Skip to main content
Top
Published in: Brain Structure and Function 5/2017

Open Access 01-07-2017 | Original Article

Robust thalamic nuclei segmentation method based on local diffusion magnetic resonance properties

Authors: Giovanni Battistella, Elena Najdenovska, Philippe Maeder, Naghmeh Ghazaleh, Alessandro Daducci, Jean-Philippe Thiran, Sébastien Jacquemont, Constantin Tuleasca, Marc Levivier, Meritxell Bach Cuadra, Eleonora Fornari

Published in: Brain Structure and Function | Issue 5/2017

Login to get access

Abstract

The thalamus is an essential relay station in the cortical–subcortical connections. It is characterized by a complex anatomical architecture composed of numerous small nuclei, which mediate the involvement of the thalamus in a wide range of neurological functions. We present a novel framework for segmenting the thalamic nuclei, which explores the orientation distribution functions (ODFs) from diffusion magnetic resonance images at 3 T. The differentiation of the complex intra-thalamic microstructure is improved by using the spherical harmonic (SH) representation of the ODFs, which provides full angular characterization of the diffusion process in each voxel. The clustering was performed using the k-means algorithm initialized in a data-driven manner. The method was tested on 35 healthy volunteers and our results show a robust, reproducible and accurate segmentation of the thalamus in seven nuclei groups. Six of them closely matched the anatomy and were labeled as anterior, ventral anterior, medio-dorsal, ventral latero-ventral, ventral latero-dorsal and pulvinar, while the seventh cluster included the centro-lateral and the latero-posterior nuclei. Results were evaluated both qualitatively, by comparing the segmented nuclei to the histological atlas of Morel, and quantitatively, by measuring the clusters’ extent and the clusters’ spatial distribution across subjects and hemispheres. We also showed the robustness of our approach across different sequences and scanners, as well as intra-subject reproducibility of the segmented clusters using additional two scan–rescan datasets. We also observed an overlap between the path of the main long-connection tracts passing through the thalamus and the spatial distribution of the nuclei identified with our clustering algorithm. Our approach, based on SH representations of the ODFs, outperforms the one based on angular differences between the principle diffusion directions, which is considered so far as state-of-the-art method. Our findings show an anatomically reliable segmentation of the main groups of thalamic nuclei that could be of potential use in many clinical applications.
Appendix
Available only for authorised users
Literature
go back to reference Abosch A, Yacoub E, Ugurbil K, Harel N (2010) An assessment of current brain targets for deep brain stimulation surgery with susceptibility-weighted imaging at 7 tesla. Neurosurgery 67:1745–1756 (discussion 1756) Abosch A, Yacoub E, Ugurbil K, Harel N (2010) An assessment of current brain targets for deep brain stimulation surgery with susceptibility-weighted imaging at 7 tesla. Neurosurgery 67:1745–1756 (discussion 1756)
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 64:554–566PubMedPubMedCentral 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 64:554–566PubMedPubMedCentral
