Top

Published in:

Open Access 01-06-2019 | Brain Tumor | Technical Note - Neurosurgical Anatomy

Manual for clinical language tractography

Authors: Lucius Fekonja, Ziqian Wang, Ina Bährend, Tizian Rosenstock, Judith Rösler, Lara Wallmeroth, Peter Vajkoczy, Thomas Picht

Published in: Acta Neurochirurgica | Issue 6/2019

Abstract

Background

We introduce a user-friendly, standardized protocol for tractography of the major language fiber bundles.

Method

The introduced method uses dMRI images for tractography whereas the ROI definition is based on structural T1 MPRAGE MRI templates, without normalization to MNI space. ROIs for five language-relevant fiber bundles were visualized on an axial, coronal, or sagittal view of T1 MPRAGE images. The ROIs were defined based upon the tracts’ obligatory pathways, derived from literature and own experiences in peritumoral tractography.

Results

The resulting guideline was evaluated for each fiber bundle in ten healthy subjects and ten patients by one expert and three raters.

Overall, 300 ROIs were evaluated and compared. The targeted language fiber bundles could be tracked in 88% of the ROI pairs, based on the raters’ result blinded ROI placements. The evaluation indicated that the precision of the ROIs did not relate to the varying experience of the raters.

Conclusions

Our guideline introduces a standardized language tractography method for routine preoperative workup and for research contexts. The ROI placement guideline based on easy-to-identify anatomical landmarks proved to be user-friendly and accurate, also in inexperienced test persons.

Bizzi A, Nava S, Ferre F et al (2012) Aphasia induced by gliomas growing in the ventrolateral frontal region: assessment with diffusion MR tractography, functional MR imaging and neuropsychology. Cortex 48:255–272. https://doi.org/10.1016/j.cortex.2011.11.015 CrossRefPubMed

Catani M, Dell'acqua F, Bizzi A et al (2012) Beyond cortical localization in clinico-anatomical correlation. Cortex 48:1262–1287. https://doi.org/10.1016/j.cortex.2012.07.001 CrossRefPubMed

Catani M, Dell'acqua F, Vergani F et al (2012) Short frontal lobe connections of the human brain. Cortex 48:273–291. https://doi.org/10.1016/j.cortex.2011.12.001 CrossRefPubMed

Catani M, Howard RJ, Pajevic S et al (2002) Virtual in vivo interactive dissection of white matter fasciculi in the human brain. Neuroimage 17:77–94CrossRefPubMed

Catani M, Jones DK, Donato R et al (2003) Occipito-temporal connections in the human brain. Brain 126:2093–2107. https://doi.org/10.1093/brain/awg203 CrossRefPubMed

Catani M, Mesulam MM, Jakobsen E et al (2013) A novel frontal pathway underlies verbal fluency in primary progressive aphasia. Brain 136:2619–2628. https://doi.org/10.1093/brain/awt163 CrossRefPubMedPubMedCentral

Catani M, Thiebaut de Schotten M (2008) A diffusion tensor imaging tractography atlas for virtual in vivo dissections. Cortex 44:1105–1132. https://doi.org/10.1016/j.cortex.2008.05.004 CrossRefPubMed

Caverzasi E, Papinutto N, Amirbekian B et al (2014) Q-ball of inferior fronto-occipital fasciculus and beyond. PLoS One 9:e100274. https://doi.org/10.1371/journal.pone.0100274 CrossRefPubMedPubMedCentral

Cochereau J, Deverdun J, Herbet G et al (2016) Comparison between resting state fMRI networks and responsive cortical stimulations in glioma patients. Hum Brain Mapp 37:3721–3732. https://doi.org/10.1002/hbm.23270 CrossRefPubMedPubMedCentral

10.

Duffau H (2008) The anatomo-functional connectivity of language revisited. New insights provided by electrostimulation and tractography. Neuropsychologia 46:927–934. https://doi.org/10.1016/j.neuropsychologia.2007.10.025 CrossRefPubMed

11.

Duffau H (2015) Stimulation mapping of white matter tracts to study brain functional connectivity. Nat Rev Neurol 11:255–265. https://doi.org/10.1038/nrneurol.2015.51 CrossRefPubMed

12.

Duffau H, Gatignol P, Mandonnet E et al (2005) New insights into the anatomo-functional connectivity of the semantic system: a study using cortico-subcortical electrostimulations. Brain 128:797–810. https://doi.org/10.1093/brain/awh423 CrossRefPubMed

13.

Duffau H, Lopes M, Arthuis F et al (2005) Contribution of intraoperative electrical stimulations in surgery of low grade gliomas: a comparative study between two series without (1985-96) and with (1996-2003) functional mapping in the same institution. J Neurol Neurosurg Psychiatry 76:845–851. https://doi.org/10.1136/jnnp.2004.048520 CrossRefPubMedPubMedCentral

14.

