Repetitive Peripheral Magnetic Stimulation of Wrist Extensors Enhances Cortical Excitability and Motor Performance in Healthy Individuals

Abstract

Repetitive peripheral magnetic stimulation (rPMS) may improve motor function following central nervous system lesions, but the optimal parameters of rPMS to induce neural plasticity and mechanisms underlying its action remain unclear. We examined the effects of rPMS over wrist extensor muscles on neural plasticity and motor performance in 26 healthy volunteers. In separate experiments, the effects of rPMS on motor evoked potentials (MEPs), short-interval intracortical inhibition (SICI), intracortical facilitation (ICF), direct motor response (M-wave), Hoffmann-reflex, and ballistic wrist extension movements were assessed before and after rPMS. First, to examine the effects of stimulus frequency, rPMS was applied at 50, 25, and 10 Hz by setting a fixed total number of stimuli. A significant increase in MEPs of wrist extensors was observed following 50 and 25 Hz rPMS, but not 10 Hz rPMS. Next, we examined the time required to induce plasticity by increasing the number of stimuli, and found that at least 15 min of 50 and 25 Hz rPMS was required. Based on these parameters, lasting effects were evaluated following 15 min of 50 or 25 Hz rPMS. A significant increase in MEP was observed up to 60 min following 50 and 25 Hz rPMS; similarly, an attenuation of SICI and enhancement of ICF were also observed. The maximal M-wave and Hoffmann-reflex did not change, suggesting that the increase in MEP was due to plastic changes at the motor cortex. This was accompanied by increasing force and electromyograms during wrist ballistic extension movements following 50 and 25 Hz rPMS. These findings suggest that 15 min of rPMS with 25 Hz or more induces an increase in cortical excitability of the relevant area rather than altering the excitability of spinal circuits, and has the potential to improve motor output.

Keywords: corticospinal tract; intracortical circuits; plasticity; rehabilitation; spinal networks; upper extremity.

FIGURE 1

Experimental protocol. (A) Time course of Experiments 1 and 2. (B) Stimulation conditions for Experiments 1 and (C) 2. (D) Time course of Experiments 3 and 4. (E) In Experiments 3 and 4, three sessions (a total of 225 ON-OFF cycles) were performed.

FIGURE 2

Effects of rPMS frequency on motor evoked potentials (MEPs). (A) MEP amplitudes of extensor carpi radialis (ECR) and (B) flexor carpi radialis (FCR) muscles were normalized to baseline amplitude. Each box plot indicates results following rPMS at 50 (white), 25 (dark gray), or 10 Hz (light gray). Median and interquartile ranges are represented by horizontal lines within boxes and whiskers (representing minimum and maximum values), respectively. Asterisks indicate significant differences compared to “T0” (p < 0.05).

FIGURE 3

Effects of rPMS stimulus dose on motor evoked potentials (MEPs). (A) MEP amplitudes of extensor carpi radialis (ECR) and (B) flexor carpi radialis (FCR) were normalized to baseline amplitude. Each box plot indicates results following rPMS at 50 (white) and 25 Hz (dark gray). Median and interquartile ranges are represented by horizontal lines within boxes and whiskers (representing minimum and maximum values), respectively. Asterisks indicate significant differences compared to “T0” (p < 0.05).

FIGURE 4

Lasting effects of rPMS on motor evoked potentials (MEPs). (A) MEP amplitudes of extensor carpi radialis (ECR) and (B) flexor carpi radialis (FCR) were normalized to baseline amplitude. Each box plot indicates that results following rPMS at 5 (white) and 25 Hz (dark gray). Median and interquartile ranges are represented by horizontal lines within boxes and whiskers (representing minimum and maximum values), respectively. Asterisks indicate significant differences compared to “Pre” (p < 0.05).

FIGURE 5

Lasting effects of rPMS on short-interval intracortical inhibition (SICI) and intracortical facilitation (ICF). Conditioned MEP amplitudes in the ECR (A,C) and FCR (B,D) were normalized to mean test MEP amplitudes to calculate SICI (inter-stimulus interval: 2.5 ms) (A,B) and ICF (inter-stimulus interval: 10 ms) (C,D). The mean values and 95% confidence interval obtained from 20 participants are indicated. Each symbol indicates results following rPMS at 50 (white box) and 25 Hz (dark gray circle). Asterisks indicate significant differences compared to “Pre” (p < 0.05).

FIGURE 6

Changes in force and electromyogram (EMG) during wrist ballistic movements. Raw traces of force (upper) and rectified EMG from the ECR (lower) obtained from a subject during brief, fast, isometric voluntary wrist extension movements before and after rPMS at 50 (A) and 25 Hz (B). Each waveform represents the average of 10 trials. Individual changes in force (C,D) and EMGs (E,F) during the movements before and immediately after rPMS are shown. Group data of force (G) and EMGs (H) are also shown. The mean values and 95% confidence intervals obtained from 20 participants are indicated. Asterisks indicate significant differences compared to “Pre” (p < 0.05).