J Neurol Surg A Cent Eur Neurosurg 2020; 81(02): 111-129
DOI: 10.1055/s-0039-1698382
Original Article
Georg Thieme Verlag KG Stuttgart · New York

Impact of Priming on Effectiveness of TMS in Detecting Language-eloquent Brain Areas in Tumor Patients

Sascha Freigang
1   Department of Neurosurgery, Medical University of Graz, Graz, Austria
2   Department of Basic and Clinical Neuroscience, King's College London, London, United Kingdom
,
3   Institute of Psychology, University of Graz, Graz, Austria
4   BioTechMed, Graz, Graz, Austria
,
Kariem Mahdy Ali
1   Department of Neurosurgery, Medical University of Graz, Graz, Austria
,
Karla Zaar
1   Department of Neurosurgery, Medical University of Graz, Graz, Austria
,
Margit Jehna
5   Department of Radiology, Medical University of Graz, Graz, Austria
,
Gernot Reishofer
5   Department of Radiology, Medical University of Graz, Graz, Austria
,
Katrin Rammel
1   Department of Neurosurgery, Medical University of Graz, Graz, Austria
,
Fritz Studencnik
5   Department of Radiology, Medical University of Graz, Graz, Austria
,
Anja Ischebeck
3   Institute of Psychology, University of Graz, Graz, Austria
4   BioTechMed, Graz, Graz, Austria
,
Gord von Campe
1   Department of Neurosurgery, Medical University of Graz, Graz, Austria
› Author Affiliations
Further Information

Publication History

18 December 2018

16 April 2019

Publication Date:
14 January 2020 (online)

Abstract

Background and Study Aims Language is characteristically human, and preserving it is critical when resecting tumors in language-eloquent brain areas. Navigated repetitive transcranial magnetic stimulation (nrTMS) has been used in recent years as a noninvasive technique to identify preoperatively the language-eloquent cortical areas in tumor patients. An important objective is to increase the sensitivity and specificity of nrTMS in detecting language-related areas and increase the positive correlation of its results to that of intraoperative direct cortical stimulation (DCS). Although the technical aspects of the procedure have received enormous interest, factors related to the targeted cortical area such as previous cortical history or activity have been neglected. Therefore, the present study explores the impact of previous cortical history or activity on the effectiveness of a subsequent nrTMS mapping paradigm.

Materials and Methods Twelve right-handed patients with a left hemispheric glioma underwent presurgical nrTMS language mapping and intraoperative language mapping with DCS. nrTMS was performed using a continuous theta burst stimulation paradigm to inhibit possible language relevant areas in the vicinity of the tumor, determined anatomically or based on functional magnetic resonance imaging hotspots. The nrTMS was applied in two separate sessions. One of the sessions randomly included a priming paradigm to precondition the targeted cortical areas.

Results Priming stimulation decreased the error detection of the subsequent nrTMS mapping paradigm. This effect was more robust on major types of errors such as speech arrest and hesitation.

Conclusion Prior cortical activity as induced by the priming stimulation has a profound impact on the responsiveness to the nrTMS mapping paradigm. Our findings further showed that metaplasticity, a type of homeostatic plastic process, could be elicited even in cortical areas affected by a growing tumor.

