Intermittent Theta Burst Stimulation to the Primary Motor Cortex Reduces Cortical Inhibition: A TMS-EEG Study

Abstract

Introduction: The aim of this study was to reveal the effects of intermittent theta burst stimulation (iTBS) in modulating cortical networks using transcranial magnetic stimulation and electroencephalography (TMS-EEG) recording.

Methods: Eighteen young adults participated in our study and received iTBS to the primary motor cortex (M1), supplementary motor area, and the primary visual cortex in three separate sessions. A finger tapping task and ipsilateral single-pulse TMS-EEG recording for the M1 were administrated before and after iTBS in each session. The effects of iTBS in motor performance and TMS-evoked potentials (TEPs) were investigated.

Results: The results showed that iTBS to the M1, but not supplementary motor area or the primary visual cortex, significantly reduced the N100 amplitude of M1 TEPs in bilateral hemispheres (p = 0.019), with a more prominent effect in the contralateral hemisphere than in the stimulated hemisphere. Moreover, only iTBS to the M1 decreased global mean field power (corrected ps < 0.05), interhemispheric signal propagation (t = 2.53, p = 0.030), and TMS-induced early α-band synchronization (p = 0.020).

Conclusion: Our study confirmed the local and remote after-effects of iTBS in reducing cortical inhibition in the M1. TMS-induced oscillations after iTBS for changed cortical excitability in patients with various neurological and psychiatric conditions are worth further exploration.

Keywords: TMS-evoked potentials; cortical inhibition; primary motor cortex; transcranial magnetic stimulation.

Figure 1

Experimental procedures and the finger tapping task. (a) TMS-EEG recording of 90 single-pulse of SMA and V1. Resting motor threshold was determined in the first session only and the stimulation intensity was maintained the same for the conditions that followed. (b) Illustration of the finger tapping task (only the left hand is shown). FTT: finger tapping task; RMT: resting motor threshold; TMS-EEG: transcranial magnetic stimulation and electroencephalography; iTBS: intermittent theta burst stimulation; M1: primary motor cortex; SMA: supplementary motor area; V1: primary visual cortex.

Figure 2

The effect of iTBS in TMS-evoked potentials. (a) Only pre-iTBS data of the M1 condition are presented. “x” indicates the stimulation site. (b) TEP difference of a representative electrode (FC1). The grey shadows indicate the predefined time windows of five peaks and the green shadow indicates the significant difference in the N100 of M1 TEPs. Topographical plots are the difference of N100 amplitudes ($$\mathrm{post}-\mathrm{pre}$$) and “*” represents electrodes with a significant difference. (c) “*” represents electrodes with a significant difference induced by iTBS to the M1 in four small time windows of N100. (d) The global mean field power pre- and post-iTBS. Green shadows indicate a significant difference identified by paired t-tests and the blue shadows indicate comparisons survived after FDR corrections were applied. TEPs: TMS-evoked potentials; iTBS: intermittent theta burst stimulation; M1: primary motor cortex; SMA: supplementary motor area; V1: primary visual cortex; GMFP: global mean field power.

Figure 3

Results of the finger tapping task. (a,b) Accuracy rates of the left and right hands; (c,d) reaction time of left and right hands in milliseconds. (e,f) Comparisons of normalized reaction time. Error bars are standard diversions. L: left; R: right; ACC: accuracy rate; RT: reaction time; M1: primary motor cortex; SMA: supplementary motor area; V1: primary visual cortex.

Figure 4

The effects on TMS-induced interhemispheric signal propagation. (a) The difference in TMS-induced interhemispheric signal propagation pre- and post-iTBS to the three brain regions. (b) Comparisons of the change of ISP among the three conditions. Error bars are standard diversions. ISP: interhemispheric signal propagation; M1: primary motor cortex; SMA: supplementary motor area; V1: primary visual cortex.

Figure 5

The effect of iTBS in TMS-induced oscillations. The power of each frequency was normalized by dividing all time bins by the mean of baseline power (−650 to −350 ms), and an absolute baseline correction was also carried out. (a) Only pre-iTBS data of the M1 condition are presented. (b) Topographical plots are the difference of early (30–200 ms) and late (200–400 ms) oscillations. (c) The red rectangle indicates significantly decreased TMS-induced early α-band oscillation. “*” represents electrodes with a significant difference. TMS: transcranial magnetic stimulation; iTBS: intermittent theta burst stimulation; M1: primary motor cortex; SMA: supplementary motor area; V1: primary visual cortex.

Figure 6

Relationship between the N100 amplitude of M1 TEPs and TMS-induced oscillations. (a–c) Correlation coefficients between the N100 amplitude of M1 TEPs and TMS-induced early θ-, α-, and β-band synchronization. “*” represents electrodes with significant correlation. (d) Scatter plots of the relationship between oscillations and the N100 amplitude of a representative electrode (Cz). TMS: transcranial magnetic stimulation.