Hostname: page-component-7c8c6479df-8mjnm Total loading time: 0 Render date: 2024-03-28T16:16:26.172Z Has data issue: false hasContentIssue false

Tractography in the Study of the Human Brain: A Neurosurgical Perspective

Published online by Cambridge University Press:  02 December 2014

David Fortin*
Affiliation:
Division of neurosurgery and neuro-oncology, Faculté de medicine et des sciences de la santé
Camille Aubin-Lemay
Affiliation:
Division of neurosurgery and neuro-oncology, Faculté de medicine et des sciences de la santé
Arnaud Boré
Affiliation:
Sherbrooke Connectivity Imaging Laboratory (SCIL), Computer Science Department, Université de Sherbrooke, Sherbrooke, Québec, Canada
Gabriel Girard
Affiliation:
Sherbrooke Connectivity Imaging Laboratory (SCIL), Computer Science Department, Université de Sherbrooke, Sherbrooke, Québec, Canada
Jean-Christophe Houde
Affiliation:
Sherbrooke Connectivity Imaging Laboratory (SCIL), Computer Science Department, Université de Sherbrooke, Sherbrooke, Québec, Canada
Kevin Whittingstall
Affiliation:
Diagnostic Radiology Department, Faculté de medicine et des sciences de la santé
Maxime Descoteaux
Affiliation:
Sherbrooke Connectivity Imaging Laboratory (SCIL), Computer Science Department, Université de Sherbrooke, Sherbrooke, Québec, Canada
*
Université de Sherbrooke, Division of Neurosurgery and Neuro-oncology, 3001, 12th Avenue North, Sherbrooke (Québec) J1H 5N4, Canada. Email: david.fortin@usherbrooke.ca
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.
Background:

The brain functions as an integrated multi-networked organ. Complex neurocognitive functions are not attributed to a single brain area but depend on the dynamic interactions of distributed brain areas operating in large-scale networks. This is especially important in the field of neurosurgery where intervention within a spatially localized area may indirectly lead to unwanted effects on distant areas. As part of a preliminary integrated work on functional connectivity, we present our initial work on diffusion tensor imaging tractography to produce in vivo white matter tracts dissection.

Methods:

Diffusion weighted data and high-resolution T1-weighted images were acquired from a healthy right-handed volunteer (25 years old) on a whole-body 3 T scanner. Two approaches were used to dissect the tractography results: 1) a standard region of interest technique and 2) the use of Brodmann's area as seeding points, which represents an innovation in terms of seeds initiation.

Results:

Results are presented as tri-dimensional tractography images. The uncinate fasciculus, the inferior longitudinal fasciculus, the inferior fronto-occipital fasiculus, the corticospinal tract, the corpus callosum, the cingulum, and the optic radiations where studied by conventional seeding approach, while Broca's and Wernicke's areas, the primary motor as well as the primary visual cortices were used as seeding areas in the second approach.

Conclusions:

We report state-of-the-art tractography results of some of the major white matter bundles in a normal subject using DTI. Moreover, we used Brodmann's area as seeding areas for fiber tracts to study the connectivity of known major functional cortical areas.

Résumé

RÉSUMÉContexte:

Le cerveau fonctionne comme un organe constitué en multiréseaux intégrés et les fonctions neurocognitives complexes ne sont pas restreintes à une seule zone du cerveau. Elles dépendent d'interactions dynamiques de différentes régions du cerveau opérant en réseaux de grande envergure. Ceci est particulièrement important dans le domaine de la neurochirurgie où une intervention à l'intérieur d'une zone très localisée peut provoquer indirectement des effets indésirables à distance. Nous présentons, dans le cadre d'un travail intégré préliminaire sur la connectivité fonctionnelle, nos travaux initiaux sur la tractographie par IRM de diffusion pour obtenir in vivo la dissection de faisceaux de la substance blanche.

Méthode:

Des données de l'IRM pondérée en diffusion et des images de haute résolution pondérées en T1 ont été acquises chez un volontaire sain droitier de 25 ans au moyen d'un scanner T3 du corps entier. Deux approches ont été utilisées pour disséquer les résultats de la tractographie: 1) une technique standard ciblant une région spécifique et 2) l'utilisation de la zone de Brodmann comme point d'essaimage, ce qui constitue une innovation.

Résultats:

Nous présentons des images de tractographie tridimensionnelles. Le faisceau unciné, le faisceau longitudinal inférieur, le faisceau fronto-occipital inférieur, le faisceau pyramidal, le corps calleux, le cingulum et les radiations optiques de Gratiolet ont été étudiés par la méthode d'essaimage conventionnelle alors que les zones de Broca et de Wernicke ainsi que les cortex primaires moteurs et visuels ont été utilisés comme zones d'essaimage dans la deuxième approche.

