Letter to the editor: No influence of static magnetic stimulation applied for 30 minutes over the human M1 on corticospinal excitability

We have read with great interest the article recently published by Dileone et al. (2018) [[1]Dileone M. Mordillo-Mateos L. Oliviero A. Foffani G. Long-lasting effects of transcranial static magnetic field stimulation on motor cortex excitability.Brain Stimul. 2018; 11: 676-688Abstract Full Text Full Text PDF PubMed Scopus (38) Google Scholar] reporting that a 30-min application of transcranial static magnetic stimulation (tSMS) over the human primary motor cortex (M1) can yield long-lasting (∼30 min) inhibition of corticospinal excitability (CSE), an effect that is reminiscent of long-term depression plasticity. These results are exciting as they open the door for potential therapeutic applications of tSMS, especially since the technique is portable, inexpensive, and requires little training for its utilization. Due to the potential implications of these results, and because they were obtained in small (n ≤ 10) and non-independent samples, it appears important to ascertain the effectiveness of tSMS to induce lasting changes in CSE and, hopefully, to avoid the pitfalls and controversies encountered with other non-invasive brain stimulation techniques (NIBS) in the past [[2]Horvath J.C. Forte J.D. Carter O. Evidence that transcranial direct current stimulation (tDCS) generates little-to-no reliable neurophysiologic effect beyond MEP amplitude modulation in healthy human subjects: a systematic review.Neuropsychologia. 2015; 66: 213-236Crossref PubMed Scopus (356) Google Scholar]. Here, tSMS (nickel-plated neodymium disc magnet; 50 mm diameter, 50 mm thickness, axially magnetized, 139Kg pull force) was applied over M1 for 30 min (n = 18) and CSE was assessed immediately after and up to 58 min after tSMS removal by recording motor evoked potentials (MEPs). Neuronavigation was used to ensure stable coil positioning, and 30 MEPs were collected at each measurement, providing a 100% probability of falling inside the 95% confidence intervals around the average MEP amplitude [[3]Chang W.H. et al.Optimal number of pulses as outcome measures of neuronavigated transcranial magnetic stimulation.Clin Neurophysiol Off J Int Fed Clin Neurophysiol. 2016; 127: 2892-2897Crossref PubMed Scopus (72) Google Scholar]. Globally, the present results revealed that tSMS failed to alter CSE at any post-measurement (see Fig. 1). To determine if tSMS altered normalized MEP amplitude, each post-measurement was separately compared to the value of 1 (100%) using two-tailed one-sample t-tests. The results revealed no effect of tSMS on MEP amplitude at any of the 6 post-measurements (uncorrected p values; all t(17) < 1.733, all p > 0.101, all Cohen’s dz < 0.408), suggesting that tSMS did not alter CSE. A repeated measures ANOVA conducted on the raw (non-normalized) MEP data also failed to indicate a tSMS-induced alteration of CSE (F(6,102) = 0.958, p = 0.458, np2 = 0.053), confirming that the null results were not due to data normalization. To determine the sample size required to detect a significant decrease in MEP amplitude in the timeframe (∼30 min) reported by Dileone et al. (2018) [[1]Dileone M. Mordillo-Mateos L. Oliviero A. Foffani G. Long-lasting effects of transcranial static magnetic field stimulation on motor cortex excitability.Brain Stimul. 2018; 11: 676-688Abstract Full Text Full Text PDF PubMed Scopus (38) Google Scholar], the effect size of the average of the first three post-measurements corresponding to that timeframe (∼25 min) was used to perform a sample size calculation (t(17) = 1.529, p = 0.145, Cohen’s dz = 0.360) with G*Power (v3.1.9.2). Assuming an 80% statistical power, this analysis revealed that 63 individuals would be required to detect a significant difference with a two-tailed one-sample t-test. The possibility that tSMS could exert inhibitory influences on CSE that outlast the stimulation period would open the door to exciting applications of the technique. For this reason, we attempted to replicate the original findings of Dileone et al. (2018) [[1]Dileone M. Mordillo-Mateos L. Oliviero A. Foffani G. Long-lasting effects of transcranial static magnetic field stimulation on motor cortex excitability.Brain Stimul. 2018; 11: 676-688Abstract Full Text Full Text PDF PubMed Scopus (38) Google Scholar]. Despite a larger sample, the use of neuronavigation, and an optimal number of pulses to reliably assess MEP amplitude, we found no influence of a 30-min application of tSMS over M1 on CSE for nearly an hour after its removal. These null results corroborate those of Kufner et al. (2017) [[4]Kufner M. Brückner S. Kammer T. No modulatory effects by transcranial static magnetic field stimulation of human motor and somatosensory cortex.Brain Stimul. 2017; 10: 703-710Abstract Full Text Full Text PDF PubMed Scopus (18) Google Scholar], who also failed to show any effects of tSMS on CSE (10–15 min application; n = 15), and suggest that tSMS, like other NIBS techniques [[5]Guerra A. López-Alonso V. Cheeran B. Suppa A. Variability in non-invasive brain stimulation studies: reasons and results.Neurosci Lett. 2017; 133330https://doi.org/10.1016/j.neulet.2017.12.058Crossref Scopus (82) Google Scholar], is subject to considerable variability. These results emphasize the crucial need to implement strategies to minimize variability [[6]Guerra A. López-Alonso V. Cheeran B. Suppa A. Solutions for managing variability in non-invasive brain stimulation studies.Neurosci Lett. 2017; https://doi.org/10.1016/j.neulet.2017.12.060Crossref Scopus (50) Google Scholar] to firmly establish the reliability and efficiency of tSMS. Such strategies include performing sample size calculations [[7]Algermissen J. Mehler D.M.A. May the power be with you: are there highly powered studies in neuroscience, and how can we get more of them?.J Neurophysiol. 