Abstract
fMRI language mapping studies report right-hemispheric contribution to language in healthy individuals. However, it remains unclear whether these right-hemispheric patterns of activity are critical for language, which is highly relevant for clinical preoperative language mapping. The available findings are controversial. In this study, we first measured individual patterns of language lateralization with an fMRI language localizer in healthy participants with different handedness (N = 31). Then, the same participants received rTMS over the individual coordinates of peak fMRI-based activation in the left and right inferior frontal gyri. During rTMS, participants performed a picture naming task. It included both objects and actions to test whether naming of nouns and verbs would be equally modulated by rTMS. Stimulation of the left inferior frontal gyrus resulted in accuracy facilitation of verb production regardless of individual language lateralization. No modulation of object naming was found at any stimulation site in terms of accuracy nor reaction time. This study causally confirmed the critical contribution of the left, but not the right hemisphere to verb production regardless of the language lateralization patterns observed with fMRI. Also, the results stress that action rather than object naming is the task of choice for mapping language in the frontal lobe.
Similar content being viewed by others
Data availability
The datasets generated during and/or analysed during the current study are not publicly available, but are available from the corresponding author on reasonable request.
Change history
17 October 2022
The author names in reference section has been corrected.
References
Akinina Y, Malyutina S, Ivanova M, Iskra E, Mannova E, Dragoy O (2015) Russian normative data for 375 action pictures and verbs. Behav Res Methods 47(3):691–707. https://doi.org/10.3758/s13428-014-0492-9
Ardila A, Rosselli M (1994) Averbia as a selective naming disorder: a single case report. J Psycholinguist Res 23(2):139–148. https://doi.org/10.1007/bf02143920
Barnett A, Marty-Dugas J, McAndrews MP (2014) Advantages of sentence-level fMRI language tasks in presurgical language mapping for temporal lobe epilepsy. Epilepsy and Behav 32:114–120. https://doi.org/10.1016/j.yebeh.2014.01.010
Becker M, Sommer T, Kühn S (2020) Inferior frontal gyrus involvement during search and solution in verbal creative problem solving: a parametric fMRI study. Neuroimage. https://doi.org/10.1016/j.neuroimage.2019.116294
Bolgina T, Malyutina S, Zavyalova V, Ignatev G, Ushakov V, Akinina Y, Ivanova M, Dragoy O (2016) The paradigm of language lateralization in the brain: natural sciences method for linguistics. Russ Found Basic Res J 3(91):83–91
Bradshaw AR, Thompson PA, Wilson AC, Bishop DVM, Woodhead ZVJ (2017) Measuring language lateralisation with different language tasks: a systematic review. PeerJ. https://doi.org/10.7717/peerj.3929
Cappa SF, Sandrini M, Rossini PM, Sosta K, Miniussi C (2002) The role of the left frontal lobe in action naming rTMS evidence. Neurology 59(5):720–723. https://doi.org/10.1212/WNL.59.5.720
Carey DP, Johnstone LT (2014) Quantifying cerebral asymmetries for language in dextrals and adextrals with random-effects meta analysis. Front Psychol. https://doi.org/10.3389/fpsyg.2014.01128
Chang EF, Raygor KP, Berger MS (2015) Contemporary model of language organization: an overview for neurosurgeons. J Neurosurg 122(2):250–261. https://doi.org/10.3171/2014.10.JNS132647
