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Cortical Inhibition of Face and Jaw Muscle Activity and Discomfort Induced by Repetitive and Paired-Pulse TMS During an Overt Object Naming Task

  • Carolin Weiss LucasEmail author
  • Elisa Kallioniemi
  • Volker Neuschmelting
  • Charlotte Nettekoven
  • Julia Pieczewski
  • Kristina Jonas
  • Roland Goldbrunner
  • Jari Karhu
  • Christian Grefkes
  • Petro Julkunen
Original Paper

Abstract

Modulatory effects of transcranial magnetic stimulation (TMS) strongly depend on the stimulation parameters. Here, we compared the immediate, task-locked inhibitory effects on speech-related muscles and the tolerability of different TMS protocols during a language production task. Repetitive TMS (rTMS) and paired-pulse TMS (PP) were applied in 13 healthy subjects over the primary motor cortex (M1) during a finger-tapping/tongue-twisting tasks. The lowest subject-specific TMS intensity leading to movement disruptions was used for TMS over left-sided speech-related areas during picture naming. Here, time-locked PP and rTMS (10/30/50 Hz; randomized sequence) were applied. Cortical silent periods (cSPs) were analyzed from electromyography obtained from various face muscles. 30 Hz- and 50 Hz-rTMS reliably evoked tongue movement disruption (ICC = 0.65) at lower rTMS intensities compared to 10 Hz-rTMS or PP. CSPs were elicited from the left hemisphere by all TMS protocols, most reliably by PP (p < 0.001). Also, cSPs with longest durations were induced by PP. Exploratory analyses of PP suggest that the trials with strongest motor inhibitory effects (presence of cSP) were associated with more articulatory naming errors, hence hinting at the utility of TMS-elicited, facial cSP for mapping of language production areas. Higher-frequency rTMS and PP evoked stronger inhibitory effects as compared to 10 Hz-rTMS during a language task, thus enabling a probably more efficient and tolerable routine for language mapping. The spatial distribution of cranial muscle cSPs implies that TMS might affect not only M1, but also distant parts of the language network.

Keywords

rTMS cSP Tolerability Tongue Language Inhibition 

Abbreviations

APB

Abductor pollicis brevis muscle

aILT

Inferior longitudinal tongue muscle; anterior third

cSP

Cortical silent period

FDR

False discovery rate

E-field

Electric field

EMG

Electromyography

ICC

Intraclass correlation coefficient

ISI

Interstimulus interval

M1

Primary motor cortex

MEP

Motor-evoked potential

MIT

Motor inhibition threshold

MSO

Maximum stimulator output

NRS

Numeric rating scale (0–10; for pain assessment)

nTMS

Neuronavigated transcranial magnetic stimulation

PP

Paired-pulse TMS

RMT

Resting motor threshold

rTMS

Repetitive transcranial magnetic stimulation

SEM

Standard error of the mean

TMS

Transcranial magnetic stimulation

Notes

Acknowledgements

The navigated TMS system used in the study was funded by the German Research Foundation (DFG, INST 1850/50-1). Author CWL received funding from the University of Cologne, Faculty of Medicine (Grant: Gerok 8/2016). The study received funding from the State Research Funding granted for the Kuopio University Hospital Catchment Area (project 5041730, Kuopio, Finland). In addition, author EK was funded by the Kaute Foundation, Helsinki, Finland, The Paulo Foundation, Helsinki, Finland, and The Finnish Concordia Fund, Helsinki, Finland.

Compliance with Ethical Standards

Disclosure of Potential Conflicts of interest

Petro Julkunen has received unrelated consulting pay from Nexstim Plc., manufacturer of the nTMS device. Jari Karhu is employed part-time by Nexstim Plc., manufacturer of the nTMS device and holds shares of the company but was not involved in data acquisition, processing or analysis.

Research Involving Human Participants and/or Animals

The research involved voluntary human participants who received a minor financial compensation for participating in the study. The study was approved by the local Ethics Committee. All procedures were performed in accordance with the ethical standards of the institutional committee and have been performed in accordance with the ethical standards as laid down in the 1964 Declaration of Helsinki and its later amendments.

Informed Consent

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

Supplementary material

10548_2019_698_MOESM1_ESM.tif (48.5 mb)
Supplementary Figure S1. Amounts of cSPs induced by different rTMS protocols in three sessions. Average cSP amounts of all muscle recordings, all participants and all three sessions (data set A), grouped by rTMS frequency, are displayed. Mean and inter-individual variability are expressed as standard error of the mean (SEM). Significant differences between frequencies are indicated with an asterisk (*pEMM &#x003C; 0.05, FDR-corrected). (TIF 49668 KB)
10548_2019_698_MOESM2_ESM.tif (28.3 mb)
Supplementary Figure S2. Latencies of cSPs elicited by different rTMS protocols and PP in the distinct muscles. Mean and inter-individual variability are expressed as standard error of the mean (SEM) for all muscles (data set B). Missing values were not included. (L = left, R = right; (i) = ipsilateral). (TIF 28954 KB)
10548_2019_698_MOESM3_ESM.tif (28.5 mb)
Supplementary Figure S3. Durations of cSPs elicited by different TMS protocols and in the distinct evaluated muscles. Missing values were not included in the data set. (L = left, R = right; (i) = ipsilateral). (TIF 29165 KB)

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Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Carolin Weiss Lucas
    • 1
    Email author
  • Elisa Kallioniemi
    • 2
    • 3
  • Volker Neuschmelting
    • 1
  • Charlotte Nettekoven
    • 1
  • Julia Pieczewski
    • 1
  • Kristina Jonas
    • 5
  • Roland Goldbrunner
    • 1
  • Jari Karhu
    • 4
  • Christian Grefkes
    • 6
    • 7
  • Petro Julkunen
    • 2
    • 8
  1. 1.Faculty of Medicine and University Hospital Cologne, Center of NeurosurgeryUniversity of CologneCologneGermany
  2. 2.Department of Clinical NeurophysiologyKuopio University HospitalKuopioFinland
  3. 3.Department of PsychiatryUT Southwestern Medical CenterDallasUSA
  4. 4.Nexstim PlcHelsinkiFinland
  5. 5.Department of Special Education and Rehabilitation, Faculty of Human SciencesUniversity of CologneCologneGermany
  6. 6.Institute of Neuroscience and Medicine (INM-3)Research Centre JülichJuelichGermany
  7. 7.Faculty of Medicine and University Hospital Cologne, Department of NeurologyUniversity of CologneCologneGermany
  8. 8.Department of Applied PhysicsUniversity of Eastern FinlandKuopioFinland

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