go back to reference Battistella G, Niederhauser J, Fornari E, Hippolyte L, Gronchi Perrin A, Lesca G, Forzano F, Hagmann P, Vingerhoets FJ, Draganski B, Maeder P, Jacquemont S (2013) Brain structure in asymptomatic FMR1 premutation carriers at risk for fragile X-associated tremor/ataxia syndrome. Neurobiol Aging 34:1700–1707CrossRefPubMed Battistella G, Niederhauser J, Fornari E, Hippolyte L, Gronchi Perrin A, Lesca G, Forzano F, Hagmann P, Vingerhoets FJ, Draganski B, Maeder P, Jacquemont S (2013) Brain structure in asymptomatic FMR1 premutation carriers at risk for fragile X-associated tremor/ataxia syndrome. Neurobiol Aging 34:1700–1707CrossRefPubMed
go back to reference Baumann PS, Cammoun L, Conus P, Do KQ, Marquet P, Meskaldji D, Meuli R, Thiran J-P, Hagmann P (2012) High b-value diffusion-weighted imaging: a sensitive method to reveal white matter differences in schizophrenia. Psychiatry Res Neuroimaging 201:144–151CrossRefPubMed Baumann PS, Cammoun L, Conus P, Do KQ, Marquet P, Meskaldji D, Meuli R, Thiran J-P, Hagmann P (2012) High b-value diffusion-weighted imaging: a sensitive method to reveal white matter differences in schizophrenia. Psychiatry Res Neuroimaging 201:144–151CrossRefPubMed
go back to reference Behrens TE, Johansen-Berg H, Woolrich MW, Smith SM, Wheeler-Kingshott CA, Boulby PA, Barker GJ, Sillery EL, Sheehan K, Ciccarelli O, Thompson AJ, Brady JM, Matthews PM (2003) Non-invasive mapping of connections between human thalamus and cortex using diffusion imaging. Nat Neurosci 6:750–757CrossRefPubMed Behrens TE, Johansen-Berg H, Woolrich MW, Smith SM, Wheeler-Kingshott CA, Boulby PA, Barker GJ, Sillery EL, Sheehan K, Ciccarelli O, Thompson AJ, Brady JM, Matthews PM (2003) Non-invasive mapping of connections between human thalamus and cortex using diffusion imaging. Nat Neurosci 6:750–757CrossRefPubMed
go back to reference Cordova JQ, Pearson CE (1988) On a modified streamline curvature method for the Euler equations. Commun Appl Numer M 4:327–333CrossRef Cordova JQ, Pearson CE (1988) On a modified streamline curvature method for the Euler equations. Commun Appl Numer M 4:327–333CrossRef
go back to reference Deoni SC, Josseau MJ, Rutt BK, Peters TM (2005) Visualization of thalamic nuclei on high resolution, multi-averaged T1 and T2 maps acquired at 1.5 T. Hum Brain Mapp 25:353–359CrossRefPubMed Deoni SC, Josseau MJ, Rutt BK, Peters TM (2005) Visualization of thalamic nuclei on high resolution, multi-averaged T1 and T2 maps acquired at 1.5 T. Hum Brain Mapp 25:353–359CrossRefPubMed
go back to reference Descoteaux M, Angelino E, Fitzgibbons S, Deriche R (2007) Regularized, fast, and robust analytical Q-ball imaging. Magn Reson Med 58:497–510CrossRefPubMed Descoteaux M, Angelino E, Fitzgibbons S, Deriche R (2007) Regularized, fast, and robust analytical Q-ball imaging. Magn Reson Med 58:497–510CrossRefPubMed
go back to reference Dubuisson MP, Jain AK (1994) A modified Hausdorff distance for object matching, vol 1, pp 566–568, 9–13 Oct 1994 Dubuisson MP, Jain AK (1994) A modified Hausdorff distance for object matching, vol 1, pp 566–568, 9–13 Oct 1994
go back to reference Eidelberg D, Galaburda AM (1982) Symmetry and asymmetry in the human posterior thalamus. I. Cytoarchitectonic analysis in normal persons. Arch Neurol 39:325–332CrossRefPubMed Eidelberg D, Galaburda AM (1982) Symmetry and asymmetry in the human posterior thalamus. I. Cytoarchitectonic analysis in normal persons. Arch Neurol 39:325–332CrossRefPubMed
go back to reference Fischl B, Salat DH, Busa E, Albert M, Dieterich M, Haselgrove C, van der Kouwe A, 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 33:341–355CrossRefPubMed Fischl B, Salat DH, Busa E, Albert M, Dieterich M, Haselgrove C, van der Kouwe A, 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 33:341–355CrossRefPubMed
