The value of preoperative functional cortical mapping using navigated TMS

The surgical removal of brain tumours in so-called eloquent regions is frequently associated with a high risk of causing disabling postoperative deficits. Among the preoperative techniques proposed to help neurosurgical planning and procedure, navigated transcranial magnetic stimulation (nTMS) is increasingly performed. A high level of evidence is now available in the literature regarding the anatomical and functional accuracy of this mapping technique. This article presents the principles and facts demonstrating the value of using nTMS in clinical practice to preserve motor or language functions from deleterious lesions secondary to brain tumour resection or epilepsy surgery.

[1]  Bernhard Meyer,et al.  Presurgical navigated transcranial magnetic brain stimulation for recurrent gliomas in motor eloquent areas , 2013, Clinical Neurophysiology.

[2]  H. Tokimura,et al.  Identification of the cerebral motor cortex by focal magnetic stimulation: clinical application to neurosurgical patients. , 1994, Stereotactic and functional neurosurgery.

[3]  S. S. Ayache,et al.  Comparison of “standard” and “navigated” procedures of TMS coil positioning over motor, premotor and prefrontal targets in patients with chronic pain and depression , 2010, Neurophysiologie Clinique/Clinical Neurophysiology.

[4]  Jan S. Bauer,et al.  Correlating subcortical interhemispheric connectivity and cortical hemispheric dominance in brain tumor patients: A repetitive navigated transcranial magnetic stimulation study , 2016, Clinical Neurology and Neurosurgery.

[5]  M. Berger,et al.  Impact of intraoperative stimulation brain mapping on glioma surgery outcome: a meta-analysis. , 2012, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[6]  Francesco Tomasello,et al.  Integration of functional neuroimaging in CyberKnife radiosurgery: feasibility and dosimetric results. , 2013, Neurosurgical focus.

[7]  Peter Vajkoczy,et al.  NAVIGATED TRANSCRANIAL MAGNETIC STIMULATION FOR PREOPERATIVE FUNCTIONAL DIAGNOSTICS IN BRAIN TUMOR SURGERY , 2009, Neurosurgery.

[8]  Bernhard Meyer,et al.  Impairment of preoperative language mapping by lesion location: a functional magnetic resonance imaging, navigated transcranial magnetic stimulation, and direct cortical stimulation study. , 2015, Journal of neurosurgery.

[9]  S. Rossi,et al.  Non-invasive electrical and magnetic stimulation of the brain, spinal cord, roots and peripheral nerves: Basic principles and procedures for routine clinical and research application. An updated report from an I.F.C.N. Committee , 2015, Clinical Neurophysiology.

[10]  L. Friberg,et al.  Speech localization using repetitive transcranial magnetic stimulation , 1994, Neurology.

[11]  P. Vajkoczy,et al.  Presurgical navigated TMS motor cortex mapping improves outcome in glioblastoma surgery: a controlled observational study , 2016, Journal of Neuro-Oncology.

[12]  Eero Salli,et al.  Combined use of non-invasive techniques for improved functional localization for a selected group of epilepsy surgery candidates , 2009, NeuroImage.

[13]  Shalini Narayana,et al.  Clinical Applications of Transcranial Magnetic Stimulation in Pediatric Neurology , 2015, Journal of child neurology.

[14]  P. Fox,et al.  Column‐based model of electric field excitation of cerebral cortex , 2004, Human brain mapping.

[15]  Dietmar Frey,et al.  Functional brain mapping of patients with arteriovenous malformations using navigated transcranial magnetic stimulation: first experience in ten patients , 2014, Acta Neurochirurgica.

[16]  S. Vulliemoz,et al.  The Wada test in Austrian, Dutch, German, and Swiss epilepsy centers from 2000 to 2005: a review of 1421 procedures , 2008, Epilepsy & Behavior.

[17]  Juha E. Jääskeläinen,et al.  Non-invasive preoperative localization of primary motor cortex in epilepsy surgery by navigated transcranial magnetic stimulation , 2010, Epilepsy Research.

[18]  A. Barker,et al.  NON-INVASIVE MAGNETIC STIMULATION OF HUMAN MOTOR CORTEX , 1985, The Lancet.