Conclusions:

Nous rapportons des résultats de tractographie par IRM de diffusion, une technologie de pointe, de certains des faisceaux importants de la substance blanche chez un sujet normal. De plus, nous avons utilisé la zone de Brodmann comme zone d'essaimage afin d'étudier la connectivité des zones corticales fonctionnelles majeures connues.

Type
Original Articles
Copyright
Copyright © The Canadian Journal of Neurological 2012

References

1. de Benedictis, A, Duffau, H. Brain hodotopy: from esoteric concept to practical surgical applications. Neurosurgery. 2011;68(6):170923.Google Scholar
2. Broadmann, K. Vergleichende Lokalisationslehre der Grosshirnrinde. Verlag von Johann Ambrosius Barth. Leipzig. 1990.Google Scholar
3. Duffau, H. Nouveautés thérapeutiques chirurgicales dans les gliomes diffus de bas grade: cartographie cérébrale, hodotopie et neuroplasticité. Bull Acad Natl Med. 2011;195(1):3749.Google Scholar
4. Duffau, H. Introduction. Surgery of gliomas in eloquent areas: from brain hodotopy and plasticity to functional neurooncology. Neurosurg Focus. 2010;28(2).CrossRefGoogle ScholarPubMed
5. Bressler, SL, Menon, V. Large-scale brain networks in cognition: emerging methods and principles. Trends Cogn Sci. 2010;14(6): 27790.CrossRefGoogle ScholarPubMed
6. Young, MP, Scannell, JW, Burns, GA, Blakemore, C. Analysis of connectivity: neural systems in the cerebral cortex. Rev Neurosci. 1994;5(3):27250.CrossRefGoogle ScholarPubMed
7. Honey, CJ, Kötter, R, Breakspear, M, Sporns, O. Network structure of cerebral cortex shapes functional connectivity on multiple time scales. Proc Natl Acad Sci USA. 2007;104(24):102405.CrossRefGoogle ScholarPubMed
8. Passingham, RE, Stephan, KE, Kötter, R. The anatomical basis of functional localization in the cortex. Nat Rev Neurosci. 2002;3(8):60616.CrossRefGoogle ScholarPubMed
9. Catani, M, Howard, RJ, Pajevic, S, Jones, DK. Virtual in vivo interactive dissection of white matter fasciculi in the human brain. Neuroimage. 2002;17(1):7794.CrossRefGoogle ScholarPubMed
10. Behrens, TH, Johansen-Berg, H. Diffusion MRI: From quantitative measurement to in-vivo neuroanatomy. Amsterdam. Elsevier. 2009.Google Scholar
11. Jones, DK. Diffusion MRI: theory, methods and applications. New York. Oxford University Press. 2010.Google Scholar
12. Descoteaux, M, Deriche, R, Knoesche, T, Anwander, A. Deterministic and probabilistic tractography based on complex fiber orientation distributions. IEEE Trans Med Imaging. 2009;28(2):26986.CrossRefGoogle Scholar
13. Descoteaux, M, Poupon, C. Diffusion-weighted MRI. In: Comprehensive biomedical physics. Belvic, D, Belvic, K, editors. Elsevier. Forthcoming 2012.Google Scholar
14. Anwander, A, Tittgemeyer, M, Von Cramon, DY, Friederici, AD, Knosche, TR. Connectivity-based parcellation of Broca’s area. Cereb Cortex. 2007;17(4):81625.Google Scholar
15. Jones, DK. The effect of gradient sampling schemes on measures derived from diffusion tensor MRI: a Monte Carlo study. Magn Reson Med. 2004;51:80715.CrossRefGoogle ScholarPubMed
16. Talairach, J, Tournoux, P. Coplanar stereotaxic atlas of the human brain: 3-dimensional proportional system: an approach to cerebral imaging. Amsterdam. Thieme Medical Publishers; 1988.Google Scholar
17. Smith, SM, Jenkinson, M, Woolrich, MW, et al. Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage. [serial on the Internet]. 2004;23(S1):208-19. Available from: http://www.fmrib.ox.ac.uk/fsl/ CrossRefGoogle ScholarPubMed
18. MedINRIA [homepage on the Internet]. Asclepios Research Project. Inria Sophia Antipolis. Available from: http://www-sop.inria.fr/asclepios/software/MedINRIA/index.php Google Scholar
19. Fibernavigator [homepage on the Internet]. Google Project Hosting. Available from: http://code.google.com/p/fibernavigator/ Google Scholar
20. Mori, S, Kaufmann, WE, Davatzikos, C, et al. Imaging cortical association tracts in the human brain using diffusion-tensor-based axonal tracking. Magn Reson Med. 2002;47(2):21523.Google Scholar
