Function-specific Tractography of Language Pathways Based on nTMS Mapping in Patients with Supratentorial Lesions
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In patients with supratentorial lesions diffusion tensor imaging fiber tracking (DTI-FT) is increasingly used to visualize subcortical fiber courses. Navigated transcranial magnetic stimulation (nTMS) was applied in this study to reveal specific cortical functions by investigating the particular language errors elicited by stimulation. To make DTI-FT more function-specific, the identified language-positive nTMS spots were used as regions of interest (ROIs).
In this study 40 patients (mean age 53.8 ± 16.0 years) harboring language-eloquent left hemispheric lesions underwent preoperative nTMS language mapping. All induced error categories were separately defined as a ROI and used for function-specific nTMS-based DTI-FT. The fractions of patients showing various subcortical language-related pathways and the fibers-per-tract ratio (number of visualized fibers divided by the number of visualized tracts) were evaluated and compared for tractography with the single error types against less specific tractography including all identified cortical language sites (all errors except hesitations).
The nTMS-based DTI-FT using all errors except hesitations led to high fractions of visualized tracts (81.1% of patients), with a fibers-per-tract ratio of 538.4 ± 340.5. When only using performance errors, a predominant visualization of the superior longitudinal fascicle (SLF) occurred, which is known to be involved in articulatory processes. Fibers-per-tract ratios were comparatively stable for all single error categories when compared to all errors except hesitations (p > 0.05).
This is one of the first studies aiming on function-specific tractography. The results demonstrated that when using different error categories as ROIs, more detailed nTMS-based DTI-FT and, therefore, potentially superior intraoperative guidance becomes possible.
KeywordsDiffusion tensor imaging Fiber tracking Glioma Navigated transcranial magnetic stimulation Preoperative imaging
Aachen Aphasia Test
British Medical Research Council
Direct electrical stimulation
Diffusion tensor imaging
Diffusion tensor imaging fiber tracking
Fractional anisotropy threshold
Fluid attenuated inversion recovery
Functional magnetic resonance imaging
Inferior longitudinal fascicle
Karnofsky performance status
Magnetic resonance imaging
Navigated transcranial magnetic stimulation
Resting motor threshold
Region of interest
Superior longitudinal fascicle
World Health Organization
The study was completely financed by institutional grants from the Department of Neurosurgery and the Department of Neuroradiology.
Compliance with ethical guidelines
Conflict of interest
N. Sollmann received fees from Nexstim Plc (Helsinki, Finland). S.M. Krieg is consultant for Nexstim Plc (Helsinki, Finland) and received fees from Medtronic (Meerbusch, Germany) and Carl Zeiss Meditec (Oberkochen, Germany). S.M. Krieg and B. Meyer received research grants and are consultants for Brainlab AG (Munich, Germany). B. Meyer received fees, consulting fees, and research grants from Medtronic (Meerbusch, Germany), Icotec ag (Altstätten, Switzerland), and Relievant Medsystems (Sunnyvale, CA, USA), fees and research grants from Ulrich Medical (Ulm, Germany), fees and consulting fees from Spineart Deutschland GmbH (Frankfurt, Germany) and DePuy Synthes (West Chester, PA, USA), and royalties from Spineart Deutschland GmbH (Frankfurt, Germany). N. Sollmann, H. Zhang, S. Schramm, S. Ille, C. Negwer, K. Kreiser, B. Meyer and S.M. Krieg declare that they have no conflict of interest regarding the materials used or the results presented in this study.
All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. Informed consent was obtained from all individual participants included in the study.
