Acute modulation of cortical oscillatory activities during short trains of high-frequency repetitive transcranial magnetic stimulation of the human motor cortex: a combined EEG and TMS study

Abstract

In this study, a combined repetitive transcranial magnetic stimulation/electroencephalography (rTMS/EEG) method was used to explore the acute changes of cortical oscillatory activity induced by intermittent short trains of high-frequency (5-Hz) rTMS delivered over the left primary motor cortex (M1). We evaluated the electrophysiological reaction to magnetic stimulation during and 2-4 s after 20 trains of 20-pulses rTMS, using event-related power (ERPow) that reflects the regional oscillatory activity of neural assemblies, and event-related coherence (ERCoh) that reflects the interregional functional connectivity of oscillatory neural activity. These event-related transformations were for the upper alpha (10-12 Hz) and beta (18-22 Hz) frequency ranges, respectively. For the alpha band, threshold rTMS and subthreshold rTMS induced an ERPow increase during the trains of stimulation mainly in frontal and central regions ipsilateral to stimulation. For the beta band, a similar synchronization of cortical oscillations for both rTMS intensities was seen. Moreover, subthreshold rTMS affected alpha-band activity more than threshold rTMS, inducing a specific ERCoh decrease over the posterior regions during the trains of stimulation. For beta band, the decrease in functional coupling was observed mainly during threshold rTMS. These findings provide a better understanding of the cortical effects of high-frequency rTMS, whereby the induction of oscillations reflects the capacity of electromagnetic pulses to alter regional and interregional synaptic transmissions of neural populations.

Figure 1

Experimental design: the study design consisted of four experimental conditions (rTMS 80%, rTMS 100%, Sham rTMS, and Repetitive peripheral electric stimulation, respectively) that comprised four blocks of epochs of EEG and EMG measurements recorded continuously immediately before, during, and immediately after repetitive 5‐Hz stimulation (Pre, rTMS, Post, respectively). The order execution of four conditions was counterbalanced among individuals.

Figure 2

Electrode montage and placement according to the 10/20 system with additional electrodes for a total of 30. The filled circles indicate the nine electrodes of interest on which the EEG signal and statistical analyses of event‐related power and event‐related coherence transformations were based.

Figure 3

Raw data showing EEG and EMG recording of a subject in which rTMS pulses were delivered to left M1 at 80% RMT. Panel A represents 3 s of recorded raw data. Panel B shows 0.5 s of recorded raw data. We analyzed the EEG signal starting 30 ms from each pulse during rTMS trains.

Figure 4

Grand average of event‐related power transformation for upper α (10–12 Hz) band of nine electrodes analyzed, as a function of the experimental condition and epoch of time (n = 11). Repetitive TMS at 100% RMT induced an increase in amplitude in EEG oscillations mainly for F3 electrode compared with C4 electrode. At epoch 1, during the trains of stimulation, there was an increase in power for F3, Fz, and F4 frontal electrodes compared with the second epoch after each train of repetitive stimulation. [Color figure can be viewed in the online issue, which is available at www.interscience.wiley.com.]

Figure 5

Grand average of event‐related power transformation for β (18–22 Hz) band of nine electrodes analyzed, as a function of the experimental condition and epoch of time (n = 11). The F3, C3, and P4 were the most sensitive electrode to experimental manipulations. At epoch 1, during repetitive stimulation, for the C3 electrode there was a significant increase in amplitude of EEG oscillations with rTMS at 100% RMT compared with repetitive peripheral electric stimulation. [Color figure can be viewed in the online issue, which is available at www.interscience.wiley.com.]

Figure 6

Grand average of event‐related coherence transformation for upper α (10–12 Hz) band of nine electrodes analyzed referenced to C3 electrode, as a function of the experimental condition and epoch of time (n = 11). At epoch 1, during the trains of stimulation, subthreshold more than threshold rTMS produced a significant decrease in functional coupling in the posterior P3‐C3 pair of electrodes in contrast with the absence of increase in connectivity for both control conditions of sham rTMS and repetitive peripheral electrical stimulation. [Color figure can be viewed in the online issue, which is available at www.interscience.wiley.com.]

Figure 7

Grand average of event‐related coherence transformation for β (18–22 Hz) band of nine electrodes analyzed referenced to C3 electrode, as a function of the experimental condition and epoch of time (n = 11). During each train of repetitive stimulation rTMS 100% RMT induced a significant decrease of functional coupling mainly for the posterior P3‐C3 electrodes pair compared with F3‐C3, and Fz‐C3 frontal couple of electrodes. [Color figure can be viewed in the online issue, which is available at www.interscience.wiley.com.]