21. Blumenfeld, H. Neuroanatomy through clinical cases. 1st ed. Sunderland. Sinauer Associates. January 2002.Google Scholar
22. Conturo, TE, Lori, NF, Cull, TS, et al. Tracking neuronal fiber pathways in the living human brain. Proc Natl Acad Sci. 1999;96:104227.CrossRefGoogle ScholarPubMed
23. MRIcro [homepage on the Internet]. Colombia: Chris Rorden. Available from: http://www.cabiatl.com/mricro/mricro/index.html Google Scholar
24. Catani, M, Mesulam, M. The arcuate fasciculus and the disconnection theme in language and aphasia: history and current state. Cortex. 2008;44(8):95361.CrossRefGoogle ScholarPubMed
25. Shinoura, N, Suzuki, Y, Tsukada, M, et al. Deficits in the left inferior longitudinal fasciculus results in impairments in object naming. Neurocase. 2010;16(2):1359.CrossRefGoogle ScholarPubMed
26. Shinoura, N, Suzuki, Y, Yamada, R, Tabei, Y, Saito, K, Yagi, K. Damage to the right superior longitudinal fasciculus in the inferior parietal lobe plays a role in spatial neglect. Neuropsychologia. 2009;47(12):26003.Google Scholar
27. Ebeling, U, von Cramon, D. Topography of the uncinate fascicle and adjacent temporal fiber tracts. Acta Neurochir (Wien). 1992;115:1438.Google Scholar
28. Schmahmann, JD, Pandya, DN, Wang, R, et al. Association fibre pathways of the brain: parallel observations from diffusion spectrum imaging and autoradiography. Brain. 2007;130:63053.CrossRefGoogle ScholarPubMed
29. Sincoff, EH, Tan, Y, Abdulrauf, SI. White matter fiber dissection of the optic radiations of the temporal lobe and implications for surgical approaches to the temporal horn. J Neurosurg. 2004;101:73946.CrossRefGoogle Scholar
30. Papagno, C. Naming and the role of the uncinate fasciculus in language function. Curr Neurol Neurosci Rep. 2011;11(6):5539.CrossRefGoogle ScholarPubMed
31. Papagno, C, Miracapillo, C, Casarotti, A, et al. What is the role of the uncinate fasciculus? Surgical removal and proper name retrieval. Brain. 2011 Feb;134(Pt 2):40514.CrossRefGoogle ScholarPubMed
32. Dejerine, J. Anatomie des Centres Nerveux. Vol. 1, Paris: Rueff et Cie. 1895.Google Scholar
33. Martino, J, Brogna, C. Anatomy of the white-matter pathways. In: Brain Mapping, editors. Wien. Springer-Verlag. 2011. p. 2741.CrossRefGoogle Scholar
34. Shinoura, N, Suzuki, Y, Tsukada, M, et al. Deficits in the left inferior longitudinal fasciculus results in impairments in object naming. Neurocase. 2010;16(2):1359.CrossRefGoogle ScholarPubMed
35. Gloor, P. The temporal lobe and the limbic system. New York: Oxford Univ Press; 1997.Google Scholar
36. Crosby, EC, Humphrey, T, Lauer, EW. Correlative anatomy of the nervous system. New York: Macmillian Co; 1962.Google Scholar
37. Philippi, CL, Mehta, S, Grabowski, T, Adolphs, R, Rudrauf, D. Damage to association fiber tracts impairs recognition of the facial expression of emotion. J Neurosci. 2009;29(48):1508999.CrossRefGoogle ScholarPubMed
38. Leclercq, D, Delmaire, C, De Champfleur, NM, Chiras, J, Lehericy, S. Diffusion tractography: methods, validation and applications in patients with neurosurgical lesions. Neurosurg Clin N Am. 2011;22(2):25368.CrossRefGoogle Scholar
39. Krieg, S.M, Buchmann, NH, Gempt, J, Shiban, E, Meyer, B, Ringel, F. Diffusion tensor imaging fiber tracking using navigated brain stimulation-a feasibility study. Acta Neurochir (Wien). 2012 Mar;154(3):55563.Google Scholar
40. Romano, A, D’Andrea, G, Calabria, LF, et al. Pre- and intraoperative tractographic evaluation of corticospinal tract shift. Neurosurgery. 2011;69(3):696704.CrossRefGoogle ScholarPubMed
41. Buchmann, N, Gempt, J, Stoffel, M, Foerschler, A, Meyer, B, Ringel, F. Utility of diffusion tensor-imaged (DTI) motor fiber tracking for the resection of intracranial tumors near the corticospinal tract. Acta Neurochir. 2011;153(1):6874.CrossRefGoogle ScholarPubMed
