Abstract
With the advances in diffusion MRI and tractography, numerous atlases of the human pyramidal tract (PyT) have been proposed, but the inherent limitation of tractography to resolve crossing bundles within the centrum semiovale has so far prevented the complete description of the most lateral PyT projections. Here, we combined a precise manual positioning of individual subcortical regions of interest along the descending pathway of the PyT with a new bundle-specific tractography algorithm. This later is based on anatomical priors to improve streamlines tracking in crossing areas. We then extracted both left and right PyT in a large cohort of 410 healthy participants and built a population-based atlas of the whole-fanning PyT with a complete description of its most corticolateral projections. Clinical applications are envisaged, the whole-fanning PyT atlas being likely a better marker of corticospinal integrity metrics than those currently used within the frame of prediction of poststroke motor recovery. The present population-based PyT, freely available, provides an interesting tool for clinical applications to locate specific PyT damage and its impact to the short- and long-term motor recovery after stroke.
Similar content being viewed by others
References
Angstmann S, Madsen KS, Skimminge A, Jernigan TL, Baare WF, Siebner HR (2016) Microstructural asymmetry of the corticospinal tracts predicts right-left differences in circle drawing skill in right-handed adolescents. Brain Struct Funct 221:4475–4489
Archer DB, Vaillancourt DE, Coombes SA (2018) A template and probabilistic atlas of the human sensorimotor tracts using diffusion MRI. Cereb Cortex 28:1685–1699
Armand J (1982) The origin, course and terminations of corticospinal fibers in various mammals. In: Kuypers HGJM, Martin GF (eds) Progress in brain research, Elsevier, New York, pp 329–360
Avants BB, Tustison NJ, Wu J, Cook PA, Gee JC (2011) An open source multivariate framework for n-tissue segmentation with evaluation on public data. Neuroinformatics 9:381–400
Bigourdan A, Munsch F, Coupe P, Guttmann CR, Sagnier S, Renou P, Debruxelles S, Poli M, Dousset V, Sibon I, Tourdias T (2016) Early fiber number ratio is a surrogate of corticospinal tract integrity and predicts motor recovery after stroke. Stroke 47:1053–1059
Bürgel U, Amunts K, Hoemke L, Mohlberg H, Gilsbach JM, Zilles K (2006) White matter fiber tracts of the human brain: three-dimensional mapping at microscopic resolution, topography and intersubject variability. NeuroImage 29:1092–1105
Catani M, Thiebaut de Schotten M (2008) A diffusion tensor imaging tractography atlas for virtual in vivo dissections. Cortex 44:1105–1132
Côté M-A, Garyfallidis E, Larochelle H, Descoteaux M (2015) Cleaning up the mess: tractography outlier removal using hierarchical QuickBundles clustering. In: 23rd ISMRM Annual Meeting. Toronto, Canada
Curnes JT, Burger PC, Djang WT, Boyko OB (1988) MR imaging of compact white matter pathways. Am J Neuroradiol 9:1061–1068
De Benedictis A, Petit L, Descoteaux M, Marras CE, Barbareschi M, Corsini F, Dallabona M, Chioffi F, Sarubbo S (2016) New insights in the homotopic and heterotopic connectivity of the frontal part of the human corpus callosum revealed by microdissection and diffusion tractography. Hum Brain Mapp 37:4718–4735
Dejerine J, Dejerine-Klumpke A (1901) Anatomie des centres nerveux. Tome 2. Rueff et Cie, Paris
Descoteaux M, Deriche R, Knosche TR, Anwander A (2009) Deterministic and probabilistic tractography based on complex fibre orientation distributions. IEEE Trans Med Imaging 28:269–286
Dhollander T, Emsell L, Van Hecke W, Maes F, Sunaert S, Suetens P (2014) Track orientation density imaging (TODI) and track orientation distribution (TOD) based tractography. NeuroImage 94:312–336