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

[20]  Dietmar Frey,et al.  Preoperative Functional Mapping for Rolandic Brain Tumor Surgery: Comparison of Navigated Transcranial Magnetic Stimulation to Direct Cortical Stimulation , 2011, Neurosurgery.

[21]  Srikantan S. Nagarajan,et al.  Safety and tolerability of navigated TMS for preoperative mapping in neurosurgical patients , 2016, Clinical Neurophysiology.

[22]  Stefan Klöppel,et al.  Alternatives to the Wada test: a critical view of functional magnetic resonance imaging in preoperative use , 2005, Current opinion in neurology.

[23]  K. Meador,et al.  Optimum stimulus parameters for lateralized suppression of speech with magnetic brain stimulation , 1996, Neurology.

[24]  Phiroz E. Tarapore,et al.  Preoperative multimodal motor mapping: a comparison of magnetoencephalography imaging, navigated transcranial magnetic stimulation, and direct cortical stimulation. , 2012, Journal of neurosurgery.

[25]  B. Meyer,et al.  Functional Language Shift to the Right Hemisphere in Patients with Language-Eloquent Brain Tumors , 2013, PloS one.

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

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

[28]  I Diane Cooper,et al.  What is a "mapping study?". , 2016, Journal of the Medical Library Association : JMLA.

[29]  K. Zilles,et al.  Functional neuroanatomy of the primate isocortical motor system , 2000, Anatomy and Embryology.

[30]  B R Rosen,et al.  Stereotactic transcranial magnetic stimulation: correlation with direct electrical cortical stimulation. , 1997, Neurosurgery.

[31]  S. Baxendale The Wada test , 2009, Current opinion in neurology.

[32]  Mauro Silvestrini,et al.  Ipsilateral activation of the unaffected motor cortex in patients with hemiparetic stroke , 2000, Clinical Neurophysiology.

[33]  S. Brandt,et al.  A case of pathological excitability located with navigated-TMS: presurgical evaluation of focal neocortical epilepsy. , 2010, Restorative neurology and neuroscience.

[34]  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.

[35]  H Duffau,et al.  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 , 2005, Journal of Neurology, Neurosurgery & Psychiatry.

[36]  Peter Vajkoczy,et al.  Assessment of the influence of navigated transcranial magnetic stimulation on surgical planning for tumors in or near the motor cortex. , 2012, Neurosurgery.

[37]  Elke Hattingen,et al.  Navigated Transcranial Magnetic Stimulation and Functional Magnetic Resonance Imaging: Advanced Adjuncts in Preoperative Planning for Central Region Tumors , 2011, Neurosurgery.

[38]  M. Berger,et al.  Dynamics of hemispheric dominance for language assessed by magnetoencephalographic imaging , 2012, Annals of neurology.

[39]  B. Meyer,et al.  Utility of presurgical navigated transcranial magnetic brain stimulation for the resection of tumors in eloquent motor areas. , 2012, Journal of neurosurgery.

[40]  D Passarelli,et al.  Rapid‐rate transcranial magnetic stimulation and hemispheric language dominance , 1994, Neurology.

[41]  RP Dum,et al.  Topographic organization of corticospinal projections from the frontal lobe: motor areas on the lateral surface of the hemisphere , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[42]  Bernhard Meyer,et al.  Motor areas of the frontal cortex in patients with motor eloquent brain lesions. , 2016, Journal of neurosurgery.

[43]  F. Pulvermüller,et al.  Early Parallel Activation of Semantics and Phonology in Picture Naming: Evidence from a Multiple Linear Regression MEG Study , 2014, Cerebral cortex.

[44]  J. Rademacher,et al.  Variability and asymmetry in the human precentral motor system. A cytoarchitectonic and myeloarchitectonic brain mapping study. , 2001, Brain : a journal of neurology.

[45]  RP Dum,et al.  Topographic organization of corticospinal projections from the frontal lobe: motor areas on the medial surface of the hemisphere , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[46]  G A Ojemann,et al.  Neurophysiological monitoring during astrocytoma surgery. , 1990, Neurosurgery clinics of North America.

