Advertisement

Brain Structure and Function

, Volume 224, Issue 2, pp 599–612 | Cite as

A population-based atlas of the human pyramidal tract in 410 healthy participants

  • Quentin Chenot
  • Nathalie Tzourio-Mazoyer
  • François Rheault
  • Maxime Descoteaux
  • Fabrice Crivello
  • Laure Zago
  • Emmanuel Mellet
  • Gaël Jobard
  • Marc Joliot
  • Bernard Mazoyer
  • Laurent PetitEmail author
Original Article
  • 117 Downloads

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.

Keywords

White-matter anatomy Pyramidal tract Corticospinal tract Corticobulbar tract Healthy human Diffusion imaging Tractography 

Notes

Acknowledgements

We are grateful to Dr. Thomas Tourdias for the helpful comments and discussion.

Funding

No specific funding to mention.

Compliance with ethical standards

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.

Supplementary material

429_2018_1798_MOESM1_ESM.pdf (4.2 mb)
Supplementary material 1 (PDF 4308 KB)
429_2018_1798_MOESM2_ESM.pdf (15.3 mb)
Supplementary material 2 (PDF 15659 KB)

References

  1. 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 221:4475–4489CrossRefPubMedPubMedCentralGoogle Scholar
  2. Archer DB, Vaillancourt DE, Coombes SA (2018) A template and probabilistic atlas of the human sensorimotor tracts using diffusion MRI. Cereb Cortex 28:1685–1699CrossRefPubMedGoogle Scholar
  3. 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 329–360Google Scholar
  4. 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 9:381–400CrossRefPubMedPubMedCentralGoogle Scholar
  5. 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 47:1053–1059CrossRefPubMedGoogle Scholar
  6. 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 29:1092–1105CrossRefPubMedGoogle Scholar
  7. Catani M, Thiebaut de Schotten M (2008) A diffusion tensor imaging tractography atlas for virtual in vivo dissections. Cortex 44:1105–1132CrossRefPubMedGoogle Scholar
  8. 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, CanadaGoogle Scholar
  9. Curnes JT, Burger PC, Djang WT, Boyko OB (1988) MR imaging of compact white matter pathways. Am J Neuroradiol 9:1061–1068PubMedGoogle Scholar
  10. 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 37:4718–4735CrossRefPubMedGoogle Scholar
  11. Dejerine J, Dejerine-Klumpke A (1901) Anatomie des centres nerveux. Tome 2. Rueff et Cie, ParisGoogle Scholar
  12. Descoteaux M, Deriche R, Knosche TR, Anwander A (2009) Deterministic and probabilistic tractography based on complex fibre orientation distributions. IEEE Trans Med Imaging 28:269–286CrossRefPubMedGoogle Scholar
  13. 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 94:312–336CrossRefPubMedGoogle Scholar
  14. Dum RP, Strick PL (1991) The origin of corticospinal projections from the premotor areas in the frontal lobe. J Neurosci 11:667–689CrossRefPubMedGoogle Scholar
  15. Ebeling U, Reulen HJ (1992) Subcortical topography and proportions of the pyramidal tract. Acta Neurochir (Wien) 118:164–171CrossRefGoogle Scholar
  16. Englander RN, Netsky MG, Adelman LS (1975) Location of human pyramidal tract in the internal capsule: anatomic evidence. Neurology 25:823–826CrossRefPubMedGoogle Scholar
  17. 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 118:1367–1377CrossRefPubMedGoogle Scholar
  18. 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 4:166–194CrossRefPubMedGoogle Scholar
  19. Garyfallidis E, Brett M, Correia MM, Williams GB, Nimmo-Smith I (2012) QuickBundles, a method for tractography simplification. Front Neurosci 6:175CrossRefPubMedPubMedCentralGoogle Scholar
  20. 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 8:8CrossRefPubMedPubMedCentralGoogle Scholar
  21. Girard G, Whittingstall K, Deriche R, Descoteaux M (2014) Towars quantitative connectivity analysis: Reducing tractography biaises. NeuroImage 98:266–278CrossRefPubMedGoogle Scholar
  22. Groisser BN, Copen WA, Singhal AB, Hirai KK, Schaechter JD (2014) Corticospinal tract diffusion abnormalities early after stroke predict motor outcome. Neurorehabilit Neural Repair 28:751–760CrossRefGoogle Scholar
  23. 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 222:1645–1662CrossRefPubMedGoogle Scholar