Costafreda SG, Fu CHY, Lee L, Everitt B, Brammer MJ, David AS (2006) A systematic review and quantitative appraisal of fMRI studies of verbal fluency: role of the left inferior frontal gyrus. Hum Brain Mapp 27(10):799–810. https://doi.org/10.1002/hbm.20221
Damasio AR, Tranel D (1993) Nouns and verbs are retrieved with differently distributed neural systems. Proc Natl Acad Sci 90(11):4957–4960. https://doi.org/10.1073/pnas.90.11.4957
Daniele A, Giustolisi L, Silveri MC, Colosimo C, Gainotti G (1994) Evidence for a possible neuroanatomical basis for lexical processing of nouns and verbs. Neuropsychologia 32(11):1325–1341
Dragoy O, Chrabaszcz A, Tolkacheva V, Buklina S (2016) Russian intraoperative naming test: a standardized tool to map noun and verb production during awake neurosurgeries. Russ J Cogn Sci 3(4):4–25
Elin K, Malyutina S, Bronov O, Stupina E, Marinets A, Zhuravleva A, Dragoy O (2022) A new functional magnetic resonance imaging localizer for preoperative language mapping using a sentence completion task: validity, choice of baseline condition, and test-retest reliability. Front Hum Neurosci 16:791577. https://doi.org/10.3389/fnhum.2022.791577
Foltys H, Sparing R, Boroojerdi B, Krings T, Meister I, Mottaghy F (2001) Motor control in simple bimanual movements: a transcranial magnetic stimulation and reaction time study. Clin Neurophysiol 112(2):265–274
Hartwigsen G, Siebner HR (2012) Probing the involvement of the right hemisphere in language processing with online transcranial magnetic stimulation in healthy volunteers. Aphasiology 26(9):1131–1152. https://doi.org/10.1080/02687038.2011.590573
Hartwigsen G, Price CJ, Baumgaertner A, Geiss G, Koehnke M, Ulmer S, Siebner HR (2010) The right posterior inferior frontal gyrus contributes to phonological word decisions in the healthy brain: evidence from dual-site TMS. Neuropsychologia 48(10):3155–3163. https://doi.org/10.1016/j.neuropsychologia.2010.06.032
Havas V, Gabarrós A, Juncadella M, Rifa-Ros X, Plans G, Acebes JJ, RodríguezFornells A (2015) Electrical stimulation mapping of nouns and verbs in Broca’s area. Brain Lang 145:53–63
Hernandez-Pavon JC, Mäkelä N, Lehtinen H, Lioumis P, Mäkelä JP (2014) Effects of navigated TMS on object and action naming. Front Hum Neurosci. https://doi.org/10.3389/fnhum.2014.00660
Indefrey P (2011) The spatial and temporal signatures of word production components: a critical update. Front Psychol. https://doi.org/10.3389/fpsyg.2011.00255
JASP Team (2022). JASP (Version 0.16.3) [Computer software]
Josse G, Tzourio-Mazoyer N (2004) Hemispheric specialization for language. Brain Res Rev 44(1):1–12. https://doi.org/10.1016/j.brainresrev.2003.10.001
Jung J, Bungert A, Bowtell R, Jackson SR (2016) Vertex stimulation as a control site for transcranial magnetic stimulation: a concurrent TMS/fMRI study. Brain Stim 9(1):58–64
Kane SP(2018) Post. ClinCalc. https://clincalc.com/stats/Power.aspx https://clincalc.com/stats/Power.aspx. Updated November 10, 2018.
Klaus J, Schutter DJLG (2018) Non-invasive brain stimulation to investigate language production in healthy speakers: a meta-analysis. Brain Cogn 123:10–22. https://doi.org/10.1016/j.bandc.2018.02.007
Könönen M, Tamsi N, Säisänen L, Kemppainen S, Määttä S, Julkunen P, Jutila L, Äikiä M, Kälviäinen R, Niskanen E, Vanninen R, Karjalainen P, Mervaala E (2015) Non-invasive mapping of bilateral motor speech areas using navigated transcranial magnetic stimulation and functional magnetic resonance imaging. J Neurosci Methods 248:32–40. https://doi.org/10.1016/j.jneumeth.2015.03.030
Krieg SM, Sollmann N, Hauck T, Ille S, Foerschler A, Meyer B, Ringel F (2013) Functional language shift to the right hemisphere in patients with language-eloquent brain tumors. PLoS ONE. https://doi.org/10.1371/journal.pone.0075403