Dum RP, Strick PL (1991) The origin of corticospinal projections from the premotor areas in the frontal lobe. J Neurosci 11:667–689
Ebeling U, Reulen HJ (1992) Subcortical topography and proportions of the pyramidal tract. Acta Neurochir (Wien) 118:164–171
Englander RN, Netsky MG, Adelman LS (1975) Location of human pyramidal tract in the internal capsule: anatomic evidence. Neurology 25:823–826
Farquharson S, Tournier JD, Calamante F, Fabinyi G, Schneider-Kolsky M, Jackson GD, Connelly A (2013) White matter fiber tractography: why we need to move beyond DTI. J Neurosurg 118:1367–1377
Galea MP, Darian-Smith I (1994) Multiple corticospinal neuron populations in the macaque monkey are specified by their unique cortical origins, spinal terminations, and connections. Cereb Cortex 4:166–194
Garyfallidis E, Brett M, Correia MM, Williams GB, Nimmo-Smith I (2012) QuickBundles, a method for tractography simplification. Front Neurosci 6:175
Garyfallidis E, Brett M, Amirbekian B, Rokem A, van der Walt S, Descoteaux M, Nimmo-Smith I, Dipy C (2014) Dipy, a library for the analysis of diffusion MRI data. Front Neuroinform 8:8
Girard G, Whittingstall K, Deriche R, Descoteaux M (2014) Towars quantitative connectivity analysis: Reducing tractography biaises. NeuroImage 98:266–278
Groisser BN, Copen WA, Singhal AB, Hirai KK, Schaechter JD (2014) Corticospinal tract diffusion abnormalities early after stroke predict motor outcome. Neurorehabilit Neural Repair 28:751–760
Hau J, Sarubbo S, Houde JC, Corsini F, Girard G, Deledalle C, Crivello F, Zago L, Mellet E, Jobard G, Joliot M, Mazoyer B, Tzourio-Mazoyer N, Descoteaux M, Petit L (2017) Revisiting the human uncinate fasciculus, its subcomponents and asymmetries with stem-based tractography and microdissection validation. Brain Struct Funct 222:1645–1662
Hervé P-Y, Leonard G, Perron M, Pike B, Pitiot A, Richer L, Veillette S, Pausova Z, Paus T (2009) Handedness, motor skills and maturation of the corticospinal tract in the adolescent brain. Hum Brain Mapp 30:3151–3162
Hervé P-Y, Cox EF, Lotfipour AK, Mougin OE, Bowtell RW, Gowland PA, Paus T (2011) Structural properties of the corticospinal tract in the human brain: a magnetic resonance imaging study at 7 T. Brain Struct Funct 216:255–262
Jane JA, Yashon D, DeMyer W, Bucy PC (1967) The contribution of the precentral gyrus to the pyramidal tract of man. J Neurosurg 26:244–248
Jbabdi S, Behrens TEJ (2012) Specialization: the connections have it. Nat Neurosci 15:171–172
Jbabdi S, Sotiropoulos SN, Haber SN, Van Essen DC, Behrens TE (2015) Measuring macroscopic brain connections in vivo. Nat Neurosci 18:1546–1555
Jones DK, Knosche TR, Turner R (2013) White matter integrity, fiber count, and other fallacies: the do’s and don’ts of diffusion MRI. Neuroimage 73:239–254
Kretschmann HJ (1988) Localisation of the corticospinal fibres in the internal capsule in man. J Anat 160:219–225
Kumar A, Juhasz C, Asano E, Sundaram SK, Makki MI, Chugani DC, Chugani HT (2009) Diffusion tensor imaging study of the cortical origin and course of the corticospinal tract in healthy children. Am J Neuroradiol 30:1963–1970
Kwon HG, Hong JH, Jang SH (2011) Anatomic location and somatotopic arrangement of the corticospinal tract at the cerebral peduncle in the human brain. Am J Neuroradiol 32:2116–2119
Maier-Hein KH et al (2017) The challenge of mapping the human connectome based on diffusion tractography. Nat Commun 8:1349
Mayka MA, Corcos DM, Leurgans SE, Vaillancourt DE (2006) Three-dimensional locations and boundaries of motor and premotor cortices as defined by functional brain imaging: a meta-analysis. NeuroImage 31:1453
