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Acta Neurochirurgica

, Volume 158, Issue 11, pp 2185–2193 | Cite as

The evolving utility of diffusion tensor tractography in the surgical management of temporal lobe epilepsy: a review

  • Sananthan SivakanthanEmail author
  • Elliot Neal
  • Ryan Murtagh
  • Fernando L. Vale
Review Article - Functional

Abstract

Background

Diffusion tensor imaging (DTI) is a relatively new imaging modality that has found many peri-operative applications in neurosurgery.

Methods

A comprehensive survey of the applications of diffusion tensor imaging (DTI) in planning for temporal lobe epilepsy surgery was conducted. The presentation of this literature is supplemented by a case illustration.

Results

The authors have found that DTI is well utilized in epilepsy surgery, primarily in the tractography of Meyer’s loop. DTI has also been used to demonstrate extratemporal connections that may be responsible for surgical failure as well as perioperative planning. The tractographic anatomy of the temporal lobe is discussed and presented with original DTI pictures.

Conclusions

The uses of DTI in epilepsy surgery are varied and rapidly evolving. A discussion of the technology, its limitations, and its applications is well warranted and presented in this article.

Keywords

Diffusion tensor imaging Temporal lobe epilepsy Perioperative planning 

Notes

Compliance with ethical standards

Funding

No funding was received for this research.

Conflicts of interest

Author Mr. Elliot Neal is an employee of Brainlab Inc. The other authors have nothing to disclose.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.

Informed consent

Informed consent was obtained from all individual participants included in the study.

Supplementary material

Supplemental Video

Three dimensional tractography anatomy of the temporal lobe. Supplemental video is original. (MP4 30290 kb)