42. Morita, N, Wang, S, Kadakia, P, Chawla, S, Poptani, H, Melhem, ER. Diffusion tensor imaging of the corticospinal tract in patients with brain neoplasms. Magn Reson Med Sci. 2011;10(4):23943.CrossRefGoogle ScholarPubMed
43. Bello, L, Gambini, A, Castellano, A, et al. Motor and language DTI Fiber Tracking combined with intraoperative subcortical mapping for surgical removal of gliomas. Neuroimage. 2008;39(1):36982.CrossRefGoogle ScholarPubMed
44. Hofer, S, Karaus, A, Frahm, J. Reconstruction and dissection of the entire human visual pathway using diffusion tensor MRI. Front Neuroanat. 2010;4:15.Google ScholarPubMed
45. Kitajima, M, Korogi, Y, Takahashi, M, Eto, K. MR signal intensity of the optic radiation. Am J Neuroradiol. 1996;17:137983.Google ScholarPubMed
46. Brodmann, K. Vergleichende Lokalisationslehre der Grosshirnrinde in ihren Prinzipien dargestellt auf Grund des Zellenbaues. Leipzig: J. A. Barth. 1909.Google Scholar
47. Geyer, S, Matelli, M, Luppino, G, Zilles, K. Functional neuroanatomy of the primate isocortical motor system. Anat Embryol (Berl). 2000;202(6):44374.CrossRefGoogle ScholarPubMed
48. Zilles, K, Schlaug, G, Geyer, S, et al. Anatomy and transmitter receptors of the supplementary motor areas in the human and nonhuman primate brain. Adv Neurol. 1996;70:2943.Google ScholarPubMed
49. Yasargil, MG. Microneurosurgery. vol 4a. New York: Georg Thieme Verlag Stuttgart. 1994.Google Scholar
50. McGirt, MJ, Chaichana, KL, Gathinji, M, et al. Independent association of extent of resection with survival in patients with malignant brain astrocytoma. J Neurosurg. 2009;110(1):15662.Google Scholar
51. Sanai, N, Berger, MS. Glioma extent of resection and its impact on patient outcome. Neurosurgery. 2008;62(4):75364.CrossRefGoogle ScholarPubMed
52. McGirt, MJ, Mukherjee, D, Chaichana, KL, Than, KD, Weingart, JD, Quinones-Hinojosa, A. Association of surgically acquired motor and language deficits on overall survival after resection of glioblastoma multiforme. Neurosurgery. 2009;65(3):4639.CrossRefGoogle ScholarPubMed
53. Dea, N, Fournier-Gosselin, MP, Mathieu, D, Fortin, D: Does extent of resection impact survival in patients bearing glioblastoma? CJNS. 2012, in press.Google Scholar
54. Ojemann, G, Ojemann, J, Lettich, E, Berger, M. Cortical language localization in left, dominant hemisphere. An electrical stimulation mapping investigation in 117 patients. J Neurosurg. 1989;71(3):31626.Google Scholar
55. Veilleux, N, Goffaux, P, Boudrias, M, Mathieu, D, Daigle, K, Fortin, D. Quality of life in neurooncology-age matters. J Neurosurg. 2010;113(2):32532.Google Scholar
56. Goffaux, P, Boudrias, M, Mathieu, D, Charpentier, C, Veilleux, N, Fortin, D. Development of a concise QOL questionnaire for brain tumor patients. Can J Neurol Sci. 2009;36(3):3408.CrossRefGoogle ScholarPubMed
57. Goffaux, P, Daigle, K, Fortin, D. Patients with brain cancer: health related quality of life. M. A. Hayat, editors. Tumors of the Central Nervous System, Vol. 4, 2012;341.Google Scholar
58. Cammoun, L, Gigandet, X, Meskaldji, D, et al. Mapping the human connectome at multiple scales with diffusion spectrum MRI. J Neurosci Methods. 2012;203(2):38697.CrossRefGoogle ScholarPubMed
59. Duffau, H. The anatomo-functional connectivity of language revisited: new insights provided by electrostimulation and tractography. Neuropsychologia. 2008;4:92734.CrossRefGoogle Scholar
60. Duffau, H. Lessons from brain mapping in surgery for low-grade glioma: insights into associations between tumour and brain plasticity. Lancet Neurol. 2005;4:47686.Google Scholar
61. Quiñones-Hinojosa, A, Ojemann, SG, Sanai, N, Dillon, WP, Berger, MS. Preoperative correlation of intraoperative cortical mapping with magnetic resonance imaging landmarks to predict localization of the broca area. J Neurosurg. 2003;99:31118.Google Scholar
62. Tournier, JD, Calamante, F, Connelly, A. MRtrix: Diffusion tractography in crossing fiber regions. Int J Imag Sys Tech. 2012; 22(1):5366.CrossRefGoogle Scholar