Static magnetic field stimulation of the supplementary motor area modulates resting-state activity and motor behavior

José A Pineda-Pardo,Guglielmo Foffani,Bryan A Strange,Ignacio Obeso,José A Obeso,Pasqualina Guida,Michele Dileone,Antonio Oliviero

doi:10.1038/s42003-019-0643-8

Abstract

Focal application of a strong static magnetic field over the human scalp induces measurable local changes in brain function. Whether it also induces distant effects across the brain and how these local and distant effects collectively affect motor behavior remains unclear. Here we applied transcranial static magnetic field stimulation (tSMS) over the supplementary motor area (SMA) in healthy subjects. At a behavioral level, tSMS increased the time to initiate movement while decreasing errors in choice reaction-time tasks. At a functional level, tSMS increased SMA resting-state fMRI activity and bilateral functional connectivity between the SMA and both the paracentral lobule and the lateral frontotemporal cortex, including the inferior frontal gyrus. These results suggest that tSMS over the SMA can induce behavioral aftereffects associated with modulation of both local and distant functionally-connected cortical circuits involved in the control of speed-accuracy tradeoffs, thus offering a promising protocol for cognitive and clinical research.

Highlights

Focal application of a strong static magnetic field over the human scalp induces measurable local changes in brain function
Transcranial static magnetic field stimulation is a recent non-invasive brain stimulation (NIBS) technique that consists of focally applying a relatively strong neodymium magnet over the scalp22. transcranial static magnetic field stimulation (tSMS) induces a reduction of cortical excitability that outlasts the duration of the stimulation, as measured by decreased motor-evoked potentials, somatosensory-evoked potentials, and intra-epidermal electrical stimulation-evoked potentials when applied over the motor cortex[22,23,24,25,26,27,28,29,30,31,32], and by locally increased electroencephalography α-activity when applied over the visual cortex[33] or the somatosensory cortex[34]
In order to investigate whether the increased functional connectivity between the supplementary motor area (SMA) and the distant clusters genuinely reflected increased co-activity of the underlying networks rather than being an artifact of the local changes[42], we analyzed the activity in the distant clusters, and we found a trend toward significant change in amplitude of low-frequency fluctuations (ALFF) (three-way repeated-measures analysis of variance (ANOVA), Time × Stimulation: F(1,18) = 3.7, p = 0.069) and a significant change in regional homogeneity (ReHo) (F(1,18) = 5.9, p = 0.0255)

Summary

Introduction

Focal application of a strong static magnetic field over the human scalp induces measurable local changes in brain function. TSMS increased SMA resting-state fMRI activity and bilateral functional connectivity between the SMA and both the paracentral lobule and the lateral frontotemporal cortex, including the inferior frontal gyrus These results suggest that tSMS over the SMA can induce behavioral aftereffects associated with modulation of both local and distant functionally-connected cortical circuits involved in the control of speed-accuracy tradeoffs, offering a promising protocol for cognitive and clinical research. The most anterior section of the SMA—the pre-SMA2 has wide connections to the prefrontal cortex[3,8] and is predominantly involved in cognitive operations underlying behavioral change, such as action switching[9,10], movement stopping[11,12,13], and setting speed-accuracy tradeoffs in decision making[14,15]. We investigated the local and distant tSMS after-effects by quantifying the amplitude of low-frequency fluctuations (ALFF), the regional homogeneity (ReHo), and the whole-brain seed-based functional connectivity using left and right SMA regions of interest (ROIs)

Methods

Results

Conclusion