Krieg SM, Sollmann N, Tanigawa N, Foerschler A, Meyer B, Ringel F (2016) Cortical distribution of speech and language errors investigated by visual object naming and navigated transcranial magnetic stimulation. Brain Struct Func 221(4):2259–2286. https://doi.org/10.1007/s00429-015-1042-7
Krieg SM, Lioumis P, Mäkelä JP, Wilenius J, Karhu J, Hannula H, Savolainen P, Lucas CW, Seidel K, Laakso A, Islam M, Vaalto S, Lehtinen H, Vitikainen AM, Tarapore PE, Picht T (2017) Protocol for motor and language mapping by navigated TMS in patients and healthy volunteers; workshop report. Acta Neurochir 159(7):1187–1195. https://doi.org/10.1007/s00701-017-3187-z
Lehtinen H, Mäkelä JP, Mäkelä T, Lioumis P, Metsähonkala L, Hokkanen L, Wilenius J, Gaily E (2018) Language mapping with navigated transcranial magnetic stimulation in pediatric and adult patients undergoing epilepsy surgery: comparison with extraoperative direct cortical stimulation. Epilepsia Open 3(2):224–235. https://doi.org/10.1002/epi4.12110
Lubrano V, Filleron T, Démonet JF, Roux FE (2014) Anatomical correlates for category-specific naming of objects and actions: a brain stimulation mapping study. Hum Brain Map 35:429–433
Medina J, Norise C, Faseyitan O, Coslett HB, Turkeltaub PE, Hamilton RH (2012) Finding the right words: transcranial magnetic stimulation improves discourse productivity in non-fluent aphasia after stroke. Aphasiology 26(9):1153–1168. https://doi.org/10.1080/02687038.2012.710316
Naeser MA, Martin PI, Ho M, Treglia E, Kaplan E, Bashir S, Pascual-Leone A (2012) Transcranial magnetic stimulation and aphasia rehabilitation. Arch Phys Med Rehabil. https://doi.org/10.1016/j.apmr.2011.04.026
Nyffeler T, Wurtz P, Pflugshaupt T, von Wartburg R, Luthi M, Hess CW (2006) One-hertz transcranial magnetic stimulation over the frontal eye field induces lasting inhibition of saccade triggering. NeuroReport 17(3):273–275
Ojemann GA (1979) Individual variability in cortical localization of language. J Neurosurg 50(2):164–169. https://doi.org/10.3171/jns.1979.50.2.0164
Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113
Packheiser J, Schmitz J, Arning L, Beste C, Güntürkün O, Ocklenburg S (2020) A large-scale estimate on the relationship between language and motor lateralization. Sci Rep. https://doi.org/10.1038/s41598-020-70057-3
Pascual-Leone A, Valls-Sole J, Wassermann EM, Hallett M (1994) Responses to rapid-rate transcranial magnetic stimulation of the human motor cortex. Brain, 117. http://brain.oxfordjournals.org/
Petrovich Brennan NM, Whalen S, de Morales BD, O’Shea JP, Norton IH, Golby AJ (2007) Object naming is a more sensitive measure of speech localization than number counting: converging evidence from direct cortical stimulation and fMRI. Neuroimage. https://doi.org/10.1016/j.neuroimage.2007.04.052
Połczyńska M, Japardi K, Curtiss S, Moody T, Benjamin C, Cho A, Vigil C, Kuhn T, Jones M, Bookheimer S (2017) Improving language mapping in clinical fMRI through assessment of grammar. Neuroimage Clin 15:415–427. https://doi.org/10.1016/j.nicl.2017.05.021
Price CJ (2012) A review and synthesis of the first 20 years of PET and fMRI studies of heard speech spoken language and reading. NeuroImage 62(2):816–847. https://doi.org/10.1016/j.neuroimage.2012.04.062
Rofes A, Miceli G (2014) Language mapping with verbs and sentences in awake surgery: a review. Neuropsychol Rev 24:185–199
Rofes A, Spena G, Talacchi A, Santini B, Miozzo A, Miceli G (2017) Mapping nouns and finite verbs in left hemisphere tumors: a direct electrical stimulation study. Neurocase 23(2):105–113