Field AS, Alexander AL, Wu YC et al (2004) Diffusion tensor eigenvector directional color imaging patterns in the evaluation of cerebral white matter tracts altered by tumor. J Magn Reson Imaging 20:555–562. https://doi.org/10.1002/jmri.20169 CrossRefPubMed

15.

Friederici AD (2011) The brain basis of language processing: from structure to function. Physiol Rev 91:1357–1392. https://doi.org/10.1152/physrev.00006.2011 CrossRefPubMed

16.

Greve DN, Fischl B (2009) Accurate and robust brain image alignment using boundary-based registration. Neuroimage 48:63–72. https://doi.org/10.1016/j.neuroimage.2009.06.060 CrossRefPubMed

17.

Grossman M, McMillan C, Moore P et al (2004) What’s in a name: voxel-based morphometric analyses of MRI and naming difficulty in Alzheimer’s disease, frontotemporal dementia and corticobasal degeneration. Brain 127:628–649. https://doi.org/10.1093/brain/awh075 CrossRefPubMed

18.

Hau J, Sarubbo S, Perchey G et al (2016) Cortical terminations of the inferior fronto-occipital and uncinate fasciculi: anatomical stem-based virtual dissection. Front Neuroanat 10:58. https://doi.org/10.3389/fnana.2016.00058 CrossRefPubMedPubMedCentral

19.

Jellison BJ, Field AS, Medow J et al (2004) Diffusion tensor imaging of cerebral white matter: a pictorial review of physics, fiber tract anatomy, and tumor imaging patterns. AJNR Am J Neuroradiol 25:356–369PubMedPubMedCentral

20.

Jenkinson M, Bannister P, Brady M et al (2002) Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage 17:825–841CrossRefPubMed

21.

Jenkinson M, Smith S (2001) A global optimisation method for robust affine registration of brain images. Med Image Anal 5:143–156CrossRefPubMed

22.

Jurgens U, von Cramon D (1982) On the role of the anterior cingulate cortex in phonation: a case report. Brain Lang 15:234–248CrossRefPubMed

23.

Landis JR, Koch GG (1977) The measurement of observer agreement for categorical data. Biometrics 33:159–174CrossRefPubMed

24.

Lanfermann H, Schindler C, Jordan J et al (2015) Pharmacological MRI (phMRI) of the human central nervous system. Clin Neuroradiol 25(Suppl 2):259–266. https://doi.org/10.1007/s00062-015-0457-0 CrossRefPubMed

25.

Leclercq D, Duffau H, Delmaire C et al (2010) Comparison of diffusion tensor imaging tractography of language tracts and intraoperative subcortical stimulations. J Neurosurg 112:503–511. https://doi.org/10.3171/2009.8.JNS09558 CrossRefPubMed

26.

Lu LH, Crosson B, Nadeau SE et al (2002) Category-specific naming deficits for objects and actions: semantic attribute and grammatical role hypotheses. Neuropsychologia 40:1608–1621CrossRefPubMed

27.

Makris N, Kennedy DN, McInerney S et al (2005) Segmentation of subcomponents within the superior longitudinal fascicle in humans: a quantitative, in vivo, DT-MRI study. Cereb Cortex 15:854–869. https://doi.org/10.1093/cercor/bhh186 CrossRefPubMed

28.

Mandonnet E, Nouet A, Gatignol P et al (2007) Does the left inferior longitudinal fasciculus play a role in language? A brain stimulation study. Brain 130:623–629. https://doi.org/10.1093/brain/awl361 CrossRefPubMed

29.

Martino J, Brogna C, Robles SG et al (2010) Anatomic dissection of the inferior fronto-occipital fasciculus revisited in the lights of brain stimulation data. Cortex 46:691–699. https://doi.org/10.1016/j.cortex.2009.07.015 CrossRefPubMed

30.

Mori S, Crain BJ, Chacko VP et al (1999) Three-dimensional tracking of axonal projections in the brain by magnetic resonance imaging. Ann Neurol 45:265–269CrossRefPubMed

31.

Mummery CJ, Patterson K, Wise RJ et al (1999) Disrupted temporal lobe connections in semantic dementia. Brain 122 ( Pt 1:61–73CrossRefPubMed

32.

Negwer C, Ille S, Hauck T et al (2017) Visualization of subcortical language pathways by diffusion tensor imaging fiber tracking based on rTMS language mapping. Brain Imaging Behav 11:899–914. https://doi.org/10.1007/s11682-016-9563-0 CrossRefPubMed

33.

Negwer C, Sollmann N, Ille S et al (2017) Language pathway tracking: comparing nTMS-based DTI fiber tracking with a cubic ROIs-based protocol. J Neurosurg 126:1006–1014. https://doi.org/10.3171/2016.2.JNS152382 CrossRefPubMed

34.