References

  1. 1.
    Borius PY, Roux FE, Valton L, Sol JC, Lotterie JA, Berry I (2014) Can DTI fiber tracking of the optic radiations predict visual deficit after surgery? Clin Neurol Neurosurg 122:87–91CrossRefPubMedGoogle Scholar
  2. 2.
    Campbell JS, Pike GB (2014) Potential and limitations of diffusion MRI tractography for the study of language. Brain Lang 131:65–73CrossRefPubMedGoogle Scholar
  3. 3.
    Chen X, Weigel D, Ganslandt O, Buchfelder M, Nimsky C (2009) Prediction of visual field deficits by diffusion tensor imaging in temporal lobe epilepsy surgery. Neuroimage 45:286–297CrossRefPubMedGoogle Scholar
  4. 4.
    Choi C, Rubino PA, Fernandez-Miranda JC, Abe H, Rhoton AL, Jr. (2006) Meyer’s loop and the optic radiations in the transsylvian approach to the mediobasal temporal lobe. Neurosurgery 59:ONS228-235; discussion ONS235-226Google Scholar
  5. 5.
    Colnat-Coulbois S, Mok K, Klein D, Penicaud S, Tanriverdi T, Olivier A (2010) Tractography of the amygdala and hippocampus: anatomical study and application to selective amygdalohippocampectomy. J Neurosurg 113:1135–1143CrossRefPubMedGoogle Scholar
  6. 6.
    Cui Z, Ling Z, Pan L, Song H, Chen X, Shi W, Liu Z, Wang Q, Zhang Z, Li Y, Wang X, Qing Y, Xu X, Mao Z, Xu B, Yu X, Luan G (2015) Optic radiation mapping reduces the risk of visual field deficits in anterior temporal lobe resection. Int J Clin Exp Med 8:14283–14295PubMedPubMedCentralGoogle Scholar
  7. 7.
    Daga P, Winston G, Modat M, White M, Mancini L, Cardoso MJ, Symms M, Stretton J, McEvoy AW, Thornton J, Micallef C, Yousry T, Hawkes DJ, Duncan JS, Ourselin S (2012) Accurate localization of optic radiation during neurosurgery in an interventional MRI suite. IEEE Trans Med Imaging 31:882–891CrossRefPubMedGoogle Scholar
  8. 8.
    Douek P, Turner R, Pekar J, Patronas N, Le Bihan D (1991) MR color mapping of myelin fiber orientation. J Comput Assist Tomogr 15:923–929CrossRefPubMedGoogle Scholar
  9. 9.
    Gleissner U, Helmstaedter C, Schramm J, Elger CE (2004) Memory outcome after selective amygdalohippocampectomy in patients with temporal lobe epilepsy: one-year follow-up. Epilepsia 45:960–962CrossRefPubMedGoogle Scholar
  10. 10.
    Guye M, Regis J, Tamura M, Wendling F, McGonigal A, Chauvel P, Bartolomei F (2006) The role of corticothalamic coupling in human temporal lobe epilepsy. Brain 129:1917–1928CrossRefPubMedGoogle Scholar
  11. 11.
    Hagmann P (2005) From diffusion MRI to brain connectomics. Université de LausanneGoogle Scholar
  12. 12.
    Hofer S, Karaus A, Frahm J (2010) Reconstruction and dissection of the entire human visual pathway using diffusion tensor MRI. Front Neuroanat 4:15PubMedPubMedCentralGoogle Scholar
  13. 13.
    Irfanoglu MO, Walker L, Sarlls J, Marenco S, Pierpaoli C (2012) Effects of image distortions originating from susceptibility variations and concomitant fields on diffusion MRI tractography results. Neuroimage 61:275–288CrossRefPubMedGoogle Scholar
  14. 14.
    James JS, Radhakrishnan A, Thomas B, Madhusoodanan M, Kesavadas C, Abraham M, Menon R, Rathore C, Vilanilam G (2015) Diffusion tensor imaging tractography of Meyer’s loop in planning resective surgery for drug-resistant temporal lobe epilepsy. Epilepsy Res 110:95–104CrossRefPubMedGoogle Scholar
  15. 15.
    Jezzard P, Balaban RS (1995) Correction for geometric distortion in echo planar images from B0 field variations. Magn Reson Med 34:65–73CrossRefPubMedGoogle Scholar
  16. 16.
    Jolesz FA (2011) Intraoperative imaging in neurosurgery: where will the future take us? Acta Neurochir Suppl 109:21–25CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Kamiya K, Amemiya S, Suzuki Y, Kunii N, Kawai K, Mori H, Kunimatsu A, Saito N, Aoki S, Ohtomo K (2016) Machine learning of DTI structural brain connectomes for lateralization of temporal lobe epilepsy. Magn Reson Med Sci 15:121–129CrossRefPubMedGoogle Scholar
  18. 18.
    Kammen A, Law M, Tjan BS, Toga AW, Shi Y (2016) Automated retinofugal visual pathway reconstruction with multi-shell HARDI and FOD-based analysis. Neuroimage 125:767–779CrossRefPubMedGoogle Scholar
  19. 19.
    Kang N, Zhang J, Carlson ES, Gembris D (2005) White matter fiber tractography via anisotropic diffusion simulation in the human brain. IEEE Trans Med Imaging 24:1127–1137CrossRefPubMedGoogle Scholar
  20. 20.
    Keller SS, Richardson MP, Schoene-Bake JC, O’Muircheartaigh J, Elkommos S, Kreilkamp B, Goh YY, Marson AG, Elger C, Weber B (2015) Thalamotemporal alteration and postoperative seizures in temporal lobe epilepsy. Ann Neurol 77:760–774CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Kiernan JA (2012) Anatomy of the temporal lobe. Epilepsy Res Treat 2012:176157PubMedPubMedCentralGoogle Scholar