2018; 119: 2114-2117Crossref PubMed Scopus (23) Google Scholar], using neuronavigation to ensure stable coil positioning [[6]Guerra A. López-Alonso V. Cheeran B. Suppa A. Solutions for managing variability in non-invasive brain stimulation studies.Neurosci Lett. 2017; https://doi.org/10.1016/j.neulet.2017.12.060Crossref Scopus (50) Google Scholar], and refraining from pre-selecting or pooling participants on the basis of being responders or not to a given NIBS intervention [[8]van de Ruit M. Grey M.J. False positives associated with responder/non-responder analyses based on motor evoked potentials.Brain Stimul. 2019; 12: 314-318Abstract Full Text Full Text PDF PubMed Scopus (9) Google Scholar]. Finally, as the relevance of MEP amplitude alterations in drawing inferences on cortical functioning remains poorly understood [[9]Bestmann S. Krakauer J.W. The uses and interpretations of the motor-evoked potential for understanding behaviour.Exp Brain Res. 2015; 233: 679-689Crossref PubMed Scopus (189) Google Scholar], the failure of tSMS to alter CSE does not necessarily entail that tSMS has no influence on cortical functioning [[10]Gonzalez-Rosa J.J. et al.Static magnetic field stimulation over the visual cortex increases alpha oscillations and slows visual search in humans.J Neurosci Off J Soc Neurosci. 2015; 35: 9182-9193Crossref PubMed Scopus (45) Google Scholar]. Nonetheless, the neurophysiological effects of tSMS should be clarified and confirmed before considering a widespread implementation of the technique. A total of 18 participants (7 females; 21.7 ± 1.2 years old; mean ± SEM) were recruited to ensure a 98.7% chance (achieved power analysis conducted with G*Power v3.1.9.2) of replicating the effect size reported by Dileone et al., 2018 [[1]Dileone M. Mordillo-Mateos L. Oliviero A. Foffani G. Long-lasting effects of transcranial static magnetic field stimulation on motor cortex excitability.Brain Stimul. 2018; 11: 676-688Abstract Full Text Full Text PDF PubMed Scopus (38) Google Scholar] (two-tailed t-tests; Cohen’s dz = 1.070; comparison immediately following tSMS removal). Participants were neurologically healthy and were screened for TMS contraindications prior to the experiment. Procedures were approved by the local ethics committee and participants gave their informed written consent. Electromyographic (EMG) data were recorded in a tendon-belly arrangement from the right FDI. The ground electrode was placed on the lateral epicondyle of the right humerus, and the reference electrode on the distal portion of the right index. The EMG signal was amplified using a Powerlab 4/20 system (ADinstruments, Colorado Springs, CO), filtered with a 0.3–1000Hz bandpass and digitized at a sampling rate of 4 kHz. tSMS was applied for 30 minutes over the FDI hotspot in the left M1. tSMS was tightly held in place against the scalp using a custom-made set of nonskid straps comfortably attached around participants’ head. Single pulses of TMS were delivered using a Magstim BiStim [[2]Horvath J.C. Forte J.D. Carter O. Evidence that transcranial direct current stimulation (tDCS) generates little-to-no reliable neurophysiologic effect beyond MEP amplitude modulation in healthy human subjects: a systematic review.Neuropsychologia. 2015; 66: 213-236Crossref PubMed Scopus (356) Google Scholar] (The Magstim Company, Whitland, UK) with a 70mm figure-of-eight coil. The resting motor threshold of the right FDI muscle was defined as the intensity needed to generate MEPs of peak-to-peak amplitude higher than 50 μV in the FDI for 5 out of 10 consecutive pulses. The intensity of TMS pulses was individually adjusted to elicit MEPs of ± 1mV of peak-to-peak amplitude at the pre-measurement and was subsequently kept constant for all post-measurements. An interval of 8 minutes separated each MEP post-measurement. MEPs were recorded at a jittered frequency of 0.15–0.25 Hz. Once acquired, individual MEP data were separately averaged at each measurement. The authors have no conflict of interest to declare. This work was funded by the Natural Sciences and Engineering Research Council of Canada (Grant number: RGPIN-2017-05510) and Fonds de la recherche en sante du Québec (Grant number: 33140). The following is the supplementary data to this article: Download .xlsx (.05 MB) Help with xlsx files Multimedia component 1 Response to significant influence of static magnetic stimulation applied for 30 minutes over the human M1 on corticospinal excitabilityBrain Stimulation: Basic, Translational, and Clinical Research in NeuromodulationVol. 13Issue 5PreviewWe are pleased that our recent attempt to replicate the methods and results from Dileone et al. [1] has garnered attention from the authors of the original findings. Briefly, despite having a ∼99% probability of replicating the results from Dileone et al. [1], our results revealed that transcranial static magnetic stimulation (tSMS) yielded neither significant (all uncorrected p values > 0.101) nor meaningful (effect size values below medium-sized benchmark values; all Cohen’s dz < 0.408) depression of corticospinal excitability (CSE) [2], a finding also reported by another group using a smaller sample [3]. Full-Text PDF Open Access

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