 
  • References

  • 1 Picht T, Krieg SM, Sollmann N. , et al. A comparison of language mapping by preoperative navigated transcranial magnetic stimulation and direct cortical stimulation during awake surgery. Neurosurgery 2013; 72 (05) 808-819
  • 2 Hervey-Jumper SL, Berger MS. Maximizing safe resection of low- and high-grade glioma. J Neurooncol 2016; 130 (02) 269-282
  • 3 Sollmann N, Picht T, Mäkelä JP, Meyer B, Ringel F, Krieg SM. Navigated transcranial magnetic stimulation for preoperative language mapping in a patient with a left frontoopercular glioblastoma. J Neurosurg 2013; 118 (01) 175-179
  • 4 Gasser T, Ganslandt O, Sandalcioglu E, Stolke D, Fahlbusch R, Nimsky C. Intraoperative functional MRI: implementation and preliminary experience. Neuroimage 2005; 26 (03) 685-693
  • 5 Forster M-T, Hattingen E, Senft C, Gasser T, Seifert V, Szelényi A. Navigated transcranial magnetic stimulation and functional magnetic resonance imaging: advanced adjuncts in preoperative planning for central region tumors. Neurosurgery 2011; 68 (05) 1317-1324 ; discussion 1324–1325
  • 6 Roux FE, Boulanouar K, Lotterie JA, Mejdoubi M, LeSage JP, Berry I. Language functional magnetic resonance imaging in preoperative assessment of language areas: correlation with direct cortical stimulation. Neurosurgery 2003; 52 (06) 1335-1345 ; discussion 1345–1347
  • 7 Zandbelt BB, Gladwin TE, Raemaekers M. , et al. Within-subject variation in BOLD-fMRI signal changes across repeated measurements: quantification and implications for sample size. Neuroimage 2008; 42 (01) 196-206
  • 8 Giussani C, Roux FE, Ojemann J, Sganzerla EP, Pirillo D, Papagno C. Is preoperative functional magnetic resonance imaging reliable for language areas mapping in brain tumor surgery? Review of language functional magnetic resonance imaging and direct cortical stimulation correlation studies. Neurosurgery 2010; 66 (01) 113-120
  • 9 Krieg SM, Lioumis P, Mäkelä JP. , et al. Protocol for motor and language mapping by navigated TMS in patients and healthy volunteers; workshop report. Acta Neurochir (Wien) 2017; 159 (07) 1187-1195
  • 10 Shamov T, Spiriev T, Tzvetanov P, Petkov A. The combination of neuronavigation with transcranial magnetic stimulation for treatment of opercular gliomas of the dominant brain hemisphere. Clin Neurol Neurosurg 2010; 112 (08) 672-677
  • 11 Hendrix P, Senger S, Simgen A, Griessenauer CJ, Oertel J. Preoperative rTMS language mapping in speech-eloquent brain lesions resected under general anesthesia: a pair-matched cohort study. World Neurosurg 2017; 100: 425-433
  • 12 Barker AT, Jalinous R, Freeston IL. Non-invasive magnetic stimulation of human motor cortex. Lancet 1985; 1 (8437): 1106-1107
  • 13 Pascual-Leone A, Valls-Solé J, Wassermann EM, Hallett M. Responses to rapid-rate transcranial magnetic stimulation of the human motor cortex. Brain 1994; 117 (Pt 4): 847-85
  • 14 Houdayer E, Degardin A, Cassim F, Bocquillon P, Derambure P, Devanne H. The effects of low- and high-frequency repetitive TMS on the input/output properties of the human corticospinal pathway. Exp Brain Res 2008; 187 (02) 207-217
  • 15 Wassermann EM, Wedegaertner FR, Ziemann U, George MS, Chen R. Crossed reduction of human motor cortex excitability by 1-Hz transcranial magnetic stimulation. Neurosci Lett 1998; 250 (03) 141-144
  • 16 Huang Y-Z, Edwards MJ, Rounis E, Bhatia KP, Rothwell JC. Theta burst stimulation of the human motor cortex. Neuron 2005; 45 (02) 201-206
  • 17 Hoogendam JM, Ramakers GMJ, Di Lazzaro V. Physiology of repetitive transcranial magnetic stimulation of the human brain. Brain Stimul 2010; 3 (02) 95-118
  • 18 Pascual-Leone A, Walsh V, Rothwell J. Transcranial magnetic stimulation in cognitive neuroscience—virtual lesion, chronometry, and functional connectivity. Curr Opin Neurobiol 2000; 10 (02) 232-237
