J Neurol Surg A Cent Eur Neurosurg 2020; 81(02): 130-137
DOI: 10.1055/s-0040-1701236
Original Article
Georg Thieme Verlag KG Stuttgart · New York

Hemispheric Dominance for Language and Side Effects in Mapping the Inferior Frontal Junction Area with Transcranial Magnetic Stimulation

1   Department of Neurosurgery, Medical Faculty, RWTH Aachen University, Aachen, Germany
2   Department of Psychiatry, Psychotherapy and Psychosomatics, Medical Faculty, RWTH Aachen University, Aachen, Germany
,
Johanna Blume-Schnitzler
1   Department of Neurosurgery, Medical Faculty, RWTH Aachen University, Aachen, Germany
,
Grit Frankemölle
1   Department of Neurosurgery, Medical Faculty, RWTH Aachen University, Aachen, Germany
,
Vanessa Drews
1   Department of Neurosurgery, Medical Faculty, RWTH Aachen University, Aachen, Germany
,
Stefan Heim
2   Department of Psychiatry, Psychotherapy and Psychosomatics, Medical Faculty, RWTH Aachen University, Aachen, Germany
3   Research Centre Jülich, Institute of Neuroscience and Medicine (INM-1), Jülich, Germany
4   JARA – Translational Brain Medicine, Aachen, Germany
,
Klaus Willmes
5   Department of Neurology, Medical Faculty, RWTH Aachen University, Aachen, Germany
,
Hans Clusmann
1   Department of Neurosurgery, Medical Faculty, RWTH Aachen University, Aachen, Germany
,
Georg Neuloh
1   Department of Neurosurgery, Medical Faculty, RWTH Aachen University, Aachen, Germany
› Author Affiliations
Further Information

Publication History

12 December 2018

30 October 2019

Publication Date:
11 February 2020 (online)

Abstract

Background and Study Aims Language mapping by navigated transcranial magnetic stimulation (TMS) is commonly applied over the left language-dominant hemisphere to indicate the language-related cortex. Detailed language mapping of Broca's region including stimulation targets in the immediate vicinity to the premotor cortex may raise concern about confounding unspecific motor effects. We performed interhemispheric comparisons to delineate such possible unspecific effects from true TMS-induced language inhibition.

Material and Methods Fifteen healthy German speakers named object pictures during navigated TMS over a left- and right-hemispheric target array covering the left inferior frontal junction area. Six mapping repetitions were conducted per hemisphere. Order of stimulation side was randomized between participants. Self-rating of discomfort was assessed after each stimulation; language errors and motor side effects were evaluated offline.

Results Naming errors were observed significantly more frequently during left- than right-hemispheric stimulation. The same pattern was found for the most frequent error category of performance errors. Hierarchical cluster analyses of normalized ratings of error severity revealed a clear focus of TMS susceptibility for language inhibition in object naming at the dorsoposterior target sites only in the left hemisphere. We found no statistical difference in discomfort ratings between both hemispheres and also no interhemispheric difference in motor side effects, but we observed significantly stronger muscle contractions of the eyes as compared with the mouth.

Conclusion Our results of (1) unspecific pre-/motor effects similarly induced in both hemispheres, and (2) a specific focus of TMS susceptibility in the language-dominant hemisphere render any substantial contribution of nonlanguage-specific effects in TMS language mapping of the inferior frontal junction area highly unlikely.

Note

An oral presentation of this work took place at the 15th Annual Meeting of the German Society of Neurosurgery (Deutsche Gesellschaft für Neurochirurgie); May 2017; Magdeburg, Germany.


