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Cortical distribution of speech and language errors investigated by visual object naming and navigated transcranial magnetic stimulation

Abstract

Navigated transcranial magnetic stimulation (nTMS) gains increasing importance in presurgical language mapping. Although bipolar direct cortical stimulation (DCS) is regarded as the gold standard for intraoperative mapping of language-related areas, it cannot be used to map the healthy human brain due to its invasive character. Therefore, the present study employed a non-invasive virtual-lesion modality to provide a causality-confirmed cortical language map of the healthy human brain by repetitive nTMS (rTMS) with functional specifications beyond language-positive/language-negative distinction. Fifty right-handed healthy volunteers underwent rTMS language mapping of the left hemisphere combined with an object-naming task. The induced errors were categorized and frequency maps were calculated. Moreover, a principal component analysis (PCA) was performed on the basis of language-positive cortical regions for each error category. The left hemisphere was stimulated at 258–789 sites (median: 361.5 sites), and 12–241 naming errors (median: 72.5 errors) were observed. In male subjects, a total number of 2091 language errors were elicited by 9579 stimulation trains, which is equal to an error rate of 21.8 %. Within females, 10,238 stimulation trains elicited 2032 language errors (19.8 %). PCA revealed that the inferior parietal lobe (IPL) and middle frontal gyrus (MFG) were causally involved in object naming as a semantic center and an executive control center. For the first time, this study provides causality-based data and a model that approximates the distribution of language-related cortical areas grouped for different functional aspects of single-word production processes by PCA.

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Abbreviations

APB:

Abductor pollicis brevis muscle

CPS:

Cortical parcellation system

DCS:

Bipolar direct cortical stimulation

ECoG:

Electrocorticography

fMRI:

Functional magnetic resonance imaging

IPI:

Inter-picture interval

IPL:

Inferior parietal lobe

ITG:

Inferior temporal gyrus

IPNP:

International Picture Naming Project

MEG:

Magnetoencephalography

MEP:

Motor evoked potential

MFG:

Middle frontal gyrus

MRI:

Magnetic resonance imaging

MTG:

Middle temporal gyrus

NPV:

Negative predictive value

nTMS:

Navigated transcranial magnetic stimulation

PC:

Principal component

PCA:

Principal component analysis

PPV:

Positive predictive value

RMT:

Resting motor threshold

rTMS:

Repetitive navigated transcranial magnetic stimulation

SD:

Standard deviation

SMG:

Supramarginal gyrus

STG:

Superior temporal gyrus

TMS:

Transcranial magnetic stimulation

VAS:

Visual analog scale

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Acknowledgments

We want to thank Maria Becker for performing this high amount of required MRI studies perfectly in addition to her daily routine. The study was primarily financed by institutional grants from the Department of Neurosurgery and the Section of Neuroradiology, TU Munich. Moreover, SK received a grant of the “Stiftung Neurochirurgische Forschung” of the German Neurosurgical Society (DGNC).

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical standard

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.

Author information

Correspondence to Sandro M. Krieg.

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Krieg, S.M., Sollmann, N., Tanigawa, N. et al. Cortical distribution of speech and language errors investigated by visual object naming and navigated transcranial magnetic stimulation. Brain Struct Funct 221, 2259–2286 (2016). https://doi.org/10.1007/s00429-015-1042-7

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Keywords

  • Cortical mapping
  • Language
  • Navigated brain stimulation
  • Object naming
  • Transcranial magnetic stimulation