  • 19 Kubben PL. Brain mapping: from neural basis of cognition to surgical applications. Surg Neurol Int 2012; 3: 77
  • 20 Shapiro KA, Pascual-Leone A, Mottaghy FM, Gangitano M, Caramazza A. Grammatical distinctions in the left frontal cortex. J Cogn Neurosci 2001; 13 (06) 713-720
  • 21 Pascual-Leone A, Gates JR, Dhuna A. Induction of speech arrest and counting errors with rapid-rate transcranial magnetic stimulation. Neurology 1991; 41 (05) 697-702
  • 22 Whitney C, Kirk M, O'Sullivan J, Lambon Ralph MA, Jefferies E. The neural organization of semantic control: TMS evidence for a distributed network in left inferior frontal and posterior middle temporal gyrus. Cereb Cortex 2011; 21 (05) 1066-1075
  • 23 Sakai KL, Noguchi Y, Takeuchi T, Watanabe E. Selective priming of syntactic processing by event-related transcranial magnetic stimulation of Broca's area. Neuron 2002; 35 (06) 1177-1182
  • 24 Cappa SF, Sandrini M, Rossini PM, Sosta K, Miniussi C. The role of the left frontal lobe in action naming: rTMS evidence. Neurology 2002; 59 (05) 720-723
  • 25 Lioumis P, Zhdanov A, Mäkelä N. , et al. A novel approach for documenting naming errors induced by navigated transcranial magnetic stimulation. J Neurosci Methods 2012; 204 (02) 349-354
  • 26 Krieg SM, Tarapore PE, Picht T. , et al. Optimal timing of pulse onset for language mapping with navigated repetitive transcranial magnetic stimulation. Neuroimage 2014; 100: 219-236
  • 27 Hauck T, Tanigawa N, Probst M. , et al. Stimulation frequency determines the distribution of language positive cortical regions during navigated transcranial magnetic brain stimulation. BMC Neurosci 2015; 16 (01) 5
  • 28 Hauck T, Tanigawa N, Probst M. , et al. Task type affects location of language-positive cortical regions by repetitive navigated transcranial magnetic stimulation mapping. PLoS One 2015; 10 (04) e0125298
  • 29 Sollmann N, Fuss-Ruppenthal S, Zimmer C, Meyer B, Krieg SM. Investigating stimulation protocols for language mapping by repetitive navigated transcranial magnetic stimulation. Front Behav Neurosci 2018; 12 (197) 197
  • 30 Ille S, Kulchytska N, Sollmann N. , et al. Hemispheric language dominance measured by repetitive navigated transcranial magnetic stimulation and postoperative course of language function in brain tumor patients. Neuropsychologia 2016; 91: 50-60
  • 31 Abraham WC. Metaplasticity: tuning synapses and networks for plasticity. Nat Rev Neurosci 2008; 9 (05) 387
  • 32 Abraham WC, Bear MF. Metaplasticity: the plasticity of synaptic plasticity. Trends Neurosci 1996; 19 (04) 126-130
  • 33 Silvanto J, Bona S, Marelli M, Cattaneo Z. On the mechanisms of transcranial magnetic stimulation (TMS): how brain state and baseline performance level determine behavioral effects of TMS. Front Psychol 2018; 9: 741
  • 34 Andoh J, Artiges E, Pallier C. , et al. Priming frequencies of transcranial magnetic stimulation over Wernicke's area modulate word detection. Cereb Cortex 2008; 18 (01) 210-216
  • 35 Iyer MB, Schleper N, Wassermann EM. Priming stimulation enhances the depressant effect of low-frequency repetitive transcranial magnetic stimulation. J Neurosci 2003; 23 (34) 10867-10872
  • 36 Kakuda W, Abo M, Momosaki R, Morooka A. Therapeutic application of 6-Hz-primed low-frequency rTMS combined with intensive speech therapy for post-stroke aphasia. Brain Inj 2011; 25 (12) 1242-1248
  • 37 Oldfield RC. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 1971; 9 (01) 97-113
  • 38 Rossi S, Hallett M, Rossini PM, Pascual-Leone A. ; Safety of TMS Consensus Group. Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research. Clin Neurophysiol 2009; 120 (12) 2008-2039