[47]  B. Abou-Khalil Methods for determination of language dominance: The wada test and proposed noninvasive alternatives , 2007, Current neurology and neuroscience reports.

[48]  M Hallett,et al.  Topographic maps of human motor cortex in normal and pathological conditions: mirror movements, amputations and spinal cord injuries. , 1991, Electroencephalography and clinical neurophysiology. Supplement.

[49]  A. Nobre,et al.  Dissociating Linguistic Processes in the Left Inferior Frontal Cortex with Transcranial Magnetic Stimulation , 2022 .

[50]  Riitta Salmelin,et al.  Cortical dynamics of visual/semantic vs. phonological analysis in picture confrontation , 2006, NeuroImage.

[51]  Peter Vajkoczy,et al.  The preoperative use of navigated transcranial magnetic stimulation facilitates early resection of suspected low-grade gliomas in the motor cortex , 2013, Acta Neurochirurgica.

[52]  Jean-Pascal Lefaucheur,et al.  Principles of therapeutic use of transcranial and epidural cortical stimulation , 2008, Clinical Neurophysiology.

[53]  J. Lefaucheur Neurophysiology of cortical stimulation. , 2012, International review of neurobiology.

[54]  J. Lefaucheur,et al.  Why image-guided navigation becomes essential in the practice of transcranial magnetic stimulation , 2010, Neurophysiologie Clinique/Clinical Neurophysiology.

[55]  Petro Julkunen,et al.  Alternative Stimulation Intensities for Mapping Cortical Motor Area with Navigated TMS , 2016, Brain Topography.

[56]  J A Maldjian,et al.  The effect of brain tumors on BOLD functional MR imaging activation in the adjacent motor cortex: implications for image-guided neurosurgery. , 2000, AJNR. American journal of neuroradiology.

[57]  O. Suess,et al.  Intra-Operative Mapping of the Motor Cortex During Surgery in and Around the Motor Cortex , 2000, Acta Neurochirurgica.

[58]  Armin Thron,et al.  Introducing navigated transcranial magnetic stimulation as a refined brain mapping methodology , 2001, Neurosurgical Review.

[59]  Pierre Brugières,et al.  The Hand Motor Hotspot is not Always Located in the Hand Knob: A Neuronavigated Transcranial Magnetic Stimulation Study , 2016, Brain Topography.

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

[61]  Johannes B Reitsma,et al.  Can fMRI safely replace the Wada test for preoperative assessment of language lateralisation? A meta-analysis and systematic review , 2013, Journal of Neurology, Neurosurgery & Psychiatry.

[62]  C. Zimmer,et al.  Combined noninvasive language mapping by navigated transcranial magnetic stimulation and functional MRI and its comparison with direct cortical stimulation. , 2015, Journal of neurosurgery.

[63]  V. Amassian,et al.  Physiological basis of motor effects of a transient stimulus to cerebral cortex. , 1987, Neurosurgery.

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

[65]  P. Matthews,et al.  The role of ipsilateral premotor cortex in hand movement after stroke , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[66]  Elke Hattingen,et al.  Motor cortex evaluation by nTMS after surgery of central region tumors: a feasibility study , 2012, Acta Neurochirurgica.

[67]  E. Chang,et al.  Stereotactic probability and variability of speech arrest and anomia sites during stimulation mapping of the language dominant hemisphere. , 2017, Journal of neurosurgery.

[68]  V. Tronnier,et al.  [Preoperative functional magnetic resonance tomography (FMRI) in patients with rolandic brain tumors: indication, investigation strategy, possibilities and limitations of clinical application]. , 2003, RoFo : Fortschritte auf dem Gebiete der Rontgenstrahlen und der Nuklearmedizin.

[69]  Pierre Brugières,et al.  Reappraisal of the anatomical landmarks of motor and premotor cortical regions for image‐guided brain navigation in TMS practice , 2014, Human brain mapping.

[70]  J. Karhu,et al.  Navigated transcranial magnetic stimulation , 2010, Neurophysiologie Clinique/Clinical Neurophysiology.