Picht T (2015) Navigated transcranial magnetic stimulation for preoperative mapping of the eloquent cortex. Nervenarzt 86:1508–1515. https://doi.org/10.1007/s00115-015-4316-7 CrossRefPubMed

35.

Qin YY, Li MW, Zhang S et al (2013) In vivo quantitative whole-brain diffusion tensor imaging analysis of APP/PS1 transgenic mice using voxel-based and atlas-based methods. Neuroradiology 55:1027–1038. https://doi.org/10.1007/s00234-013-1195-0 CrossRefPubMed

36.

Raffa G, Bahrend I, Schneider H et al (2016) A novel technique for region and linguistic specific nTMS-based DTI fiber tracking of language pathways in brain tumor patients. Front Neurosci 10:552. https://doi.org/10.3389/fnins.2016.00552 CrossRefPubMedPubMedCentral

37.

Rubens AB (1975) Aphasia with infarction in the territory of the anterior cerebral artery. Cortex 11:239–250CrossRefPubMed

38.

Sarubbo S, De Benedictis A, Merler S et al (2015) Towards a functional atlas of human white matter. Hum Brain Mapp 36:3117–3136. https://doi.org/10.1002/hbm.22832 CrossRefPubMedPubMedCentral

39.

Smith SM, Jenkinson M, Woolrich MW et al (2004) Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 23(Suppl 1):S208–S219. https://doi.org/10.1016/j.neuroimage.2004.07.051 CrossRefPubMed

40.

Tournier J-D, Calamante F, Connelly A (2010) Improved probabilistic streamlines tractography by 2nd order integration over fibre orientation distributions. Proceedings of the International Society for Magnetic Resonance in Medicine, 1670. In: International Society for Magnetic Resonance in Medicine, 2010

41.

Tustison NJ, Avants BB, Cook PA et al (2010) N4ITK: improved N3 bias correction. IEEE Trans Med Imaging 29:1310–1320. https://doi.org/10.1109/TMI.2010.2046908 CrossRefPubMedPubMedCentral

42.

Van Essen DC, Ugurbil K, Auerbach E et al (2012) The Human Connectome Project: a data acquisition perspective. Neuroimage 62:2222–2231. https://doi.org/10.1016/j.neuroimage.2012.02.018 CrossRefPubMed

43.

Vassal F, Schneider F, Boutet C et al (2016) Combined DTI tractography and functional MRI study of the language connectome in healthy volunteers: extensive mapping of white matter fascicles and cortical activations. PLoS One 11:e0152614. https://doi.org/10.1371/journal.pone.0152614 CrossRefPubMedPubMedCentral

44.

Veraart J, Novikov DS, Christiaens D et al (2016) Denoising of diffusion MRI using random matrix theory. Neuroimage 142:394–406. https://doi.org/10.1016/j.neuroimage.2016.08.016 CrossRefPubMed

45.

Weinstein D, Kindlmann G, Tensorlines LE (1999) Advection-diffusion based propagation through diffusion tensor fields. In: Proceedings of the conference on Visualization’99: celebrating ten years. IEEE Computer Society Press, Washington, D.C., pp 249–253

46.

Witwer BP, Moftakhar R, Hasan KM et al (2002) Diffusion-tensor imaging of white matter tracts in patients with cerebral neoplasm. J Neurosurg 97:568–575. https://doi.org/10.3171/jns.2002.97.3.0568 CrossRefPubMed

Title: Manual for clinical language tractography
Authors: Lucius Fekonja
Ziqian Wang
Ina Bährend
Tizian Rosenstock
Judith Rösler
Lara Wallmeroth
Peter Vajkoczy
Thomas Picht
Publication date: 01-06-2019
Publisher: Springer Vienna
Keyword: Brain Tumor
Published in: Acta Neurochirurgica / Issue 6/2019
Print ISSN: 0001-6268
Electronic ISSN: 0942-0940
DOI: https://doi.org/10.1007/s00701-019-03899-0

At a glance: The STEP trials

Springer Medicine

Manual for clinical language tractography

Abstract

Background

Method

Results

Conclusions

At a glance: The STEP trials

Springer Medicine

Abstract

Background

Method

Results

Conclusions

Please log in to get access to this content

Other articles of this Issue 6/2019

Ensuring safe surgery is more than just tackling antimicrobial resistance: making the case for a skin preparation trial

5-ALA fluorescence–guided surgery in pediatric brain tumors—a systematic review

Response to the Letter to the Editor “Lipomatosis of nerve and overgrowth syndrome: an intriguing and still unclear correlation”

Univariate comparison of PRx, PAx, and RAC—much ado about what?

Correction to: Univariate comparison of performance of different cerebrovascular reactivity indices for outcome association in adult TBI: a CENTER-TBI study

Protective STA-MCA bypass to prevent brain ischemia during high-flow bypass surgery: case series of 10 patients