  • 39 Jenkinson M, Beckmann CF, Behrens TEJ, Woolrich MW, Smith SM. FSL. Neuroimage 2012; 62 (02) 782-790 . Doi: 10.1016/j.neuroimage.2011.09.015
  • 40 Sollmann N, Goblirsch-Kolb MF, Ille S. , et al. Comparison between electric-field-navigated and line-navigated TMS for cortical motor mapping in patients with brain tumors. Acta Neurochir (Wien) 2016; 158 (12) 2277-2289
  • 41 Kilbride RD. Intraoperative functional cortical mapping of language. J Clin Neurophysiol 2013; 30 (06) 591-596
  • 42 Nicholas LE, Brookshire RH, Maclennan DL, Schumacher JG, Porrazzo SA. Revised administration and scoring procedures for the Boston Naming test and norms for non-brain-damaged adults. Aphasiology 1989; 3 (06) 569-580
  • 43 Rossini PM, Berardelli A, Deuschl G. , et al; The International Federation of Clinical Neurophysiology. Applications of magnetic cortical stimulation. Electroencephalogr Clin Neurophysiol Suppl 1999; 52: 171-185
  • 44 Saarinen T, Laaksonen H, Parviainen T, Salmelin R. Motor cortex dynamics in visuomotor production of speech and non-speech mouth movements. Cereb Cortex 2006; 16 (02) 212-222
  • 45 Ille S, Sollmann N, Hauck T. , et al. Combined noninvasive language mapping by navigated transcranial magnetic stimulation and functional MRI and its comparison with direct cortical stimulation. J Neurosurg 2015; 123 (01) 212-225
  • 46 Corina DP, Loudermilk BC, Detwiler L, Martin RF, Brinkley JF, Ojemann G. Analysis of naming errors during cortical stimulation mapping: implications for models of language representation. Brain Lang 2010; 115 (02) 101-112
  • 47 Oberman L, Edwards D, Eldaief M, Pascual-Leone A. Safety of theta burst transcranial magnetic stimulation: a systematic review of the literature. J Clin Neurophysiol 2011; 28 (01) 67-74
  • 48 Wassermann EM. Risk and safety of repetitive transcranial magnetic stimulation: report and suggested guidelines from the International Workshop on the Safety of Repetitive Transcranial Magnetic Stimulation, June 5-7, 1996. Electroencephalogr Clin Neurophysiol 1998; 108 (01) 1-16
  • 49 Sanai N, Mirzadeh Z, Berger MS. Functional outcome after language mapping for glioma resection. N Engl J Med 2008; 358 (01) 18-27
  • 50 Ojemann G, Ojemann J, Lettich E, Berger M. Cortical language localization in left, dominant hemisphere. An electrical stimulation mapping investigation in 117 patients. J Neurosurg 1989; 71 (03) 316-326
  • 51 Tarapore PE, Findlay AM, Honma SM. , et al. Language mapping with navigated repetitive TMS: proof of technique and validation. Neuroimage 2013; 82: 260-272
  • 52 Kong NW, Gibb WR, Tate MC. Neuroplasticity: insights from patients harboring gliomas. Neural Plast 2016; 2016: 2365063
  • 53 Lehtinen H, Mäkelä JP, Mäkelä T. , et al. Language mapping with navigated transcranial magnetic stimulation in pediatric and adult patients undergoing epilepsy surgery: Comparison with extraoperative direct cortical stimulation. Epilepsia Open 2018; 3 (02) 224-235
  • 54 Rösler J, Niraula B, Strack V. , et al. Language mapping in healthy volunteers and brain tumor patients with a novel navigated TMS system: evidence of tumor-induced plasticity. Clin Neurophysiol 2014; 125 (03) 526-536
  • 55 Alle H, Heidegger T, Kriváneková L, Ziemann U. Interactions between short-interval intracortical inhibition and short-latency afferent inhibition in human motor cortex. J Physiol 2009; 587 (Pt 21): 5163-5176
  • 56 Stagg CJ, Wylezinska M, Matthews PM. , et al. Neurochemical effects of theta burst stimulation as assessed by magnetic resonance spectroscopy. J Neurophysiol 2009; 101 (06) 2872-2877
  • 57 Friederici AD, Gierhan SME. The language network. Curr Opin Neurobiol 2013; 23 (02) 250-254
