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Department of Physical Therapy, Niigata University of Health and Welfare, 1398 Shimami-cho, Kita-ku, Niigata-shi, Niigata, 950-3198, Japan
Institute for Human Movement and Medical Sciences, Niigata University of Health and Welfare, 1398 Shimami-cho, Kita-ku, Niigata-shi, Niigata, 950-3198, Japan
Movement-related cortical potential (MRCP), a slow negative electroencephalographic (EEG) activity originated in the supplementary and primary motor areas (SMA and M1) [
], precedes self-initiated movements by one to 2 seconds. A short-lasting change of EEG power (event-related desynchronization/synchronization, ERD/S) also begins prior to self-initiated movements. In scalp EEG, ERD in the upper alpha or the lower beta band begins approximately 2 seconds before the self-initiated movements over the contralateral central region [
]. In electrocorticography, ERS in the high gamma band (75–100 Hz) begins before the self-initiated movements over the contralateral M1, and its distribution is more discrete and somatotopically specific than alpha and beta ERD [
]. Although MRCP and ERD/S can be a neural marker of volition and used to decode brain activity in brain-machine interfaces, the causal link between the M1 signals and the voluntary movement initiations remains unresolved [
] delivered over the left M1 (Fig. 1A) on a self-paced abduction movement of the right index finger. In the VS-tACS, we used 0.125 Hz frequency stimulation to induce a slow build-up of electrical potential similar to MRCP. In the AM-tACS, we used an amplitude modulated wave consisting of 90 Hz carrier and 0.25 Hz amplitude modulation. Its envelope was identical with the slow-wave used in the VS-tACS. The rising and falling amplitudes of the carrier signal were assumed to be similar to patterns of ERS and ERD in the high gamma band (90 Hz), respectively.
Fig. 1Stimulation waveforms, timing of movement initiation, and averaged stimulation
(A) The waveforms of VS-tACS and AM-tACS (Astim = 1 in Supplementary Methods) are shown in red and blue respectively. Note that VS-tACS is the envelope of AM-tACS. One cycle of VS-tACS is 8 seconds, and that of AM-tACS is 4 seconds. (B) The distribution of intervals between finger movements in VS-tACS (left) and AM-tACS (right). Both of them showed a rightward skew. (C) The distribution of movement initiation in reference to the phase of stimulation in VS-tACS (left) and AM-tACS (right). The distribution of movement initiation was significantly departed from uniformity (p = 0.027) in VS-tACS. (D) The averaged VS-tACS (top) showed a gradually rising waveform preceding the EMG onset (t = 0, bottom). The 95% CI of the resampled waveform and the mean of that are shown in dashed lines and dotted line respectively (top). . (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)
Details of the experimental methods are described in Supplementary Methods.
2. Results
When pooled across all participants (n = 16), the distribution of intervals between finger movements in both VS-tACS and AM-tACS showed a rightward skew (Fig. 1B), which was commonly observed in previous voluntary action studies. The intervals between finger movements were 12.0 ± 5.9 seconds in VS-tACS and 11.6 ± 6.2 seconds in AM-tACS. They were not significantly different (t-test, p = 0.253). Chi-square test demonstrated that the distribution of movement initiation was significantly departed from uniformity (p = 0.027) in VS-tACS (Fig. 1C). The movement was initiated most frequently in π/2 –π. In AM-tACS, the distribution of movement initiation was not significantly departed from uniformity (p = 0.620). The averaged VS-tACS with respect to the electromyography (EMG) onset showed a gradually rising waveform preceding it (Fig. 1D), which is similar to the waveform of MRCP [
]. It deviated significantly from the 95% CI approximately from 1.68 seconds prior to the EMG onset.
3. Discussion
The aim of this study was to investigate the relationships between the specific patterns of brain electrical activities in the M1 and voluntary movement initiations in humans. TACS have been used to entrain endogenous brain oscillations in a frequency- and phase-specific manner. The cortical excitability could be increased or decreased during anodal or cathodal phase of tACS, respectively. Since a negative EEG potential indicates an increment in the cortical excitability and vice versa in a positive EEG potential, the anodal and cathodal phases of tACS are thought to be associated with the negative and positive EEG potentials, respectively. In this study, VS-tACS over the M1 significantly induced the initiation of voluntary movements during the anodal phase. The averaged VS-tACS inducing the voluntary movement indicated a gradually rising waveform similar to the waveform of MRCP. These findings imply that the slowly increasing negative potential in the M1 induced a voluntary movement. A previous animal study showed that a specific pattern of the M1 electrical activity was necessary for voluntary movement initiations [
]. The specific M1 activity necessary for voluntary movement initiations may be represented by the slowly increasing negative potential recorded with an extracranial electrode over the M1. Recently, Armstrong et al. demonstrated that delivering tACS of 0.5 Hz frequency over the fronto-central premotor area influenced the initiation of voluntary sequential finger movement [
]. From this and the current work, it is likely that the slow, ongoing potential changes both in the SMA and the M1 influence the timing determination of voluntary motor initiation.
AM-tACS did not provoke the initiation of voluntary movements. Several reasons can be speculated: First, AM-tACS in this study could not entrain endogenous oscillations as we intended. Since a neuron's susceptibility to membrane polarization decreases with increasing frequency due to a transmembrane time constant for polarization by the applied field, it is possible that greater stimulation intensities were needed to entrain endogenous neural oscillations at such a high frequency as 90 Hz [
]. However, the stimulation intensities were not significantly different between VS-tACS and AM-tACS in this study, which suggests that the intensity of AM-tACS might not be sufficient for the entrainment. Second, AM-tACS at other frequencies than 90 Hz could provoke the initiation of voluntary movements. As ERD in the upper alpha or the lower beta band can be observed over the central region before the self-paced movements [
], we tried AM-tACS at alpha and beta frequencies in preliminary experiments; however, there were flashing lights or phosphenes rising and falling to the rhythm matched with the phase of the amplitude modulation. Since this subject's awareness of stimulation assignments did not allow for blinding of the participants, we did not adopt AM-tACS at the lower carrier frequency.
In conclusion, this study demonstrated that very slow-wave tACS of 0.125 Hz applied over the M1 could influence the onset time of simple voluntary movements. The averaged tACS inducing the voluntary movement showed a “MRCP-like” gradually rising waveform preceding the self-initiated movement. The specific pattern of cortical excitability in the contralateral M1 is behaviorally relevant and may be a necessary component of movement initiation.
There are no financial disclosures or conflicts of interest to report.
Acknowledgements
This study was partly supported by Grants-in-Aid for Scientific Research (KAKENHI) [grant number 21K17671 (S.S.), 21K19745 (T.M.), 22H04788 (T.M.)] from the Japan Society for the Promotion of Science, and a Grant-in-Aid for Research Expansion from the Niigata University of Health and Welfare, 2021.
We are grateful to Dr. Masao Matsuhashi (Department of Epilepsy, Movement Disorders and Physiology, Kyoto University Graduate School of Medicine) for providing the MATLAB script.
Appendix A. Supplementary data
The following is the Supplementary data to this article.
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