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Cortical time course of object naming investigated by repetitive navigated transcranial magnetic stimulation

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Abstract

Human language organization models and language time course patterns are still predominantly derived from meta-analyses of numerous single publications, which only investigated scattered cortical regions. Moreover, there is not much literature available on the exact impact of repetitive navigated transcranial magnetic stimulation (rTMS) onset times on object naming. We, therefore, used a virtual lesion-based approach by mapping various cortical areas with rTMS to investigate the time course of object naming, and to specifically provide data on the pattern of rTMS language mapping results depending on different stimulation onset times. Ten healthy, right-handed subjects were enrolled, and rTMS in combination with an object-naming task was performed with different stimulation onset times (0 ms, 100 ms, 200 ms, 300 ms, 400 ms, and 500 ms). Subsequent to language mapping, all naming errors detected were systematically classified with respect to previous literature. The majority of errors was elicited within the opercular inferior frontal gyrus (opIFG) and ventral precentral gyrus (vPrG), and the spatial distribution of naming errors changed according to the time point of naming disruption by varying onset times. For instance, immediate rTMS onset led to a widespread cortical distribution of no responses, whereas performance and hesitation errors increased with higher stimulation onset times.

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Abbreviations

anG:

Angular gyrus

ANOVA:

Analysis of variance

ap:

Anterior-posterior

aSMG:

Anterior supramarginal gyrus

CI:

Confidence interval

CPS:

Cortical parcellation system

DCS:

Direct cortical stimulation

DT:

Display time

EEG:

Electroencephalography

EHI:

Edinburgh Handedness Inventory

fMRI:

Functional magnetic resonance imaging

IPI:

Inter-picture-interval

MEG:

Magnetoencephalography

mMTG:

Middle middle temporal gyrus

MRI:

Magnetic resonance imaging

mSTG:

Middle superior temporal gyrus

MTG:

Middle temporal gyrus

opIFG:

Opercular inferior frontal gyrus

pMFG:

Posterior middle frontal gyrus

pMTG:

Posterior middle temporal gyrus

PPV:

Positive predictive value

pSFG:

Posterior superior frontal gyrus

pSMG:

Posterior supramarginal gyrus

pSTG:

Posterior superior temporal gyrus

PTI:

Picture-to-trigger interval

RMT:

Resting motor threshold

RT:

Reaction time

rTMS:

Repetitive navigated transcranial magnetic stimulation

SD:

Standard deviation

TMS:

Transcranial magnetic stimulation

VAS:

Visual analogue scale

vPoG:

Ventral post-central gyrus

vPrG:

Ventral pre-central gyrus

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Acknowledgments

The first author gratefully acknowledges the support of the Graduate School’s Faculty Graduate Center of our university. Furthermore, we would like to thank Mrs. Noriko Tanigawa for her support during analysis of video data.

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Authors and Affiliations

  1. Department of Neurosurgery, Klinikum rechts der Isar, Technische Universität München, Ismaninger Str. 22, 81675, Munich, Germany

    Nico Sollmann, Sebastian Ille, Chiara Negwer, Florian Ringel, Bernhard Meyer & Sandro M. Krieg

  2. TUM-Neuroimaging Center, Technische Universität München, Ismaninger Str. 22, 81675, Munich, Germany

    Nico Sollmann, Sebastian Ille, Chiara Negwer & Sandro M. Krieg

  3. Department of Radiology, Section of Neuroradiology, Klinikum rechts der Isar, Technische Universität München, Ismaninger Str. 22, 81675, Munich, Germany

    Nico Sollmann & Tobias Boeckh-Behrens

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  1. Nico Sollmann
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  2. Sebastian Ille
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  3. Chiara Negwer
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  4. Tobias Boeckh-Behrens
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  5. Florian Ringel
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  7. Sandro M. Krieg
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Corresponding author

Correspondence to Sandro M. Krieg.

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Funding

The study was primarily financed by institutional grants from the Department of Neurosurgery and the Section of Neuroradiology.

Conflict of interest

FR and SK are consultants for BrainLab AG (Feldkirchen, Germany). SK is consultant for Nexstim Oy (Helsinki, Finland). The authors declare that they have no conflict of interest.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Informed consent

Informed consent was obtained from all individual participants included in the study.

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Ethics Committee Registration Number: 222/14

Electronic supplementary material

Supplementary Figure 1

All errors. This figure shows the region-specific number of all errors, the number of stimulations, and the corresponding error rates (in %) for rTMS applied with a PTI of 0 ms (a), 100 ms (b), 200 ms (c), 300 ms (d), 400 ms (e), and 500 ms (f). (GIF 156 kb)

High Resolution Image (TIFF 4644 kb)

Supplementary Figure 2

All errors without hesitations. This graph provides information about the region-specific number of all errors except hesitations, the number of stimulations, and the corresponding error rates (in %) for rTMS applied with a PTI of 0 ms (a), 100 ms (b), 200 ms (c), 300 ms (d), 400 ms (e), and 500 ms (f). (GIF 155 kb)

High Resolution Image (TIFF 4432 kb)

Supplementary Figure 3

No responses. The number of no responses, the number of stimulations, and the corresponding no-response error rates (in %) for rTMS applied with a PTI of 0 ms (a), 100 ms (b), 200 ms (c), 300 ms (d), 400 ms (e), and 500 ms (f) are illustrated in this figure. (GIF 151 kb)

High Resolution Image (TIFF 4387 kb)

Supplementary Figure 4

Performance errors. This scheme visualizes the number of performance errors, the number of stimulations, and the corresponding performance error rates (in %) per region for rTMS applied with a PTI of 0 ms (a), 100 ms (b), 200 ms (c), 300 ms (d), 400 ms (e), and 500 ms (f). (GIF 149 kb)

High Resolution Image (TIFF 4305 kb)

Supplementary Figure 5

Hesitations. This graph provides information about the region-specific number of hesitations, the number of stimulations, and the corresponding hesitation error rates (in %) for rTMS applied with a PTI of 0 ms (a), 100 ms (b), 200 ms (c), 300 ms (d), 400 ms (e), and 500 ms (f). (GIF 156 kb)

High Resolution Image (TIFF 4495 kb)

Supplementary Table 1

Distribution of naming errors. Summary of naming errors induced by rTMS per region and picture-to-trigger interval (PTI). In detail, the table shows the total number of trials (which equals the number of rTMS trains), the total number of errors, and the corresponding error rates and ratios for each error type. The category “other” includes neologisms, semantic errors, and phonological errors, which only occurred infrequently. (DOC 185 kb)

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Sollmann, N., Ille, S., Negwer, C. et al. Cortical time course of object naming investigated by repetitive navigated transcranial magnetic stimulation. Brain Imaging and Behavior 11, 1192–1206 (2017). https://doi.org/10.1007/s11682-016-9574-x

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