Romei V, Murray MM, Merabet LB, Thut G (2007) Occipital transcranial magnetic stimulation has opposing effects on visual and auditory stimulus detection: implications for multisensory interactions. J Neurosci 27(43):11465–11472
Rösler J, Niraula B, Strack V, Zdunczyk A, Schilt S, Savolainen P, Lioumis P, Mäkelä J, Vajkoczy P, Frey D, Picht T (2014) Language mapping in healthy volunteers and brain tumor patients with a novel navigated TMS system: evidence of tumor-induced plasticity. Clin Neurophysiol 125(3):526–536. https://doi.org/10.1016/j.clinph.2013.08.015
Rossini PM, Burke D, Chen R, Cohen LG, Daskalakis Z, di Iorio R, di Lazzaro V, Ferreri F, Fitzgerald PB, George MS, Hallett M, Lefaucheur JP, Langguth B, Matsumoto H, Miniussi C, Nitsche MA, Pascual-Leone A, Paulus W, Rossi S, Ziemann U (2015) 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 IFCN committee. Clin Neurophysiol 126(6):1071–1107. https://doi.org/10.1016/j.clinph.2015.02.001
Rouder N, Morey D, Speckman L, Province JM (2012) Default bayes factors for ANOVA designs. J Math Psychol 56(5):356–374
Sakreida K, Blume-Schnitzler J, Frankemölle G, Drews V, Heim S, Willmes K, Clusmann H, Neuloh G (2020) Hemispheric dominance for language and side effects in mapping the inferior frontal junction area with transcranial magnetic stimulation. J Neurol Surg A Cent Eur Neurosurg 81(2):130–137. https://doi.org/10.1055/s-0040-1701236
Schneider W, Eschman A, Zuccolotto A (2002) E-Prime: User’s guide. Reference guide. Getting started guide. Psychology Software Tools, Incorporated
Silvanto J, Cattaneo Z, Battelli L, Pascual-Leone A (2008) Baseline cortical excitability determines whether TMS disrupts or facilitates behavior. J Neurophysiol 99(5):2725–2730
Sollmann N, Tanigawa N, Ringel F, Zimmer C, Meyer B, Krieg SM (2014) Language and its right-hemispheric distribution in healthy brains: an investigation by repetitive transcranial magnetic stimulation. Neuroimage 102:776–788. https://doi.org/10.1016/j.neuroimage.2014.09.002
Sollmann N, Ille S, Obermueller T, Negwer C, Ringel F, Meyer B, Krieg SM (2015) The impact of repetitive navigated transcranial magnetic stimulation coil positioning and stimulation parameters on human language function. Eur J Med Res 20(1):1–10. https://doi.org/10.1186/s40001-015-0138-0
Sollmann N, Ille S, Boeckh-Behrens T, Ringel F, Meyer B, Krieg SM (2016) Mapping of cortical language function by functional magnetic resonance imaging and repetitive navigated transcranial magnetic stimulation in 40 healthy subjects. Acta Neurochir 158(7):1303–1316. https://doi.org/10.1007/s00701-016-2819-z
Sollmann N, Fuss-Ruppenthal S, Zimmer C, Meyer B, Krieg SM (2018) Investigating stimulation protocols for language mapping by repetitive navigated transcranial magnetic stimulation. Front Behav Neurosci. https://doi.org/10.3389/fnbeh.2018.00197
Somers M, Aukes MF, Ophoff RA, Boks MP, Fleer W, de Visser KCL, Kahn RS, Sommer IE (2015) On the relationship between degree of hand-preference and degree of language lateralization. Brain Lang 144:10–15. https://doi.org/10.1016/j.bandl.2015.03.006
Springer JA, Jeffrey RB, Thomas AH, Sara JS, Julie AF, Patrick SFB, Cameron CB, Holly MP, George LM, Wade MM (1999) Language dominance in neurologically normal and epilepsy subjects. Brain 122(11):2033–2046. https://doi.org/10.1093/brain/122.11.2033
Szaflarski J, Binder J, Possing E, McKiernan K, Ward B, Hammeke T, Possing E (2001) Language lateralization in left-handed and ambidextrous people fMRI data. http://afni.nimh.