go back to reference Fischl B, van der Kouwe A, Destrieux C, Halgren E, Segonne F, Salat DH, Busa E, Seidman LJ, Goldstein J, Kennedy D, Caviness V, Makris N, Rosen B, Dale AM (2004) Automatically parcellating the human cerebral cortex. Cereb Cortex 14:11–22CrossRefPubMed Fischl B, van der Kouwe A, Destrieux C, Halgren E, Segonne F, Salat DH, Busa E, Seidman LJ, Goldstein J, Kennedy D, Caviness V, Makris N, Rosen B, Dale AM (2004) Automatically parcellating the human cerebral cortex. Cereb Cortex 14:11–22CrossRefPubMed
go back to reference Gringel T, Schulz-Schaeffer W, Elolf E, Frolich A, Dechent P, Helms G (2009) Optimized high-resolution mapping of magnetization transfer (MT) at 3 Tesla for direct visualization of substructures of the human thalamus in clinically feasible measurement time. J Magn Reson Imaging 29:1285–1292CrossRefPubMed Gringel T, Schulz-Schaeffer W, Elolf E, Frolich A, Dechent P, Helms G (2009) Optimized high-resolution mapping of magnetization transfer (MT) at 3 Tesla for direct visualization of substructures of the human thalamus in clinically feasible measurement time. J Magn Reson Imaging 29:1285–1292CrossRefPubMed
go back to reference Gut M, Urbanik A, Forsberg L, Binder M, Rymarczyk K, Sobiecka B, Kozub J, Grabowska A (2007) Brain correlates of right-handedness. Acta Neurobiol Exp 67:43–51 Gut M, Urbanik A, Forsberg L, Binder M, Rymarczyk K, Sobiecka B, Kozub J, Grabowska A (2007) Brain correlates of right-handedness. Acta Neurobiol Exp 67:43–51
go back to reference Hale JR, Mayhew SD, Mullinger KJ, Wilson RS, Arvanitis TN, Francis ST, Bagshaw AP (2015) Comparison of functional thalamic segmentation from seed-based analysis and ICA. NeuroImage 114:448–465CrossRefPubMed Hale JR, Mayhew SD, Mullinger KJ, Wilson RS, Arvanitis TN, Francis ST, Bagshaw AP (2015) Comparison of functional thalamic segmentation from seed-based analysis and ICA. NeuroImage 114:448–465CrossRefPubMed
go back to reference Johansen-Berg H, Behrens TE, Robson MD, Drobnjak I, Rushworth MF, Brady JM, Smith SM, Higham DJ, Matthews PM (2004) Changes in connectivity profiles define functionally distinct regions in human medial frontal cortex. Proc Natl Acad Sci USA 101:13335–13340CrossRefPubMedPubMedCentral Johansen-Berg H, Behrens TE, Robson MD, Drobnjak I, Rushworth MF, Brady JM, Smith SM, Higham DJ, Matthews PM (2004) Changes in connectivity profiles define functionally distinct regions in human medial frontal cortex. Proc Natl Acad Sci USA 101:13335–13340CrossRefPubMedPubMedCentral
go back to reference Johnson HJ, Harris GKW (2007) BRAINSFit: mutual information registrations of whole-brain 3D images, using the Insight toolkit. Insight J Johnson HJ, Harris GKW (2007) BRAINSFit: mutual information registrations of whole-brain 3D images, using the Insight toolkit. Insight J
go back to reference Jonasson L, Hagmann P, Pollo C, Bresson X, Wilson CR, Meuli R, Thiran JP (2007) A level set method for segmentation of the thalamus and its nuclei in DT-MRI. Signal Process 87:309–321CrossRef Jonasson L, Hagmann P, Pollo C, Bresson X, Wilson CR, Meuli R, Thiran JP (2007) A level set method for segmentation of the thalamus and its nuclei in DT-MRI. Signal Process 87:309–321CrossRef
go back to reference Jones EG (1985) The thalamus. Plenum Press, New York Jones EG (1985) The thalamus. Plenum Press, New York
go back to reference Jones EG (1997) Cortical development and thalamic pathology in schizophrenia. Schizophr Bull 23:483–501CrossRefPubMed Jones EG (1997) Cortical development and thalamic pathology in schizophrenia. Schizophr Bull 23:483–501CrossRefPubMed