  • 58 Binder JR. The Wernicke area: modern evidence and a reinterpretation. Neurology 2015; 85 (24) 2170-2175
  • 59 Flinker A, Korzeniewska A, Shestyuk AY. , et al. Redefining the role of Broca's area in speech. Proc Natl Acad Sci U S A 2015; 112 (09) 2871-2875
  • 60 Thiel A, Habedank B, Herholz K. , et al. From the left to the right: how the brain compensates progressive loss of language function. Brain Lang 2006; 98 (01) 57-65
  • 61 Devlin JT, Watkins KE. Stimulating language: insights from TMS. Brain 2007; 130 (Pt 3): 610-622
  • 62 Conway N, Wildschuetz N, Moser T. , et al. Cortical plasticity of motor-eloquent areas measured by navigated transcranial magnetic stimulation in patients with glioma. J Neurosurg 2017; 127 (05) 981-991
  • 63 Sarubbo S, Le Bars E, Moritz-Gasser S, Duffau H. Complete recovery after surgical resection of left Wernicke's area in awake patient: a brain stimulation and functional MRI study. Neurosurg Rev 2012; 35 (02) 287-292 ; discussion 292
  • 64 Lowe CJ, Hall PA. Reproducibility and sources of interindividual variability in the responsiveness to prefrontal continuous theta burst stimulation (cTBS). Neurosci Lett 2018; 687: 280-284
  • 65 Vernet M, Bashir S, Yoo W-K. , et al. Reproducibility of the effects of theta burst stimulation on motor cortical plasticity in healthy participants. Clin Neurophysiol 2014; 125 (02) 320-326
  • 66 Cheeran B, Talelli P, Mori F. , et al. A common polymorphism in the brain-derived neurotrophic factor gene (BDNF) modulates human cortical plasticity and the response to rTMS. J Physiol 2008; 586 (23) 5717-5725
  • 67 Jannati A, Block G, Oberman LM, Rotenberg A, Pascual-Leone A. Interindividual variability in response to continuous theta-burst stimulation in healthy adults. Clin Neurophysiol 2017; 128 (11) 2268-2278
  • 68 Southwell DG, Hervey-Jumper SL, Perry DW, Berger MS. Intraoperative mapping during repeat awake craniotomy reveals the functional plasticity of adult cortex. J Neurosurg 2016; 124 (05) 1460-1469
  • 69 Hurley R, Machado L. Using tDCS priming to improve brain function: can metaplasticity provide the key to boosting outcomes?. Neurosci Biobehav Rev 2017; 83: 155-159
  • 70 Turrigiano GG. The self-tuning neuron: synaptic scaling of excitatory synapses. Cell 2008; 135 (03) 422-435
  • 71 Cassidy JM, Gillick BT, Carey JR. Priming the brain to capitalize on metaplasticity in stroke rehabilitation. Phys Ther 2014; 94 (01) 139-150
  • 72 Bienenstock EL, Cooper LN, Munro PW. Theory for the development of neuron selectivity: orientation specificity and binocular interaction in visual cortex. J Neurosci 1982; 2 (01) 32-48
  • 73 Indefrey P. The spatial and temporal signatures of word production components: a critical update. Front Psychol 2011; 2: 255
  • 74 Fraga de Abreu VH, Peck KK, Petrovich-Brennan NM, Woo KM, Holodny AI. Brain tumors: the influence of tumor type and routine MR imaging characteristics at BOLD functional MR imaging in the primary motor gyrus. Radiology 2016; 281 (03) 876-88
  • 75 Hou BL, Bradbury M, Peck KK, Petrovich NM, Gutin PH, Holodny AI. Effect of brain tumor neovasculature defined by rCBV on BOLD fMRI activation volume in the primary motor cortex. Neuroimage 2006; 32 (02) 489-497
  • 76 Epstein CM, Meador KJ, Loring DW. , et al. Localization and characterization of speech arrest during transcranial magnetic stimulation. Clin Neurophysiol 1999; 110 (06) 1073-1079
  • 77 Sollmann N, Hauck T, Obermüller T. , et al. Inter- and intraobserver variability in motor mapping of the hotspot for the abductor policis brevis muscle. BMC Neurosci 2013; 14 (01) 94
  • 78 Histed MH, Bonin V, Reid RC. Direct activation of sparse, distributed populations of cortical neurons by electrical microstimulation. Neuron 2009; 63 (04) 508-522