Tarapore PE (2014) Speech mapping with transcranial magnetic stimulation. Neuromethod 89:361–379. https://doi.org/10.1007/978-1-4939-0879-0_17
Tomasino B, Fink GR, Sparing R, Dafotakis M, Weiss PH (2008) Action verbs and the primary motor cortex: a comparative TMS study of silent reading, frequency judgments, and motor imagery. Neuropsychologia 46(7):1915–1926
Tussis L, Sollmann N, Boeckh-Behrens T, Meyer B, Krieg SM (2016) Language function distribution in left-handers: a navigated transcranial magnetic stimulation study. Neuropsychologia 82:65–73. https://doi.org/10.1016/j.neuropsychologia.2016.01.010
Unadkat P, Fumagalli L, Rigolo L, Vangel MG, Young GS, Huang R, Mukundan S, Golby A, Tie Y (2019) Functional MRI task comparison for language mapping in neurosurgical patients. J Neuroimaging 29(3):348–356. https://doi.org/10.1111/jon.12597
van den Bergh D, Van Doorn J, Marsman M, Draws T, Van Kesteren EJ, Derks K, Wagenmakers EJ (2020) A tutorial on conducting and interpreting a Bayesian ANOVA in JASP. Lannee Psychologique 120(1):73–96
van Oers CAMM, Vink M, van Zandvoort MJE, van der Worp HB, de Haan EHF, Kappelle LJ, Ramsey NF, Dijkhuizen RM (2010) Contribution of the left and right inferior frontal gyrus in recovery from aphasia. A functional MRI study in stroke patients with preserved hemodynamic responsiveness. Neuroimage 49(1):885–893. https://doi.org/10.1016/j.neuroimage.2009.08.057
Vigliocco G, Vinson DP, Druks J, Barber H, Cappa SF (2011) Nouns and verbs in the brain: a review of behavioural, electrophysiological, neuropsychological and imaging studies. Neurosci Biobehav Rev 35(3):407–426. https://doi.org/10.1016/j.neubiorev.2010.04.007
Wang J, Yang Y, Zhao X, Zuo Z, Tan LH (2020) Evolutional and developmental anatomical architecture of the left inferior frontal gyrus. Neuroimage. https://doi.org/10.1016/j.neuroimage.2020.117268
Wilke M, Lidzba K (2007) LI-tool: a new toolbox to assess lateralization in functional MR-data. J Neurosci Method 163(1):128–136. https://doi.org/10.1016/j.jneumeth.2007.01.026
Wilson SM, Bautista A, Yen M, Lauderdale S, Eriksson DK (2017) Validity and reliability of four language mapping paradigms. Neuroimage Clin 16:399–408. https://doi.org/10.1016/j.nicl.2016.03.015
Acknowledgements
We thank Irina Sekerina for her valuable text revisions and the participants of the present and related studies, who visited the lab multiple times. This work has been carried out using HSE unique equipment (Reg. num 354937).
Funding
The article was prepared in the framework of a research grant funded by the Ministry of Science and Higher Education of the Russian Federation (grant ID: 075–15-2022–325).
Author information
Authors and Affiliations
Contributions
TB: formal analysis, methodology, investigation, project administration, writing the original draft; VS: investigation, software, validation; SFC: conceptualization, writing—review & editing; ZC: investigation, software, validation; MF: conceptualization, methodology, formal analysis, writing—review & editing; SM: investigation, methodology, writing—review & editing; AS: investigation; YS: conceptualization; OD: conceptualization, formal analysis, investigation, project administration, resources, writing—review & editing.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no competing interests.
Ethical approval
Our experimental standards and all procedures performed in this study involving human participants were in accordance with the Code of Ethics of the World Medical Association (Declaration of Helsinki), as published in the British Medical Journal in 1964, and its later amendments or comparable ethical standards and were approved by the local ethics committee of the Medical Faculty of RWTH Aachen University [EK 054/13]. Prior to investigation, we obtained written informed consent from all our volunteers.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Bolgina, T., Somashekarappa, V., Cappa, S.F. et al. Repetitive transcranial magnetic stimulation modulates action naming over the left but not right inferior frontal gyrus. Brain Struct Funct 227, 2797–2808 (2022). https://doi.org/10.1007/s00429-022-02574-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00429-022-02574-y