Optimal timing of pulse onset for language mapping with navigated repetitive transcranial magnetic stimulation

NeuroImage

Volumn 100, Issue , 2014, Pages 219-236

  Krieg, Sandro M ^a   Tarapore, Phiroz E ^b   Picht, Thomas ^c   Tanigawa, Noriko ^b   Houde, John ^b   Sollmann, Nico ^a   Meyer, Bernhard ^a   Vajkoczy, Peter ^c   Berger, Mitchel S ^b   Ringel, Florian ^a   Nagarajan, Srikantan ^b  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

Awake surgery; Language; Preoperative mapping; Transcranial magnetic stimulation; Tumor

Indexed keywords

ADULT; AGED; APHASIA; ARTICLE; AWAKE SURGERY; BRAIN DEPTH STIMULATION; BRAIN MAPPING; BRAIN SURGERY; BRAIN TUMOR; CLINICAL ARTICLE; CONTROLLED STUDY; CORRELATIONAL STUDY; DIAGNOSTIC ACCURACY; DIAGNOSTIC TEST ACCURACY STUDY; DIAGONAL BAND OF BROCA; DIRECT CORTICAL STIMULATION; FEMALE; HUMAN; INTERMETHOD COMPARISON; LANGUAGE; MALE; MIDDLE AGED; NAVIGATED REPETITIVE TRANSCRANIAL MAGNETIC STIMULATION; NERVOUS SYSTEM PARAMETERS; OUTCOME ASSESSMENT; PEROPERATIVE CARE; PREDICTIVE VALUE; PREOPERATIVE CARE; PRIORITY JOURNAL; PULSE TRAIN ONSET; RECEIVER OPERATING CHARACTERISTIC; SEMANTICS; SENSITIVITY AND SPECIFICITY; TRANSCRANIAL MAGNETIC STIMULATION; VISUAL STIMULATION; WERNICKE AREA; YOUNG ADULT; BRAIN CORTEX; BRAIN NEOPLASMS; CLINICAL TRIAL; COMPARATIVE STUDY; MULTICENTER STUDY; NEURONAVIGATION; PATIENT MONITORING; PROCEDURES; STANDARDS; TRANSCRANIAL DIRECT CURRENT STIMULATION;

ADULT; AGED; BRAIN MAPPING; BRAIN NEOPLASMS; CEREBRAL CORTEX; FEMALE; HUMANS; INTRAOPERATIVE NEUROPHYSIOLOGICAL MONITORING; LANGUAGE; MALE; MIDDLE AGED; NEURONAVIGATION; PREOPERATIVE CARE; TRANSCRANIAL DIRECT CURRENT STIMULATION; TRANSCRANIAL MAGNETIC STIMULATION;

EID: 84903878990     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2014.06.016     Document Type: Article

References (84)