  24. 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 30:3151–3162CrossRefPubMedGoogle Scholar
  25. 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 216:255–262CrossRefPubMedGoogle Scholar
  26. Jane JA, Yashon D, DeMyer W, Bucy PC (1967) The contribution of the precentral gyrus to the pyramidal tract of man. J Neurosurg 26:244–248CrossRefPubMedGoogle Scholar
  27. Jbabdi S, Behrens TEJ (2012) Specialization: the connections have it. Nat Neurosci 15:171–172CrossRefPubMedGoogle Scholar
  28. Jbabdi S, Sotiropoulos SN, Haber SN, Van Essen DC, Behrens TE (2015) Measuring macroscopic brain connections in vivo. Nat Neurosci 18:1546–1555CrossRefPubMedGoogle Scholar
  29. 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 73:239–254CrossRefPubMedGoogle Scholar
  30. Kretschmann HJ (1988) Localisation of the corticospinal fibres in the internal capsule in man. J Anat 160:219–225PubMedPubMedCentralGoogle Scholar
  31. 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 30:1963–1970CrossRefPubMedGoogle Scholar
  32. 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 32:2116–2119CrossRefPubMedGoogle Scholar
  33. Maier-Hein KH et al (2017) The challenge of mapping the human connectome based on diffusion tractography. Nat Commun 8:1349CrossRefPubMedPubMedCentralGoogle Scholar
  34. 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 31:1453CrossRefPubMedPubMedCentralGoogle Scholar
  35. 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:1225–1231CrossRefGoogle Scholar
  36. 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 172:535–539CrossRefPubMedGoogle Scholar
  37. Nathan PW, Smith MC (1955) Long descending tracts in man: I. review of present knowledge. Brain 78:248–303CrossRefPubMedGoogle Scholar
  38. Nieuwenhuys R, Voogd J, van Huijzen C (2008) The human central nervous system, 4th edn. Springer-Verlag, BerlinCrossRefGoogle Scholar
  39. Nyberg-Hansen R, Rinvik E (1963) Some comments on the pyramidal tract, with special reference to its individual variations in man. Acta Neurol Scand 39:1–30CrossRefGoogle Scholar
  40. Penfield W, Boldrey E (1937) Somatic motor and sensory representation in the cerebral cortex of man as studied by electrical stimulation. Brain 60:389–443CrossRefGoogle Scholar
  41. 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 Google Scholar
  42. 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 221:1751–1766CrossRefPubMedGoogle Scholar
  43. Ross ED (1980) Localization of the pyramidal tract in the internal capsule by whole brain dissection. Neurology 30:59–64CrossRefPubMedGoogle Scholar
  44. Seo JP, Jang SH (2013) Different characteristics of the corticospinal tract according to the cerebral origin: DTI study. AJNR 34:1359–1363CrossRefPubMedGoogle Scholar
  45. 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–S219CrossRefPubMedGoogle Scholar
  46. 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 54:49–59CrossRefPubMedGoogle Scholar
  47. Volz LJ, Cieslak M, Grafton ST (2018) A probabilistic atlas of fiber crossings for variability reduction of anisotropy measures. Brain Struct Funct 223:635–651CrossRefPubMedGoogle Scholar
  48. Yagishita A, Nakano I, Oda M, Hirano A (1994) Location of the corticospinal tract in the internal capsule at MR imaging. Radiology 191:455–460CrossRefPubMedGoogle Scholar
  49. 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 5:23CrossRefPubMedPubMedCentralGoogle Scholar
  50. 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 52:1289–1301CrossRefPubMedPubMedCentralGoogle Scholar
  51. 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) 154:1097–1104CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Quentin Chenot
    • 1
  • Nathalie Tzourio-Mazoyer
    • 1
  • François Rheault
    • 2
  • Maxime Descoteaux
    • 2
  • Fabrice Crivello
    • 1
  • Laure Zago
    • 1
  • Emmanuel Mellet
    • 1
  • Gaël Jobard
    • 1
  • Marc Joliot
    • 1
  • Bernard Mazoyer
    • 1
  • Laurent Petit
    • 1
    Email author
  1. 1.Groupe d’Imagerie Neurofonctionnelle, Institut des Maladies NeurodégénérativesUMR 5293, CNRS, CEA University of Bordeaux, Case 28, Centre Broca Nouvelle-AquitaineBordeaux CedexFrance
  2. 2.Sherbrooke Connectivity Imaging LabUniversity of SherbrookeSherbrookeCanada

Personalised recommendations