- 13.Raffa G, Conti A, Scibilia A, Sindorio C, Quattropani MC, Visocchi M, Germanò A, Tomasello F. Functional reconstruction of motor and language pathways based on navigated transcranial magnetic stimulation and DTI fiber tracking for the preoperative planning of low grade glioma surgery: a new tool for preservation and restoration of eloquent networks. Acta Neurochir Suppl. 2017;124:251–61.CrossRefPubMedGoogle Scholar
- 14.Negwer C, Beurskens E, Sollmann N, Maurer S, Ille S, Giglhuber K, Kirschke JS, Ringel F, Meyer B, Krieg SM. Loss of subcortical language pathways correlates with surgery-related aphasia in patients with brain tumor: an investigation via repetitive navigated transcranial magnetic stimulation-based diffusion tensor imaging fiber tracking. World Neurosurg. 2018;111:e806–18.CrossRefPubMedGoogle Scholar
- 16.Krieg SM, Lioumis P, Mäkelä JP, Wilenius J, Karhu J, Hannula H, Savolainen P, Lucas CW, Seidel K, Laakso A, Islam M, Vaalto S, Lehtinen H, Vitikainen AM, Tarapore PE, Picht T. Protocol for motor and language mapping by navigated TMS in patients and healthy volunteers; workshop report. Acta Neurochir (Wien). 2017;159:1187–95.CrossRefGoogle Scholar
- 17.Picht T, Krieg SM, Sollmann N, Rösler J, Niraula B, Neuvonen T, Savolainen P, Lioumis P, Mäkelä JP, Deletis V, Meyer B, Vajkoczy P, Ringel F. A comparison of language mapping by preoperative navigated transcranial magnetic stimulation and direct cortical stimulation during awake surgery. Neurosurgery. 2013;72:808–19.CrossRefPubMedGoogle Scholar
- 19.Sollmann N, Ille S, Hauck T, Maurer S, Negwer C, Zimmer C, Ringel F, Meyer B, Krieg SM. The impact of preoperative language mapping by repetitive navigated transcranial magnetic stimulation on the clinical course of brain tumor patients. BMC Cancer. 2015;15:261.CrossRefPubMedPubMedCentralGoogle Scholar
- 21.Sollmann N, Kelm A, Ille S, Schröder A, Zimmer C, Ringel F, Meyer B, Krieg SM. Setup presentation and clinical outcome analysis of treating highly language-eloquent gliomas via preoperative navigated transcranial magnetic stimulation and tractography. Neurosurg Focus. 2018;44:E2.CrossRefPubMedGoogle Scholar
- 22.Krieg SM, Sollmann N, Obermueller T, Sabih J, Bulubas L, Negwer C, Moser T, Droese D, Boeckh-Behrens T, Ringel F, Meyer B. Changing the clinical course of glioma patients by preoperative motor mapping with navigated transcranial magnetic brain stimulation. BMC Cancer. 2015;15:231.CrossRefPubMedPubMedCentralGoogle Scholar
- 24.Sollmann N, Wildschuetz N, Kelm A, Conway N, Moser T, Bulubas L, Kirschke JS, Meyer B, Krieg SM. Associations between clinical outcome and navigated transcranial magnetic stimulation characteristics in patients with motor-eloquent brain lesions: a combined navigated transcranial magnetic stimulation-diffusion tensor imaging fiber tracking approach. J Neurosurg. 2018;128:800–10.CrossRefPubMedGoogle Scholar
- 39.Sollmann N, Tanigawa N, Tussis L, Hauck T, Ille S, Maurer S, Negwer C, Zimmer C, Ringel F, Meyer B, Krieg SM. Cortical regions involved in semantic processing investigated by repetitive navigated transcranial magnetic stimulation and object naming. Neuropsychologia. 2015;70:185–95.CrossRefPubMedGoogle Scholar
- 48.Chang SM, Parney IF, McDermott M, Barker FG 2nd, Schmidt MH, Huang W, Laws ER Jr, Lillehei KO, Bernstein M, Brem H, Sloan AE, Berger M; Glioma Outcomes Investigators. Perioperative complications and neurological outcomes of first and second craniotomies among patients enrolled in the Glioma Outcome Project. J Neurosurg. 2003;98:1175–81.CrossRefPubMedGoogle Scholar
- 57.Kuhnt D, Bauer MH, Egger J, Richter M, Kapur T, Sommer J, Merhof D, Nimsky C. Fiber tractography based on diffusion tensor imaging compared with high-angular-resolution diffusion imaging with compressed sensing: initial experience. Neurosurgery. 2013;72 Suppl 1:165-75.CrossRefPubMedPubMedCentralGoogle Scholar