go back to reference Kim DJ, Park B, Park HJ (2013) Functional connectivity-based identification of subdivisions of the basal ganglia and thalamus using multilevel independent component analysis of resting state fMRI. Hum Brain Mapp 34:1371–1385CrossRefPubMed Kim DJ, Park B, Park HJ (2013) Functional connectivity-based identification of subdivisions of the basal ganglia and thalamus using multilevel independent component analysis of resting state fMRI. Hum Brain Mapp 34:1371–1385CrossRefPubMed
go back to reference Kumar V, Mang S, Grodd W (2015) Direct diffusion-based parcellation of the human thalamus. Brain Struct Funct 220:1619–1635CrossRefPubMed Kumar V, Mang S, Grodd W (2015) Direct diffusion-based parcellation of the human thalamus. Brain Struct Funct 220:1619–1635CrossRefPubMed
go back to reference Magnotta VA, Gold S, Andreasen NC, Ehrhardt JC, Yuh WT (2000) Visualization of subthalamic nuclei with cortex attenuated inversion recovery MR imaging. NeuroImage 11:341–346CrossRefPubMed Magnotta VA, Gold S, Andreasen NC, Ehrhardt JC, Yuh WT (2000) Visualization of subthalamic nuclei with cortex attenuated inversion recovery MR imaging. NeuroImage 11:341–346CrossRefPubMed
go back to reference Mang SC, Busza A, Reiterer S, Grodd W, Klose AU (2012) Thalamus segmentation based on the local diffusion direction: a group study. Magn Reson Med 67:118–126CrossRefPubMed Mang SC, Busza A, Reiterer S, Grodd W, Klose AU (2012) Thalamus segmentation based on the local diffusion direction: a group study. Magn Reson Med 67:118–126CrossRefPubMed
go back to reference Morel A, Magnin M, Jeanmonod D (1997) Multiarchitectonic and stereotactic atlas of the human thalamus. J Comp Neurol 387:588–630CrossRefPubMed Morel A, Magnin M, Jeanmonod D (1997) Multiarchitectonic and stereotactic atlas of the human thalamus. J Comp Neurol 387:588–630CrossRefPubMed
go back to reference Mori S, Zhang J (2006) Principles of diffusion tensor imaging and its applications to basic neuroscience research. Neuron 51:527–539CrossRefPubMed Mori S, Zhang J (2006) Principles of diffusion tensor imaging and its applications to basic neuroscience research. Neuron 51:527–539CrossRefPubMed
go back to reference Ohye C, Higuchi Y, Shibazaki T, Hashimoto T, Koyama T, Hirai T, Matsuda S, Serizawa T, Hori T, Hayashi M, Ochiai T, Samura H, Yamashiro K (2012) Gamma knife thalamotomy for Parkinson disease and essential tremor: a prospective multicenter study. Neurosurgery 70:526–535 (discussion 535–536) Ohye C, Higuchi Y, Shibazaki T, Hashimoto T, Koyama T, Hirai T, Matsuda S, Serizawa T, Hori T, Hayashi M, Ochiai T, Samura H, Yamashiro K (2012) Gamma knife thalamotomy for Parkinson disease and essential tremor: a prospective multicenter study. Neurosurgery 70:526–535 (discussion 535–536)
go back to reference O’Muircheartaigh J, Vollmar C, Traynor C, Barker GJ, Kumari V, Symms MR, Thompson P, Duncan JS, Koepp MJ, Richardson MP (2011) Clustering probabilistic tractograms using independent component analysis applied to the thalamus. NeuroImage 54:2020–2032CrossRefPubMedPubMedCentral O’Muircheartaigh J, Vollmar C, Traynor C, Barker GJ, Kumari V, Symms MR, Thompson P, Duncan JS, Koepp MJ, Richardson MP (2011) Clustering probabilistic tractograms using independent component analysis applied to the thalamus. NeuroImage 54:2020–2032CrossRefPubMedPubMedCentral
go back to reference Pierpaoli C, Basser PJ (1996) Toward a quantitative assessment of diffusion anisotropy. Magn Reson Med 36:893–906CrossRefPubMed Pierpaoli C, Basser PJ (1996) Toward a quantitative assessment of diffusion anisotropy. Magn Reson Med 36:893–906CrossRefPubMed