 
  • References

  • 1 Espadaler JM, Conesa G. Navigated repetitive Transcranial Magnetic Stimulation (TMS) for language mapping: a new tool for surgical planning. In: Duffau H. , ed. Brain mapping: from Neural Basis of Cognition to Surgical Applications. Vienna, Austria: Springer; 2011: 253-261
  • 2 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
  • 3 Tarapore PE, Findlay AM, Honma SM. , et al. Language mapping with navigated repetitive TMS: proof of technique and validation. Neuroimage 2013; 82: 260-272
  • 4 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
  • 5 Sollmann N, Ille S, Hauck T. , et al. 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
  • 6 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
  • 7 Tarapore PE, Picht T, Bulubas L. , et al. Safety and tolerability of navigated TMS for preoperative mapping in neurosurgical patients. Clin Neurophysiol 2016; 127 (03) 1895-1900
  • 8 Raffa G, Quattropani MC, Scibilia A. , et al. Surgery of language-eloquent tumors in patients not eligible for awake surgery: the impact of a protocol based on navigated transcranial magnetic stimulation on presurgical planning and language outcome, with evidence of tumor-induced intra-hemispheric plasticity. Clin Neurol Neurosurg 2018; 168: 127-139
  • 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 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
  • 11 Rogić M, Deletis V, Fernández-Conejero I. Inducing transient language disruptions by mapping of Broca's area with modified patterned repetitive transcranial magnetic stimulation protocol. J Neurosurg 2014; 120 (05) 1033-1041
  • 12 Krieg SM, Sollmann N, Tanigawa N, Foerschler A, Meyer B, Ringel F. Cortical distribution of speech and language errors investigated by visual object naming and navigated transcranial magnetic stimulation. Brain Struct Funct 2016; 221 (04) 2259-2286
  • 13 Sollmann N, Ille S, Boeckh-Behrens T, Ringel F, Meyer B, Krieg SM. Mapping of cortical language function by functional magnetic resonance imaging and repetitive navigated transcranial magnetic stimulation in 40 healthy subjects. Acta Neurochir (Wien) 2016; 158 (07) 1303-1316
  • 14 Sakreida K, Lange I, Willmes K. , et al. High-resolution language mapping of Broca's region with transcranial magnetic stimulation. Brain Struct Funct 2018; 223 (03) 1297-1312
  • 15 Sakreida K, Blume-Schnitzler J, Heim S, Willmes K, Clusmann H, Neuloh G. Phonological picture-word interference in language mapping with transcranial magnetic stimulation: an objective approach for functional parcellation of Broca's region. Brain Struct Funct 2019; 224 (06) 2027-2044
  • 16 Krieg SM, Sollmann N, Hauck T. , et al. Functional language shift to the right hemisphere in patients with language-eloquent brain tumors. PLoS One 2013; 8 (09) e75403
  • 17 Sollmann N, Tanigawa N, Ringel F, Zimmer C, Meyer B, Krieg SM. Language and its right-hemispheric distribution in healthy brains: an investigation by repetitive transcranial magnetic stimulation. Neuroimage 2014; 102 (Pt 2): 776-788
  • 18 Devlin JT, Watkins KE. Stimulating language: insights from TMS. Brain 2007; 130 (Pt 3): 610-622
  • 19 Hartwigsen G, Price CJ, Baumgaertner A. , et al. The right posterior inferior frontal gyrus contributes to phonological word decisions in the healthy brain: evidence from dual-site TMS. Neuropsychologia 2010; 48 (10) 3155-3163
  • 20 Hartwigsen G, Siebner HR. Probing the involvement of the right hemisphere in language processing with online transcranial magnetic stimulation in healthy volunteers. Aphasiology 2012; 26 (09) 1131-1152
  • 21 Sollmann N, Ille S, Obermueller T. , et al. The impact of repetitive navigated transcranial magnetic stimulation coil positioning and stimulation parameters on human language function. Eur J Med Res 2015; 20: 47
  • 22 Thielscher A, Opitz A, Windhoff M. Impact of the gyral geometry on the electric field induced by transcranial magnetic stimulation. Neuroimage 2011; 54 (01) 234-243
  • 23 Rossini PM, Burke D, Chen R. , 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. Clin Neurophysiol 2015; 126 (06) 1071-1107
  • 24 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
  • 25 Saur D, Kreher BW, Schnell S. , et al. Ventral and dorsal pathways for language. Proc Natl Acad Sci U S A 2008; 105 (46) 18035-18040
  • 26 Duffau H, Leroy M, Gatignol P. Cortico-subcortical organization of language networks in the right hemisphere: an electrostimulation study in left-handers. Neuropsychologia 2008; 46 (14) 3197-3209
  • 27 Chang EF, Wang DD, Perry DW, Barbaro NM, Berger MS. Homotopic organization of essential language sites in right and bilateral cerebral hemispheric dominance. J Neurosurg 2011; 114 (04) 893-902