1. Acheson D.J., Hamidi M., Binder J.R., Postle B.R. A common neural substrate for language production and verbal working memory. J. Cogn. Neurosci. 2011, 23:1358-1367.
2. Bagley S.C., White H., Golomb B.A. Logistic regression in the medical literature: standards for use and reporting, with particular attention to one medical domain. J. Clin. Epidemiol. 2001, 54:979-985.
3. Baum S.H., Martin R.C., Hamilton A.C., Beauchamp M.S. Multisensory speech perception without the left superior temporal sulcus. Neuroimage 2012, 62:1825-1832.
4. Binder J.R., Desai R.H., Graves W.W., Conant L.L. Where is the semantic system? A critical review and meta-analysis of 120 functional neuroimaging studies. Cereb. Cortex 2009, 19:2767-2796.
5. Bohland J.W., Bullock D., Guenther F.H. Neural representations and mechanisms for the performance of simple speech sequences. J. Cogn. Neurosci. 2010, 22:1504-1529.
6. Bonner M.F., Peelle J.E., Cook P.A., Grossman M. Heteromodal conceptual processing in the angular gyrus. NeuroImage 2013, 71:175-186.
7. Briganti C., Sestieri C., Mattei P.A., Esposito R., Galzio R.J., Tartaro A., Romani G.L., Caulo M. Reorganization of functional connectivity of the language network in patients with brain gliomas. AJNR Am. J. Neuroradiol. 2012, 33(10):1983-1990. (Nov).
8. Corina D.P., Gibson E.K., Martin R., Poliakov A., Brinkley J., Ojemann G.A. Dissociation of action and object naming: evidence from cortical stimulation mapping. Hum. Brain Mapp. 2005, 24:1-10.
9. Corina D.P., Loudermilk B.C., Detwiler L., Martin R.F., Brinkley J.F., Ojemann G. Analysis of naming errors during cortical stimulation mapping: implications for models of language representation. Brain Lang. 2010, 115:101-112.
10. Devlin J.T., Watkins K.E. Stimulating language: insights from TMS. Brain 2007, 130:610-622.
11. Duffau H. New concepts in surgery of WHO grade II gliomas: functional brain mapping, connectionism and plasticity-a review. J. Neurooncol. 2006, 79:77-115.
12. Edwards E., Soltani M, Kim W, Dalal SS, Nagarajan SS, Berger MS, Knight RT Comparison of time-frequency responses and the event-related potential to auditory speech stimuli in human cortex. J Neurophysiol 2009, 102(1):377-386. (Jul).
13. Edwards E., Nagarajan S.S., Dalal S.S., Canolty R.T., Kirsch H.E., Barbaro N.M., Knight R.T. Spatiotemporal imaging of cortical activation during verb generation and picture naming. NeuroImage 2010, 50:291-301.
14. Epstein C.M. Transcranial magnetic stimulation: language function. J. Clin. Neurophysiol. 1998, 15:325-332.
15. Epstein C.M., Lah J.J., Meador K., Weissman J.D., Gaitan L.E., Dihenia B. Optimum stimulus parameters for lateralized suppression of speech with magnetic brain stimulation. Neurology 1996, 47:1590-1593.
16. Findlay A.M., Ambrose J.B., Cahn-Weiner D.A., Houde J.F., Honma S., Hinkley L.B., Berger M.S., Nagarajan S.S., Kirsch H.E. Dynamics of hemispheric dominance for language assessed by magnetoencephalographic imaging. Ann. Neurol. 2012, 71:668-686.
17. FitzGerald D.B., Cosgrove G.R., Ronner S., Jiang H., Buchbinder B.R., Belliveau J.W., Rosen B.R., Benson R.R. Location of language in the cortex: a comparison between functional MR imaging and electrocortical stimulation. AJNR Am. J. Neuroradiol. 1997, 18:1529-1539.
18. Friederici A.D. The cortical language circuit: from auditory perception to sentence comprehension. Trends Cogn. Sci. 2012, 16:262-268.
19. Giussani C., Roux F.E., Ojemann J., Sganzerla E.P., 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, 66:113-120.
20. Guggisberg A.G., Honma S.M., Findlay A.M., Dalal S.S., Kirsch H.E., Berger M.S., Nagarajan S.S. Mapping functional connectivity in patients with brain lesions. Ann. Neurol. 2008, 63:193-203.
21. Haglund M.M., Berger M.S., Shamseldin M., Lettich E., Ojemann G.A. Cortical localization of temporal lobe language sites in patients with gliomas. Neurosurgery 1994, 34:567-576. (discussion 576).
22. Hannula H., Ylioja S., Pertovaara A., Korvenoja A., Ruohonen J., Ilmoniemi R.J., Carlson S. Somatotopic blocking of sensation with navigated transcranial magnetic stimulation of the primary somatosensory cortex. Hum. Brain Mapp. 2005, 26:100-109.