Mazoyer B, Mellet E, Perchey G, Zago L, Crivello F, Jobard G, Delcroix N, Vigneau M, Leroux G, Petit L, Joliot M, Tzourio-Mazoyer N (2016) BIL&GIN: a neuroimaging, cognitive, behavioral, and genetic database for the study of human brain lateralization. Neuroimage 124 Part B:1225–1231
Mirowitz S, Sartor K, Gado M, Torack R (1989) Focal signal-intensity variations in the posterior internal capsule: normal MR findings and distinction from pathologic findings. Radiology 172:535–539
Nathan PW, Smith MC (1955) Long descending tracts in man: I. review of present knowledge. Brain 78:248–303
Nieuwenhuys R, Voogd J, van Huijzen C (2008) The human central nervous system, 4th edn. Springer-Verlag, Berlin
Nyberg-Hansen R, Rinvik E (1963) Some comments on the pyramidal tract, with special reference to its individual variations in man. Acta Neurol Scand 39:1–30
Penfield W, Boldrey E (1937) Somatic motor and sensory representation in the cerebral cortex of man as studied by electrical stimulation. Brain 60:389–443
Rheault F, St-Onge E, Tzourio-Mazoyer N, Sidhu J, Petit L, Descoteaux M (2018) Bundle-specific tractography: enhancing fiber tracking with additional anatomical and orientational priors. NeuroImage. https://doi.org/10.1016/j.neuroimage.2018.11.018
Rojkova K, Volle E, Urbanski M, Humbert F, Dell’Acqua F, Thiebaut de Schotten M (2016) Atlasing the frontal lobe connections and their variability due to age and education: a spherical deconvolution tractography study. Brain Struct Funct 221:1751–1766
Ross ED (1980) Localization of the pyramidal tract in the internal capsule by whole brain dissection. Neurology 30:59–64
Seo JP, Jang SH (2013) Different characteristics of the corticospinal tract according to the cerebral origin: DTI study. AJNR 34:1359–1363
Smith SM, Jenkinson M, Woolrich MW, Beckmann CF, Behrens TEJ, Johansen-Berg H, Bannister PR, De Luca M, Drobnjak I, Flitney DE, Niazy RK, Saunders J, Vickers J, Zhang Y, De Stefano N, Brady JM, Matthews PM (2004) Advances in functional and structural MR image analysis and implementation as FSL. NeuroImage 23 Supplement 1:S208–S219
Thiebaut de Schotten M, Ffytche D, Bizzi A, Dell’acqua F, Allin M, Walshe M, Murray R, Williams S, Murphy DGM, Catani M (2011) Atlasing location, asymmetry and inter-subject variability of white matter tracts in the human brain with MR diffusion tractography. NeuroImage 54:49–59
Volz LJ, Cieslak M, Grafton ST (2018) A probabilistic atlas of fiber crossings for variability reduction of anisotropy measures. Brain Struct Funct 223:635–651
Yagishita A, Nakano I, Oda M, Hirano A (1994) Location of the corticospinal tract in the internal capsule at MR imaging. Radiology 191:455–460
Yendiki A, Panneck P, Srinivasan P, Stevens A, Zollei L, Augustinack J, Wang R, Salat D, Ehrlich S, Behrens T, 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 A, 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
Zolal A, Vachata P, Hejčl A, Bartoš R, Malucelli A, Nováková M, Derner M, Sameš M (2012) Anatomy of the supraventricular portion of the pyramidal tract. Acta Neurochir (Wien) 154:1097–1104
Acknowledgements
We are grateful to Dr. Thomas Tourdias for the helpful comments and discussion.
Funding
No specific funding to mention.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
No conflicts of interest.
Ethical approval
The study was approved by the local ethics committee (CCPRB Basse-Normandie).
Informed consent
All participants gave written consent prior to participation in the study.
Research involving human participants
The current research involved human participants.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Chenot, Q., Tzourio-Mazoyer, N., Rheault, F. et al. A population-based atlas of the human pyramidal tract in 410 healthy participants. Brain Struct Funct 224, 599–612 (2019). https://doi.org/10.1007/s00429-018-1798-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00429-018-1798-7