[71]  Alessandro Perin,et al.  Practical assessment of preoperative functional mapping techniques: navigated transcranial magnetic stimulation and functional magnetic resonance imaging , 2013, Neurological Sciences.

[72]  Mitchel S Berger,et al.  Intraoperative subcortical stimulation mapping for hemispherical perirolandic gliomas located within or adjacent to the descending motor pathways: evaluation of morbidity and assessment of functional outcome in 294 patients. , 2004, Journal of neurosurgery.

[73]  J. Rothwell,et al.  The physiological basis of transcranial motor cortex stimulation in conscious humans , 2004, Clinical Neurophysiology.

[74]  Manoel J Teixeira,et al.  Cortical mapping with navigated transcranial magnetic stimulation in low-grade glioma surgery , 2012, Neuropsychiatric disease and treatment.

[75]  Emmanuel Mandonnet,et al.  A re-examination of neural basis of language processing: Proposal of a dynamic hodotopical model from data provided by brain stimulation mapping during picture naming , 2014, Brain and Language.

[76]  Bernhard Meyer,et al.  Preoperative motor mapping by navigated transcranial magnetic brain stimulation improves outcome for motor eloquent lesions. , 2014, Neuro-oncology.

[77]  B R Rosen,et al.  Functional magnetic resonance imaging and transcranial magnetic stimulation , 1997, Neurology.

[78]  Eero Salli,et al.  Applicability of nTMS in locating the motor cortical representation areas in patients with epilepsy , 2013, Acta Neurochirurgica.

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

[80]  B. Day,et al.  Electric and magnetic stimulation of human motor cortex: surface EMG and single motor unit responses. , 1989, The Journal of physiology.

[81]  R. Salmelin Clinical neurophysiology of language: The MEG approach , 2007, Clinical Neurophysiology.

[82]  B. Meyer,et al.  Repeated mapping of cortical language sites by preoperative navigated transcranial magnetic stimulation compared to repeated intraoperative DCS mapping in awake craniotomy , 2014, BMC Neuroscience.

[83]  D Le Bihan,et al.  Correspondence between functional magnetic resonance imaging somatotopy and individual brain anatomy of the central region: comparison with intraoperative stimulation in patients with brain tumors. , 2000, Journal of neurosurgery.

[84]  Peter Vajkoczy,et al.  Plastic relocation of motor cortex in a patient with LGG (low grade glioma) confirmed by NBS (navigated brain stimulation) , 2012, Acta Neurochirurgica.

[85]  Bernhard Meyer,et al.  Diffusion tensor imaging fiber tracking using navigated brain stimulation—a feasibility study , 2012, Acta Neurochirurgica.

[86]  J. Lefaucheur Methods of therapeutic cortical stimulation , 2009, Neurophysiologie Clinique/Clinical Neurophysiology.

[87]  C. Zimmer,et al.  The impact of preoperative language mapping by repetitive navigated transcranial magnetic stimulation on the clinical course of brain tumor patients , 2015, BMC Cancer.

[88]  V E Amassian,et al.  Mapping of motor cortex gyral sites non-invasively by transcranial magnetic stimulation in normal subjects and patients. , 1991, Electroencephalography and clinical neurophysiology. Supplement.

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

[90]  Robert Chen,et al.  The clinical diagnostic utility of transcranial magnetic stimulation: Report of an IFCN committee , 2008, Clinical Neurophysiology.

[91]  Jyrki P. Mäkelä,et al.  Functional Plasticity of the Motor Cortical Structures Demonstrated by Navigated TMS in Two Patients with Epilepsy , 2013, Brain Stimulation.

[92]  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.

[93]  J. Karhu,et al.  First preoperative functional mapping via navigated transcranial magnetic stimulation in a 3-year-old boy. , 2012, Journal of neurosurgery. Pediatrics.

[94]  Thomas Picht,et al.  Current and potential utility of transcranial magnetic stimulation in the diagnostics before brain tumor surgery. , 2014, CNS oncology.

[95]  S. Schmidt,et al.  Definition of DLPFC and M1 according to anatomical landmarks for navigated brain stimulation: Inter-rater reliability, accuracy, and influence of gender and age , 2013, NeuroImage.