23. Harpaz Y., Levkovitz Y., Lavidor M. Lexical ambiguity resolution in Wernicke's area and its right homologue. Cortex 2009, 45:1097-1103.
24. Hartwigsen G., Baumgaertner A., Price C.J., Koehnke M., Ulmer S., Siebner H.R. Phonological decisions require both the left and right supramarginal gyri. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:16494-16499.
25. Hickok G. Computational neuroanatomy of speech production. Nat. Rev. Neurosci. 2012, 13:135-145.
26. Houde J.F., Nagarajan S.S. Speech production as state feedback control. Front. Hum. Neurosci. 2011, 5:82.
27. Hulten A., Vihla M., Laine M., Salmelin R. Accessing newly learned names and meanings in the native language. Hum. Brain Mapp. 2009, 30:976-989.
28. Indefrey P. The spatial and temporal signatures of word production components: a critical update. Front. Psychol. 2011, 2:255.
29. Indefrey P., Levelt W.J. The spatial and temporal signatures of word production components. Cognition 2004, 92:101-144.
30. Ius T., Angelini E., Thiebaut de Schotten M., Mandonnet E., Duffau H. Evidence for potentials and limitations of brain plasticity using an atlas of functional resectability of WHO grade II gliomas: towards a "minimal common brain". NeuroImage 2011, 56:992-1000.
31. Jacquemot C., Scott S.K. What is the relationship between phonological short-term memory and speech processing?. Trends Cogn. Sci. 2006, 10:480-486.
32. Krieg S.M., Shiban E., Buchmann N., Gempt J., Foerschler A., Meyer B., Ringel F. Utility of presurgical navigated transcranial magnetic brain stimulation for the resection of tumors in eloquent motor areas. J. Neurosurg. 2012, 116:994-1001.
33. Lalkhen A.G., McCluskey A. Clinical tests: sensitivity and specificity. Continuing Education in Anaesthesia. Crit. Care Pain 2008, 8:221-223.
34. Lee H., Devlin J.T., Shakeshaft C., Stewart L.H., Brennan A., Glensman J., Pitcher K., Crinion J., Mechelli A., Frackowiak R.S., Green D.W., Price C.J. Anatomical traces of vocabulary acquisition in the adolescent brain. J. Neurosci. 2007, 27:1184-1189.
35. Lioumis P., Zhdanov A., Makela N., Lehtinen H., Wilenius J., Neuvonen T., Hannula H., Deletis V., Picht T., Makela J.P. A novel approach for documenting naming errors induced by navigated transcranial magnetic stimulation. J. Neurosci. Methods 2012, 204:349-354.
36. Makela J.P., Forss N., Jaaskelainen J., Kirveskari E., Korvenoja A., Paetau R. Magnetoencephalography in neurosurgery. Neurosurgery 2007, 61:147-164. (discussion 164-145).
37. Makuuchi M., Friederici A.D. Hierarchical functional connectivity between the core language system and the working memory system. Cortex 2013, 49:2416-2423.
38. Makuuchi M., Bahlmann J., Anwander A., Friederici A.D. Segregating the core computational faculty of human language from working memory. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:8362-8367.
39. Martino J., Honma S.M., Findlay A.M., Guggisberg A.G., Owen J.P., Kirsch H.E., Berger M.S., Nagarajan S.S. Resting functional connectivity in patients with brain tumors in eloquent areas. Ann. Neurol. 2011, 69:521-532.
40. Mima T. The role of the left angular/supramarginal gyrus in Japanese kanji reading (MEG+fMRI+TMS). Paper presented at US-Japan Workshop: Multimodal non-invasive techniques for the study of human brain physiology 2003, NINDS, Washington, D.C.
41. Ojemann G.A., Whitaker H.A. Language localization and variability. Brain Lang. 1978, 6:239-260.
42. 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, 71:316-326.
43. Pascual-Leone A., Gates J.R., Dhuna A. Induction of speech arrest and counting errors with rapid-rate transcranial magnetic stimulation. Neurology 1991, 41:697-702.
44. Penfield W., Boldrey E. Somatic motor and sensory representation in the cerebral cortex of man as studied by electrical stimulation. Brain 1937, 60:389-443.
45. Picht T., Kombos T., Gramm H.J., Brock M., Suess O. Multimodal protocol for awake craniotomy in language cortex tumour surgery. Acta Neurochir. (Wien) 2006, 148:127-137. (discussion 137-128).