  22. 22.
    Klingler J (1956) Atlas cerebri humani. Karger, BaselGoogle Scholar
  23. 23.
    Lee SH, Kim M, Park H (2015) Planning for selective amygdalohippocampectomy involving less neuronal fiber damage based on brain connectivity using tractography. Neural Regen Res 10:1107–1112CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Lilja Y, Ljungberg M, Starck G, Malmgren K, Rydenhag B, Nilsson DT (2014) Visualizing Meyer’s loop: a comparison of deterministic and probabilistic tractography. Epilepsy Res 108:481–490CrossRefPubMedGoogle Scholar
  25. 25.
    Lilja Y, Nilsson DT (2015) Strengths and limitations of tractography methods to identify the optic radiation for epilepsy surgery. Quant Imaging Med Surg 5:288–299PubMedPubMedCentralGoogle Scholar
  26. 26.
    Lutz MT, Clusmann H, Elger CE, Schramm J, Helmstaedter C (2004) Neuropsychological outcome after selective amygdalohippocampectomy with transsylvian versus transcortical approach: a randomized prospective clinical trial of surgery for temporal lobe epilepsy. Epilepsia 45:809–816CrossRefPubMedGoogle Scholar
  27. 27.
    McDonald CR, Hagler DJ Jr, Girard HM, Pung C, Ahmadi ME, Holland D, Patel RH, Barba D, Tecoma ES, Iragui VJ, Halgren E, Dale AM (2010) Changes in fiber tract integrity and visual fields after anterior temporal lobectomy. Neurology 75:1631–1638CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Meola A, Comert A, Yeh FC, Sivakanthan S, Fernandez-Miranda JC (2016) The nondecussating pathway of the dentatorubrothalamic tract in humans: human connectome-based tractographic study and microdissection validation. J Neurosurg 124:1406–1412CrossRefPubMedGoogle Scholar
  29. 29.
    Mori S, Crain BJ, Chacko VP, van Zijl PC (1999) Three-dimensional tracking of axonal projections in the brain by magnetic resonance imaging. Ann Neurol 45:265–269CrossRefPubMedGoogle Scholar
  30. 30.
    Mori S, van Zijl PC (2002) Fiber tracking: principles and strategies—a technical review. NMR Biomed 15:468–480CrossRefPubMedGoogle Scholar
  31. 31.
    Moseley ME, Cohen Y, Kucharczyk J, Mintorovitch J, Asgari HS, Wendland MF, Tsuruda J, Norman D (1990) Diffusion-weighted MR imaging of anisotropic water diffusion in cat central nervous system. Radiology 176:439–445CrossRefPubMedGoogle Scholar
  32. 32.
    Munsell BC, Wee CY, Keller SS, Weber B, Elger C, da Silva LA, Nesland T, Styner M, Shen D, Bonilha L (2015) Evaluation of machine learning algorithms for treatment outcome prediction in patients with epilepsy based on structural connectome data. Neuroimage 118:219–230CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Nakada T, Matsuzawa H (1995) Three-dimensional anisotropy contrast magnetic resonance imaging of the rat nervous system: MR axonography. Neurosci Res 22:389–398CrossRefPubMedGoogle Scholar
  34. 34.
    Nguyen D, Vargas MI, Khaw N, Seeck M, Delavelle J, Lovblad KO, Haller S (2011) Diffusion tensor imaging analysis with tract-based spatial statistics of the white matter abnormalities after epilepsy surgery. Epilepsy Res 94:189–197CrossRefPubMedGoogle Scholar
  35. 35.
    Nilsson D, Starck G, Ljungberg M, Ribbelin S, Jonsson L, Malmgren K, Rydenhag B (2007) Intersubject variability in the anterior extent of the optic radiation assessed by tractography. Epilepsy Res 77:11–16CrossRefPubMedGoogle Scholar
  36. 36.
    Peltier J, Verclytte S, Delmaire C, Pruvo JP, Godefroy O, Le Gars D (2010) Microsurgical anatomy of the temporal stem: clinical relevance and correlations with diffusion tensor imaging fiber tracking. J Neurosurg 112:1033–1038CrossRefPubMedGoogle Scholar
  37. 37.
    Piper RJ, Yoong MM, Kandasamy J, Chin RF (2014) Application of diffusion tensor imaging and tractography of the optic radiation in anterior temporal lobe resection for epilepsy: a systematic review. Clin Neurol Neurosurg 124:59–65CrossRefPubMedGoogle Scholar
  38. 38.
    Powell HW, Parker GJ, Alexander DC, Symms MR, Boulby PA, Wheeler-Kingshott CA, Barker GJ, Koepp MJ, Duncan JS (2005) MR tractography predicts visual field defects following temporal lobe resection. Neurology 65:596–599CrossRefPubMedGoogle Scholar
  39. 39.
    Pustina D, Avants B, Sperling M, Gorniak R, He X, Doucet G, Barnett P, Mintzer S, Sharan A, Tracy J (2015) Predicting the laterality of temporal lobe epilepsy from PET, MRI, and DTI: a multimodal study. Neuroimage Clin 9:20–31CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Robson MD, Gore JC, Constable RT (1997) Measurement of the point spread function in MRI using constant time imaging. Magn Reson Med 38:733–740CrossRefPubMedGoogle Scholar
  41. 41.
    Roper SN, Rhoton AL Jr (1993) Surgical anatomy of the temporal lobe. Neurosurg Clin N Am 4:223–231PubMedGoogle Scholar
  42. 42.
