A Novel Technique for Region and Linguistic Specific nTMS-based DTI Fiber Tracking of Language Pathways in Brain Tumor Patients

Navigated transcranial magnetic stimulation (nTMS) has recently been introduced as a non-invasive tool for functional mapping of cortical language areas prior to surgery. It correlates well with intraoperative neurophysiological monitoring (IONM) findings, allowing defining the best surgical strategy to preserve cortical language areas during surgery for language-eloquent tumors. Nevertheless, nTMS allows only for cortical mapping and postoperative language deficits are often caused by injury to subcortical language pathways. Nowadays, the only way to preoperatively visualize language subcortical white matter tracts consists in DTI fiber tracking (DTI-FT). However, standard DTI-FT is based on anatomical landmarks that vary interindividually and can be obscured by the presence of the tumor itself. It has been demonstrated that combining nTMS with DTI-FT allows for a more reliable visualization of the motor pathway in brain tumor patients. Nevertheless, no description about such a combination has been reported for the language network. The aim of the present study is to describe and assess the feasibility and reliability of using cortical seeding areas defined by error type-specific nTMS language mapping (nTMS-positive spots) to perform DTI-FT in patients affected by language-eloquent brain tumors. We describe a novel technique for a nTMS-based DTI-FT to visualize the complex cortico-subcortical connections of the language network. We analyzed quantitative findings, such as fractional anisotropy values and ratios, and the number of visualized connections of nTMS-positive spots with subcortical pathways, and we compared them with results obtained by using the standard DTI-FT technique. We also analyzed the functional concordance between connected cortical nTMS-positive spots and subcortical pathways, and the likelihood of connection for nTMS-positive vs. nTMS-negative cortical spots. We demonstrated, that the nTMS-based approach, especially what we call the “single-spot” strategy, is able to provide a reliable and more detailed reconstruction of the complex cortico-subcortical language network as compared to the standard DTI-FT. We believe this technique represents a beneficial new strategy for customized preoperative planning in patients affected by tumors in presumed language eloquent location, providing anatomo-functional information to plan language-preserving surgery.

[1]  Alberto Pisoni,et al.  Long-term proper name anomia after removal of the uncinate fasciculus , 2014, Brain Structure and Function.

[2]  C. Papagno,et al.  INTRAOPERATIVE SUBCORTICAL LANGUAGETRACT MAPPING GUIDES SURGICAL REMOVALOF GLIOMAS INVOLVING SPEECH AREAS , 2007, Neurosurgery.

[3]  Volkmar Glauche,et al.  Ventral and dorsal pathways for language , 2008, Proceedings of the National Academy of Sciences.

[4]  Andreas Prescher,et al.  Fiber anatomy of dorsal and ventral language streams , 2013, Brain and Language.

[5]  Vedran Deletis,et al.  Inducing transient language disruptions by mapping of Broca's area with modified patterned repetitive transcranial magnetic stimulation protocol. , 2014, Journal of neurosurgery.

[6]  J. Mäkelä,et al.  A novel approach for documenting naming errors induced by navigated transcranial magnetic stimulation , 2012, Journal of Neuroscience Methods.

[7]  Á. Pascual-Leone,et al.  Transcranial magnetic stimulation: studying the brain-behaviour relationship by induction of 'virtual lesions'. , 1999, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[8]  P. Basser,et al.  Microstructural and physiological features of tissues elucidated by quantitative-diffusion-tensor MRI. , 1996, Journal of magnetic resonance. Series B.

[9]  Pascale Tremblay,et al.  Beyond the arcuate fasciculus: consensus and controversy in the connectional anatomy of language. , 2012, Brain : a journal of neurology.

[10]  Hugues Duffau,et al.  Middle longitudinal fasciculus delineation within language pathways: a diffusion tensor imaging study in human. , 2013, European journal of radiology.

[11]  D. Frey,et al.  A new approach for corticospinal tract reconstruction based on navigated transcranial stimulation and standardized fractional anisotropy values , 2012, NeuroImage.

[12]  Paul M. Thompson,et al.  How does angular resolution affect diffusion imaging measures? , 2010, NeuroImage.

[13]  Jürgen Finsterbusch,et al.  Microscopic diffusion anisotropy in the human brain: Reproducibility, normal values, and comparison with the fractional anisotropy , 2015, NeuroImage.

[14]  C. Zimmer,et al.  Cortical regions involved in semantic processing investigated by repetitive navigated transcranial magnetic stimulation and object naming , 2015, Neuropsychologia.

[15]  N. Papadakis,et al.  Minimal gradient encoding for robust estimation of diffusion anisotropy. , 2000, Magnetic resonance imaging.

[16]  Dietmar Frey,et al.  Navigated transcranial magnetic stimulation improves the treatment outcome in patients with brain tumors in motor eloquent locations. , 2014, Neuro-oncology.

[17]  Giuseppe Scotti,et al.  Motor and language DTI Fiber Tracking combined with intraoperative subcortical mapping for surgical removal of gliomas , 2008, NeuroImage.

[18]  K. Poeck,et al.  [The Aachen Aphasia Test Rationale and construct validity (author's transl)]. , 1980, Der Nervenarzt.

[19]  B. Meyer,et al.  nTMS-based DTI fiber tracking for language pathways correlates with language function and aphasia – A case report , 2015, Clinical Neurology and Neurosurgery.

[20]  J. Mäkelä,et al.  A comparison of language mapping by preoperative navigated transcranial magnetic stimulation and direct cortical stimulation during awake surgery. , 2013, Neurosurgery.