go back to reference Rimol LM, Specht K, Hugdahl K (2006) Controlling for individual differences in fMRI brain activation to tones, syllables, and words. NeuroImage 30:554–562CrossRefPubMed Rimol LM, Specht K, Hugdahl K (2006) Controlling for individual differences in fMRI brain activation to tones, syllables, and words. NeuroImage 30:554–562CrossRefPubMed
go back to reference Rittner L, Lotufo RA, Campbell J, Pike GB (2010) Segmentation of thalamic nuclei based on tensorial morphological gradient of diffusion tensor fields. I S Biomed Imaging 1173–1176 Rittner L, Lotufo RA, Campbell J, Pike GB (2010) Segmentation of thalamic nuclei based on tensorial morphological gradient of diffusion tensor fields. I S Biomed Imaging 1173–1176
go back to reference Saalmann YB (2014) Intralaminar and medial thalamic influence on cortical synchrony, information transmission and cognition. Frontiers Syst Neurosci 8:83CrossRef Saalmann YB (2014) Intralaminar and medial thalamic influence on cortical synchrony, information transmission and cognition. Frontiers Syst Neurosci 8:83CrossRef
go back to reference Sherman SM, Guillery RW (2002) The role of the thalamus in the flow of information to the cortex. Philos Trans R Soc Lond Ser B Biol Sci 357:1695–1708CrossRef Sherman SM, Guillery RW (2002) The role of the thalamus in the flow of information to the cortex. Philos Trans R Soc Lond Ser B Biol Sci 357:1695–1708CrossRef
go back to reference Shipp S (2003) The functional logic of cortico-pulvinar connections. Philos Trans R Soc Lond Ser B Biol Sci 358:1605–1624CrossRef Shipp S (2003) The functional logic of cortico-pulvinar connections. Philos Trans R Soc Lond Ser B Biol Sci 358:1605–1624CrossRef
go back to reference Stough J, Glaister J, Ye C, Ying S, Prince J, Carass A (2014) Automatic method for thalamus parcellation using multi-modal feature classification. In: Golland P, Hata N, Barillot C, Hornegger J, Howe R (eds) Medical image computing and computer-assisted intervention—MICCAI 2014. Springer, New York, pp 169–176 Stough J, Glaister J, Ye C, Ying S, Prince J, Carass A (2014) Automatic method for thalamus parcellation using multi-modal feature classification. In: Golland P, Hata N, Barillot C, Hornegger J, Howe R (eds) Medical image computing and computer-assisted intervention—MICCAI 2014. Springer, New York, pp 169–176
go back to reference Swenson RS (2006) Review of clinical and functional neuroscience. Dartmouth Medical School, Hanover Swenson RS (2006) Review of clinical and functional neuroscience. Dartmouth Medical School, Hanover
go back to reference Tourdias T, Saranathan M, Levesque IR, Su J, Rutt BK (2014) Visualization of intra-thalamic nuclei with optimized white-matter-nulled MPRAGE at 7 T. NeuroImage 84:534–545CrossRefPubMed Tourdias T, Saranathan M, Levesque IR, Su J, Rutt BK (2014) Visualization of intra-thalamic nuclei with optimized white-matter-nulled MPRAGE at 7 T. NeuroImage 84:534–545CrossRefPubMed
go back to reference Traynor CR, Barker GJ, Crum WR, Williams SC, Richardson MP (2011) Segmentation of the thalamus in MRI based on T1 and T2. NeuroImage 56:939–950CrossRefPubMed Traynor CR, Barker GJ, Crum WR, Williams SC, Richardson MP (2011) Segmentation of the thalamus in MRI based on T1 and T2. NeuroImage 56:939–950CrossRefPubMed
go back to reference Wassermann D, Descoteaux M, Deriche R (2008) Diffusion maps clustering for magnetic resonance q-ball imaging segmentation. Int J Biomed Imaging 2008:526906CrossRefPubMedPubMedCentral Wassermann D, Descoteaux M, Deriche R (2008) Diffusion maps clustering for magnetic resonance q-ball imaging segmentation. Int J Biomed Imaging 2008:526906CrossRefPubMedPubMedCentral
