu O, Reese TG, Van Wedeen J, Rosen BR, Davis TL (1997) Morphometry of in vivo human white matter association pathways with diffusion-weighted magnetic resonance imaging. Ann Neurol 42:951–962
Makris N, Meyer JW, Bates JF, Yeterian EH, Kennedy DN, Caviness VS (1999) MRI-based topographic parcellation of human cerebral white matter and nuclei: II. Rationale and applications with systematics of cerebral connectivity. Neuroimage 9:18–45
Makris N, Kennedy DN, McInerney S, Sorensen AG, Wang R, Caviness VS, Pandya D (2005) Segmentation of subcomponents within the superior longitudinal fascicle in humans: a quantitative, in vivo, DT-MRI study. Cereb Cortex 15:854–869
Makris N, Preti MG, Asami T, Pelavin P, Campbell B, Papadimitriou GM, Kaiser J, Baselli G, Westin C-F, Shenton ME, Kubicki M (2012) Human middle longitudinal fascicle: variations in patterns of anatomical connections. Brain Struct Funct 218(4):1–18
Malcolm JG, Michailovich O, Bouix S, Westin C-F, Shenton ME, Rathi Y (2010) A filtered approach to neural tractography using the Watson directional function. IEEE Trans Med Imaging 14:58–69
Mandonnet E, Nouet A, Gatignol P, Capelle L, Duffau H (2007) Does the left inferior longitudinal fasciculus play a role in language? A brain stimulation study. Brain 130:623–629
Mori S, van Zijl PCM (2002) Fiber tracking: principles and strategies—a technical review. NMR Biomed 15:468–480
Nichols TE, Holmes AP (2002): Nonparametric permutation tests for functional neuroimaging: a primer with examples. Human Brain Mapp 15
O’Donnell LJ, Westin C-F (2007) Automatic tractography segmentation using a high-dimensional white matter atlas. IEEE Trans Med Imaging 26:1562–1575
Parent A (1996) Carpenter’s human neuroanatomy, 9th edn. Williams & Wilkins, Philadelphia
Reveley C, Seth AK, Pierpaoli C, Silva AC, Yu D, Saunders RC, Leopold DA, Ye FQ (2015) Superficial white matter fiber systems impede detection of long-range cortical connections in diffusion MR tractography. Proc Natl Acad Sci 112:E2820–E2828. doi:10.1073/pnas.1418198112
Rilling JK, Glasser MF, Preuss TM, Ma X, Zhao T, Hu X, Behrens TEJ (2008) The evolution of the arcuate fasciculus revealed with comparative DTI. Nat Neurosci 11:426–428
Rojkova K, Volle E, Urbanski M, Humbert F, Dell’Acqua F, Thiebaut de Schotten M (2015) Atlasing the frontal lobe connections and their variability due to age and education: a spherical deconvolution tractography study. Brain Struct Funct. doi:10.1007/s00429-015-1001-3
Salat DH, Greve DN, Pacheco JL, Quinn BT, Helmer KG, Buckner RL, Fischl B (2009) Regional white matter volume differences in nondemented aging and Alzheimer’s disease. Neuroimage 44:1247–1258
Saur D, Kreher BW, Schnell S, Kummerer D, Kellmeyer P, Vry MS, Umarova R, Musso M, Glauche V, Abel S, Huber W, Rijntjes M, Hennig J, Weiller C (2008) Ventral and dorsal pathways for language. Proc Natl Acad Sci 105:18035–18040
Schmahmann JD, Pandya D (2007) The complex history of the fronto-occipital fasciculus. J Hist Neurosci 16:362–377
Schmahmann JD, Pandya D, Wang R, Dai G, D’Arceuil HE, de Crespigny AJ, Van Wedeen J (2007) Association fibre pathways of the brain: parallel observations from diffusion spectrum imaging and autoradiography. Brain 130:630
Thiebaut de Schotten M, Dell’acqua F, Forkel SJ, Simmons A, Vergani F, Murphy DGM, Catani M (2011a) A lateralized brain network for visuospatial attention. Nat Neurosci 14:1245–1246
Thiebaut de Schotten M, Ffytche DH, Bizzi A, Dell’acqua F, Allin MPG, Walshe M, Murray R, Williams SCR, Murphy DGM, Catani M (2011b) Atlasing location, asymmetry and inter-subject variability of white matter tracts in the human brain with MR diffusion tractography. Neuroimage 54:49–59
Thomas C, Ye FQ, İrfanoğlu 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 111:16574–16579. doi:10.1073/pnas.1405672111
Tuch D (2004) Q-ball imaging. MRM 52:1358–1372. doi:10.1002/mrm.20279
Wakana S, Jiang H, Nagae-Poetscher LM, van Zijl PCM, Mori S (2004) Fiber tract-based atlas of human white matter anatomy. Radiology 230:77–87
Wakana S, Caprihan A, Panzenboeck MM, Fallon JH, Perry M, Gollub RL, Hua K, Zhang J, Jiang H, Dubey P, Blitz A, van Zijl PCM, Mori S (2007) Reproducibility of quantitative tractography methods applied to cerebral white matter. Neuroimage 36:630–644
Wang X, Grimson WEL, Westin C-F (2011) Tractography segmentation using a hierarchical Dirichlet processes mixture model. Neuroimage 54:290–302
Wang Y, Fernandez-Miranda JC, Verstynen T, Pathak S, Schneider W, Yeh FC (2012) Rethinking the role of the middle longitudinal fascicle in language and auditory pathways. Cereb Cortex 23(10):2347–2356
Wassermann D, Bloy L, Kanterakis E, Verma R, Deriche R (2010) Unsupervised white matter fiber clustering and tract probability map generation: applications of a Gaussian process framework for white matter fibers. Neuroimage 51:228–241
Witelson SF (1989) Hand and sex differences in the isthmus and genu of the human corpus callosum. Brain 112:799–835
Yeatman JD, Dougherty RF, Myall NJ, Wandell BA, Feldman HM (2012) Tract profiles of white matter properties: automating fiber-tract quantification. PLoS One 7:e49790
Yendiki A, Panneck P, Srinivasan P, Stevens A, Zollei L, Augustinack J, Wang R, Salat D, Ehrlich S, Behrens TEJ, Jbabdi S, Gollub R, Fischl B (2011) Automated probabilistic reconstruction of white-matter pathways in health and disease using an atlas of the underlying anatomy. Front Neuroinform 5:23
Zhang Y, Zhang J, Oishi K, Faria AV, Jiang H, Li X, Akhter K, Rosa-Neto P, Pike GB, Evans AC, Toga AW, Woods R, Mazziotta JC, Miller MI, van Zijl PCM, Mori S (2010) Atlas-guided tract reconstruction for automated and comprehensive examination of the white matter anatomy. Neuroimage 52:1289–1301
Acknowledgments
This work has been supported by NIH grants: R01MH074794, R01MH092862, P41RR013218, R01MH097979, P41EB015902, VA Boston Healthcare System, Boston, MA and Swedish Research Council (VR) Grant 2012-3682. Demian Wassermann wishes to thank Dr. Maxime Descoteaux for helpful discussions.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
For this type of study formal consent is not required.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Supplementary material 1 (MP4 20512 kb)
Rights and permissions
About this article
Cite this article
Wassermann, D., Makris, N., Rathi, Y. et al. The white matter query language: a novel approach for describing human white matter anatomy. Brain Struct Funct 221, 4705–4721 (2016). https://doi.org/10.1007/s00429-015-1179-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00429-015-1179-4