46. Picht T., Mularski S., Kuehn B., Vajkoczy P., Kombos T., Suess O. Navigated transcranial magnetic stimulation for preoperative functional diagnostics in brain tumor surgery. Neurosurgery 2009, 65:93-98.
47. Picht T., Schmidt S., Brandt S., Frey D., Hannula H., Neuvonen T., Karhu J., Vajkoczy P., Suess O. Preoperative functional mapping for rolandic brain tumor surgery: comparison of navigated transcranial magnetic stimulation to direct cortical stimulation. Neurosurgery 2011, 69:581-588. (discussion 588).
48. Picht T., Krieg S.M., Sollmann N., Rosler J., Niraula B., Neuvonen T., Savolainen P., Lioumis P., Makela J.P., 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, 72:808-819.
49. Price C.J. A review and synthesis of the first 20years of PET and fMRI studies of heard speech, spoken language and reading. NeuroImage 2012, 62:816-847.
50. Price C.J., Crinion J.T., Macsweeney M. A generative model of speech production in Broca's and Wernicke's areas. Front. Psychol. 2011, 2:237.
51. Rauschecker J.P. Ventral and dorsal streams in the evolution of speech and language. Front. Evol. Neurosci. 2012, 4:7.
52. Robles S.G., Gatignol P., Lehericy S., Duffau H. Long-term brain plasticity allowing a multistage surgical approach to World Health Organization Grade II gliomas in eloquent areas. J. Neurosurg. 2008, 109:615-624.
53. Romero L., Walsh V., Papagno C. The neural correlates of phonological short-term memory: a repetitive transcranial magnetic stimulation study. J. Cogn. Neurosci. 2006, 18:1147-1155.
54. Roux F.E., Boulanouar K., Lotterie J.A., Mejdoubi M., LeSage J.P., Berry I. Language functional magnetic resonance imaging in preoperative assessment of language areas: correlation with direct cortical stimulation. Neurosurgery 2003, 52:1335-1345. (discussion 1345-1337).
55. Ruohonen J., Karhu J. Navigated transcranial magnetic stimulation. Neurophysiol. Clin. 2010, 40:7-17.
56. Rutten G.J., Ramsey N.F. The role of functional magnetic resonance imaging in brain surgery. Neurosurg. Focus. 2010, 28:E4.
57. Sacko O., Lauwers-Cances V., Brauge D., Sesay M., Brenner A., Roux F.E. Awake craniotomy vs surgery under general anesthesia for resection of supratentorial lesions. Neurosurgery 2011, 68:1192-1198. (discussion 1198-1199).
58. Saisanen L., Julkunen P., Niskanen E., Danner N., Hukkanen T., Lohioja T., Nurkkala J., Mervaala E., Karhu J., Kononen M. Motor potentials evoked by navigated transcranial magnetic stimulation in healthy subjects. J. Clin. Neurophysiol. 2008, 25:367-372.
59. Salmelin R., Hari R., Lounasmaa O.V., Sams M. Dynamics of brain activation during picture naming. Nature 1994, 368:463-465.
60. Sanai N., Berger M.S. Mapping the horizon: techniques to optimize tumor resection before and during surgery. Clin. Neurosurg. 2008, 55:14-19.
61. Sanai N., Berger M.S. Intraoperative stimulation techniques for functional pathway preservation and glioma resection. Neurosurg. Focus. 2010, 28:E1.
62. Sanai N., Mirzadeh Z., Berger M.S. Functional outcome after language mapping for glioma resection. N. Engl. J. Med. 2008, 358:18-27.
63. Schneidman E., Bialek W., Berry M.J. An information theoretic approach to the functional classification of neurons. Advances in Neural Information Processing 2002, 197-204. MIT Press, Cambridge, MA. S. Becker, Thrun, K. Obermayer (Eds.).
64. Schuhmann T., Schiller N.O., Goebel R., Sack A.T. The temporal characteristics of functional activation in Broca's area during overt picture naming. Cortex 2009, 45:1111-1116.
65. Schuhmann T., Schiller N.O., Goebel R., Sack A.T. Speaking of which: dissecting the neurocognitive network of language production in picture naming. Cereb. Cortex 2012, 22:701-709.
66. Seghier M.L., Fagan E., Price C.J. Functional subdivisions in the left angular gyrus where the semantic system meets and diverges from the default network. J. Neurosci. 2010, 30:16809-16817.
67. Sliwinska M.W., Khadilkar M., Campbell-Ratcliffe J., Quevenco F., Devlin J.T. Early and sustained supramarginal gyrus contributions to phonological processing. Front. Psychol. 2012, 3:161.