[21]  P. Yen,et al.  White Matter tract involvement in brain tumors: a diffusion tensor imaging analysis. , 2009, Surgical neurology.

[22]  Derek K. Jones,et al.  Perisylvian language networks of the human brain , 2005, Annals of neurology.

[23]  S. Zhuang,et al.  Effect of Increasing Diffusion Gradient Direction Number on Diffusion Tensor Imaging Fiber Tracking in the Human Brain , 2015, Korean journal of radiology.

[24]  Matthew F Glasser,et al.  DTI tractography of the human brain's language pathways. , 2008, Cerebral cortex.

[25]  Srikantan S. Nagarajan,et al.  Optimal timing of pulse onset for language mapping with navigated repetitive transcranial magnetic stimulation , 2014, NeuroImage.

[26]  H. Duffau,et al.  Intraoperative subcortical stimulation mapping of language pathways in a consecutive series of 115 patients with Grade II glioma in the left dominant hemisphere. , 2008, Journal of neurosurgery.

[27]  Catherine Lebel,et al.  Six is enough? Comparison of diffusion parameters measured using six or more diffusion‐encoding gradient directions with deterministic tractography , 2012, Magnetic resonance in medicine.

[28]  T. Picht,et al.  Language mapping in healthy volunteers and brain tumor patients with a novel navigated TMS system: Evidence of tumor-induced plasticity , 2014, Clinical Neurophysiology.

[29]  G. Johnson,et al.  Peritumoral diffusion tensor imaging of high-grade gliomas and metastatic brain tumors. , 2003, AJNR. American journal of neuroradiology.

[30]  D. Pandya,et al.  Segmentation of subcomponents within the superior longitudinal fascicle in humans: a quantitative, in vivo, DT-MRI study. , 2005, Cerebral cortex.

[31]  Mitchel S Berger,et al.  Functional outcome after language mapping for glioma resection. , 2008, The New England journal of medicine.

[32]  Christian Grefkes,et al.  Improved nTMS- and DTI-derived CST tractography through anatomical ROI seeding on anterior pontine level compared to internal capsule , 2015, NeuroImage: Clinical.

[33]  Francesco Tomasello,et al.  Navigated Transcranial Magnetic Stimulation for “Somatotopic” Tractography of the Corticospinal Tract , 2014, Neurosurgery.

[34]  I. Koerte,et al.  Diffusion Tensor Imaging , 2014 .

[35]  E. Chang,et al.  Contemporary model of language organization: an overview for neurosurgeons. , 2015, Journal of neurosurgery.

[36]  Derek K. Jones,et al.  Virtual in Vivo Interactive Dissection of White Matter Fasciculi in the Human Brain , 2002, NeuroImage.

[37]  James F. Brinkley,et al.  Analysis of naming errors during cortical stimulation mapping: Implications for models of language representation , 2010, Brain and Language.

[38]  Elsa D. Angelini,et al.  Evidence for potentials and limitations of brain plasticity using an atlas of functional resectability of WHO grade II gliomas: Towards a “minimal common brain” , 2011, NeuroImage.

[39]  J. Rothwell,et al.  Transcranial magnetic stimulation in cognitive neuroscience – virtual lesion, chronometry, and functional connectivity , 2000, Current Opinion in Neurobiology.

[40]  Christine Delmaire,et al.  Comparison of diffusion tensor imaging tractography of language tracts and intraoperative subcortical stimulations. , 2010, Journal of neurosurgery.

[41]  Costanza Papagno,et al.  Naming and the Role of the Uncinate Fasciculus in Language Function , 2011, Current neurology and neuroscience reports.

[42]  G. Ojemann,et al.  Dissociation of action and object naming: Evidence from cortical stimulation mapping , 2005, Human brain mapping.

[43]  Nader Pouratian,et al.  The reliability of neuroanatomy as a predictor of eloquence: a review. , 2010, Neurosurgical focus.

[44]  S. Maesawa,et al.  Association of dorsal inferior frontooccipital fasciculus fibers in the deep parietal lobe with both reading and writing processes: a brain mapping study. , 2014, Journal of neurosurgery.

[45]  H. Duffau,et al.  Awake mapping for low-grade gliomas involving the left sagittal stratum: anatomofunctional and surgical considerations. , 2014, Journal of neurosurgery.

[46]  P. Vachata,et al.  Distant white-matter diffusion changes caused by tumor growth. , 2013, Journal of neuroradiology. Journal de neuroradiologie.

[47]  P. Basser,et al.  MR diffusion tensor spectroscopy and imaging. , 1994, Biophysical journal.

[48]  D. Poeppel,et al.  Dorsal and ventral streams: a framework for understanding aspects of the functional anatomy of language , 2004, Cognition.

[49]  M. Catani,et al.  A diffusion tensor imaging tractography atlas for virtual in vivo dissections , 2008, Cortex.

[50]  Srikantan S. Nagarajan,et al.  Language mapping with navigated repetitive TMS: Proof of technique and validation , 2013, NeuroImage.

[51]  P. Basser,et al.  Estimation of the effective self-diffusion tensor from the NMR spin echo. , 1994, Journal of magnetic resonance. Series B.

[52]  Costanza Papagno,et al.  What is the role of the uncinate fasciculus? Surgical removal and proper name retrieval. , 2011, Brain : a journal of neurology.

[53]  Hugues Duffau,et al.  Cortico-subcortical organization of language networks in the right hemisphere: An electrostimulation study in left-handers , 2008, Neuropsychologia.

[54]  Carmen Terranova,et al.  Preoperative functional mapping for rolandic brain tumor surgery , 2014, Neuroscience Letters.