go back to reference Wedeen VJ, Wang RP, Schmahmann JD, Benner T, Tseng WY, Dai G, Pandya DN, Hagmann P, D’Arceuil H, de Crespigny AJ (2008) Diffusion spectrum magnetic resonance imaging (DSI) tractography of crossing fibers. NeuroImage 41:1267–1277CrossRefPubMed Wedeen VJ, Wang RP, Schmahmann JD, Benner T, Tseng WY, Dai G, Pandya DN, Hagmann P, D’Arceuil H, de Crespigny AJ (2008) Diffusion spectrum magnetic resonance imaging (DSI) tractography of crossing fibers. NeuroImage 41:1267–1277CrossRefPubMed
go back to reference Whitcher B, Tuch DS, Wisco JJ, Sorensen AG, Wang L (2008) Using the wild bootstrap to quantify uncertainty in diffusion tensor imaging. Hum Brain Mapp 29:346–362CrossRefPubMed Whitcher B, Tuch DS, Wisco JJ, Sorensen AG, Wang L (2008) Using the wild bootstrap to quantify uncertainty in diffusion tensor imaging. Hum Brain Mapp 29:346–362CrossRefPubMed
go back to reference Wiegell MR, Tuch DS, Larsson HB, Wedeen VJ (2003) Automatic segmentation of thalamic nuclei from diffusion tensor magnetic resonance imaging. NeuroImage 19:391–401CrossRefPubMed Wiegell MR, Tuch DS, Larsson HB, Wedeen VJ (2003) Automatic segmentation of thalamic nuclei from diffusion tensor magnetic resonance imaging. NeuroImage 19:391–401CrossRefPubMed
go back to reference Ye C, Bogovic JA, Ying SH, Prince JL (2013) Parcellation of the thalamus using diffusion tensor images and a multi-object geometric deformable model. In: Proceedings of SPIE, vol 8669. Proceedings of the international society for optical engineering, vol 8669, 13 Mar 2013. doi:10.1117/12.2006119 Ye C, Bogovic JA, Ying SH, Prince JL (2013) Parcellation of the thalamus using diffusion tensor images and a multi-object geometric deformable model. In: Proceedings of SPIE, vol 8669. Proceedings of the international society for optical engineering, vol 8669, 13 Mar 2013. doi:10.​1117/​12.​2006119
go back to reference Zhang D, Snyder AZ, Shimony JS, Fox MD, Raichle ME (2010) Noninvasive functional and structural connectivity mapping of the human thalamocortical system. Cereb Cortex 20:1187–1194CrossRefPubMed Zhang D, Snyder AZ, Shimony JS, Fox MD, Raichle ME (2010) Noninvasive functional and structural connectivity mapping of the human thalamocortical system. Cereb Cortex 20:1187–1194CrossRefPubMed
go back to reference Ziyan U, Westin CF (2008) Joint segmentation of thalamic nuclei from a population of diffusion tensor MR images. Lect Notes Comput Sci 5241:279–286CrossRef Ziyan U, Westin CF (2008) Joint segmentation of thalamic nuclei from a population of diffusion tensor MR images. Lect Notes Comput Sci 5241:279–286CrossRef
go back to reference Ziyan U, Tuch D, Westin CR (2006) Segmentation of thalamic nuclei from DTI using spectral clustering. Lect Notes Comput Sci 4191:807–814CrossRef Ziyan U, Tuch D, Westin CR (2006) Segmentation of thalamic nuclei from DTI using spectral clustering. Lect Notes Comput Sci 4191:807–814CrossRef
Metadata
Title
Robust thalamic nuclei segmentation method based on local diffusion magnetic resonance properties
Authors
Giovanni Battistella
Elena Najdenovska
Philippe Maeder
Naghmeh Ghazaleh
Alessandro Daducci
Jean-Philippe Thiran
Sébastien Jacquemont
Constantin Tuleasca
Marc Levivier
Meritxell Bach Cuadra
Eleonora Fornari
Publication date
01-07-2017
Publisher
Springer Berlin Heidelberg
Published in
Brain Structure and Function / Issue 5/2017
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-016-1336-4

Other articles of this Issue 5/2017

Brain Structure and Function 5/2017 Go to the issue