    Schmitt FC, Kaufmann J, Hoffmann MB, Tempelmann C, Kluge C, Rampp S, Voges J, Heinze HJ, Buentjen L, Grueschow M (2014) Case report: practicability of functionally based tractography of the optic radiation during presurgical epilepsy work up. Neurosci Lett 568:56–61CrossRefPubMedGoogle Scholar
  43. 43.
    Sherbondy AJ, Dougherty RF, Napel S, Wandell BA (2008) Identifying the human optic radiation using diffusion imaging and fiber tractography. J Vis 8(12):11CrossRefGoogle Scholar
  44. 44.
    Shi Y, Kammen A, Law M (2014) Technological advances in neuroimaging: neurosurgical applications for the future. World Neurosurg 82:32–34CrossRefPubMedGoogle Scholar
  45. 45.
    Sincoff EH, Tan Y, Abdulrauf SI (2004) White matter fiber dissection of the optic radiations of the temporal lobe and implications for surgical approaches to the temporal horn. J Neurosurg 101:739–746CrossRefPubMedGoogle Scholar
  46. 46.
    Sindou M, Guenot M (2003) Surgical anatomy of the temporal lobe for epilepsy surgery. Adv Tech Stand Neurosurg 28:315–343PubMedGoogle Scholar
  47. 47.
    Taoka T, Sakamoto M, Iwasaki S, Nakagawa H, Fukusumi A, Hirohashi S, Taoka K, Kichikawa K, Hoshida T, Sakaki T (2005) Diffusion tensor imaging in cases with visual field defect after anterior temporal lobectomy. AJNR Am J Neuroradiol 26:797–803PubMedGoogle Scholar
  48. 48.
    Taoka T, Sakamoto M, Nakagawa H, Nakase H, Iwasaki S, Takayama K, Taoka K, Hoshida T, Sakaki T, Kichikawa K (2008) Diffusion tensor tractography of the Meyer loop in cases of temporal lobe resection for temporal lobe epilepsy: correlation between postsurgical visual field defect and anterior limit of Meyer loop on tractography. AJNR Am J Neuroradiol 29:1329–1334CrossRefPubMedGoogle Scholar
  49. 49.
    Thudium MO, Campos AR, Urbach H, Clusmann H (2010) The basal temporal approach for mesial temporal surgery: sparing the Meyer loop with navigated diffusion tensor tractography. Neurosurgery 67:385–390PubMedGoogle Scholar
  50. 50.
    Ture U, Yasargil MG, Friedman AH, Al-Mefty O (2000) Fiber dissection technique: lateral aspect of the brain. Neurosurgery 47:417–426, discussion 426–417CrossRefPubMedGoogle Scholar
  51. 51.
    Wan X, Gullberg GT, Parker DL, Zeng GL (1997) Reduction of geometric and intensity distortions in echo-planar imaging using a multireference scan. Magn Reson Med 37:932–942CrossRefPubMedGoogle Scholar
  52. 52.
    Wang YX, Zhu XL, Deng M, Siu DY, Leung JC, Chan Q, Chan DT, Mak CH, Poon WS (2010) The use of diffusion tensor tractography to measure the distance between the anterior tip of the Meyer loop and the temporal pole in a cohort from southern China. J Neurosurg 113:1144–1151CrossRefPubMedGoogle Scholar
  53. 53.
    Wen HT, Rhoton AL Jr, de Oliveira E, Cardoso AC, Tedeschi H, Baccanelli M, Marino R Jr (1999) Microsurgical anatomy of the temporal lobe: part 1: mesial temporal lobe anatomy and its vascular relationships as applied to amygdalohippocampectomy. Neurosurgery 45:549–591, discussion 591–542CrossRefPubMedGoogle Scholar
  54. 54.
    Wieshmann UC, Symms MR, Clark CA, Lemieux L, Franconi F, Parker GJ, Barker GJ, Shorvon SD (1999) Wallerian degeneration in the optic radiation after temporal lobectomy demonstrated in vivo with diffusion tensor imaging. Epilepsia 40:1155–1158CrossRefPubMedGoogle Scholar
  55. 55.
    Winston GP, Daga P, Stretton J, Modat M, Symms MR, McEvoy AW, Ourselin S, Duncan JS (2012) Optic radiation tractography and vision in anterior temporal lobe resection. Ann Neurol 71:334–341CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Winston GP, Yogarajah M, Symms MR, McEvoy AW, Micallef C, Duncan JS (2011) Diffusion tensor imaging tractography to visualize the relationship of the optic radiation to epileptogenic lesions prior to neurosurgery. Epilepsia 52:1430–1438CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Xue R, van Zijl PC, Crain BJ, Solaiyappan M, Mori S (1999) In vivo three-dimensional reconstruction of rat brain axonal projections by diffusion tensor imaging. Magn Reson Med 42:1123–1127CrossRefPubMedGoogle Scholar
  58. 58.
    Yogarajah M, Focke NK, Bonelli S, Cercignani M, Acheson J, Parker GJ, Alexander DC, McEvoy AW, Symms MR, Koepp MJ, Duncan JS (2009) Defining Meyer’s loop-temporal lobe resections, visual field deficits and diffusion tensor tractography. Brain 132:1656–1668CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag Wien 2016

Authors and Affiliations

  1. 1.Department of Neurosurgery and Brain RepairUniversity of South Florida, Morsani College of MedicineTampaUSA
  2. 2.Brainlab IncWestchesterUSA
  3. 3.Department of RadiologyUniversity of South Florida, Morsani College of MedicineTampaUSA

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