68. Sollmann N., Picht T., Makela J.P., Meyer B., Ringel F., Krieg S.M. Navigated transcranial magnetic stimulation for preoperative language mapping in a patient with a left frontoopercular glioblastoma. J. Neurosurg. 2013, 118:175-179.
69. Soros P., Cornelissen K., Laine M., Salmelin R. Naming actions and objects: cortical dynamics in healthy adults and in an anomic patient with a dissociation in action/object naming. NeuroImage 2003, 19:1787-1801.
70. Sparing R., Mottaghy F.M., Hungs M., Brugmann M., Foltys H., Huber W., Topper R. Repetitive transcranial magnetic stimulation effects on language function depend on the stimulation parameters. J. Clin. Neurophysiol. 2001, 18:326-330.
71. Stoeckel C., Gough P.M., Watkins K.E., Devlin J.T. Supramarginal gyrus involvement in visual word recognition. Cortex 2009, 45:1091-1096.
72. Stokes M.G., Chambers C.D., Gould I.C., Henderson T.R., Janko N.E., Allen N.B., Mattingley J.B. Simple metric for scaling motor threshold based on scalp-cortex distance: application to studies using transcranial magnetic stimulation. J. Neurophysiol. 2005, 94:4520-4527.
73. Stummer W., Reulen H.J., Meinel T., Pichlmeier U., Schumacher W., Tonn J.C., Rohde V., Oppel F., Turowski B., Woiciechowsky C., Franz K., Pietsch T. Extent of resection and survival in glioblastoma multiforme: identification of and adjustment for bias. Neurosurgery 2008, 62:564-576.
74. Tarapore P.E., Martino J., Guggisberg A.G., Owen J., Honma S.M., Findlay A., Berger M.S., Kirsch H.E., Nagarajan S.S. Magnetoencephalographic imaging of resting-state functional connectivity predicts postsurgical neurological outcome in brain gliomas. Neurosurgery 2012, 71:1012-1022.
75. Tarapore P.E., Tate M.C., Findlay A.M., Honma S.M., Mizuiri D., Berger M.S., Nagarajan S.S. Preoperative multimodal motor mapping: a comparison of magnetoencephalography imaging, navigated transcranial magnetic stimulation, and direct cortical stimulation. J Neurosurg 2012, 117:354-362.
76. Tarapore P.E., Findlay A.M., Honma S.M., Mizuiri D., Houde J.F., Berger M.S., Nagarajan S.S. Language mapping with navigated repetitive TMS: proof of technique and validation. NeuroImage 2013, 82:260-272.
77. Tian X., Poeppel D. The effect of imagination on stimulation: the functional specificity of efference copies in speech processing. J. Cogn. Neurosci. 2013, 25:1020-1036.
78. Van Poppel M., Wheless J.W., Clarke D.F., McGregor A., McManis M.H., Perkins F.F., Van Poppel K., Fulton S., Boop F.A. Passive language mapping with magnetoencephalography in pediatric patients with epilepsy. J Neurosurg Pediatr. 2012, 10:96-102.
79. Vigliocco G., Vinson D.P., Druks J., Barber H., Cappa S.F. Nouns and verbs in the brain: a review of behavioural, electrophysiological, neuropsychological and imaging studies. Neurosci. Biobehav. Rev. 2011, 35:407-426.
80. Vihla M., Laine M., Salmelin R. Cortical dynamics of visual/semantic vs. phonological analysis in picture confrontation. NeuroImage 2006, 33:732-738.
81. Voss J., Meier T.B., Freidel R., Kundu B., Nair V.A., Holdsworth R., Kuo J.S., Prabhakaran V. The role of secondary motor and language cortices in morbidity and mortality: a retrospective functional MRI study of surgical planning for patients with intracranial tumors. Neurosurg. Focus. 2013, 34:E7.
82. Wassermann E.M., Blaxton T.A., Hoffman E.A., Berry C.D., Oletsky H., Pascual-Leone A., Theodore W.H. Repetitive transcranial magnetic stimulation of the dominant hemisphere can disrupt visual naming in temporal lobe epilepsy patients. Neuropsychologia 1999, 37:537-544.
83. Wheat K.L., Cornelissen P.L., Sack A.T., Schuhmann T., Goebel R., Blomert L. Charting the functional relevance of Broca's area for visual word recognition and picture naming in Dutch using fMRI-guided TMS. Brain Lang. 2013, 125:223-230.
84. Yetkin F.Z., Mueller W.M., Morris G.L., McAuliffe T.L., Ulmer J.L., Cox R.W., Daniels D.L., Haughton V.M. Functional MR activation correlated with intraoperative cortical mapping. AJNR Am. J. Neuroradiol. 1997, 18:1311-1315.