Reversal of TMS-induced motor twitch by training is associated with a reduction in excitability of the antagonist muscle

Abstract

BackgroundA single session of isolated repetitive movements of the thumb can alter the response to transcranial magnetic stimulation (TMS), such that the related muscle twitch measured post-training occurs in the trained direction. This response is attributed to transient excitability changes in primary motor cortex (M1) that form the early part of learning. We investigated; (1) whether this phenomenon might occur for movements at the wrist, and (2) how specific TMS activation patterns of opposing muscles underlie the practice-induced change in direction.MethodsWe used single-pulse suprathreshold TMS over the M1 forearm area, to evoke wrist movements in 20 healthy subjects. We measured the preferential direction of the TMS-induced twitch in both the sagittal and coronal plane using an optical goniometer fixed to the dorsum of the wrist, and recorded electromyographic (EMG) activity from the flexor carpi radialis (FCR) and extensor carpi radialis (ECR) muscles. Subjects performed gentle voluntary movements, in the direction opposite to the initial twitch for 5 minutes at 0.2 Hz. We collected motor evoked potentials (MEPs) elicited by TMS at baseline and for 10 minutes after training.ResultsRepetitive motor training was sufficient for TMS to evoke movements in the practiced direction opposite to the original twitch. For most subjects the effect of the newly-acquired direction was retained for at least 10 minutes before reverting to the original. Importantly, the direction change of the movement was associated with a significant decrease in MEP amplitude of the antagonist to the trained muscle, rather than an increase in MEP amplitude of the trained muscle.ConclusionsThese results demonstrate for the first time that a TMS-twitch direction change following a simple practice paradigm may result from reduced corticospinal drive to muscles antagonizing the trained direction. Such findings may have implications for training paradigms in neurorehabilitation.

Interhemispheric interactions associated with unilateral ballistic motor tasks

“…Our results are consistent with previous data from our laboratory, where twitch direction shifted significantly after training was performed at a distance of 90° away from the baseline twitch direction (Selvanayagam, et al, 2011). While some previous TMS studies, which involved repetitive ballistic thumb movements, reported that twitch directions shifted toward the training direction after 30 minutes of training at 180° away from baseline (Bütefisch et al, 2000;Bütefisch, et al, 2004;Classen, et al, 1998;Giacobbe, et al, 2011;Kaelin-Lang et al, 2005), we showed early neural adaptation occurred with a session of just 40 ballistic wrist contractions at 90° distance away from baseline (Selvanayagam, et al, 2011). The shift in twitch directions is likely to reflect the reweighting of connectivity among the forearm muscles to favour net force production in the training direction (Selvanayagam, et al, 2012a).…”

“…Another consequence of use-dependent learning is demonstrated by a sustained, post-training shift of involuntary (TMS-evoked) twitch direction in the active limb toward the practiced direction (Classen et al, 1998;Giacobbe et al, 2011;van Elswijk et al, 2008).…”

“…A classic example of use-dependent learning is demonstrated by a shift in the twitch direction evoked by Transcranial Magnetic Stimulation (TMS) toward the training direction after repetitive thumb ballistic movements (Classen, et al, 1998;Giacobbe, et al, 2011;van Elswijk, et al, 2008). Apart from a change in the direction of artificially-evoked twitches, use-dependent learning arising from repetitive aiming also reduces the variability of voluntary movements (Verstynen & Sabes, 2011) and biases subsequent voluntary movements toward the repeated direction (Selvanayagam, et al, 2012a;Verstynen & Sabes, 2011).…”

Mechanical effects of repetitive transcranial magnetic stimulation of upper airway muscles in awake obstructive sleep apnoea subjects

“…Moreover, if a balance towards UA constriction contributes to the effects observed with rTMS, this would explain a plateauing in MEP GG Amp , because a reduction of excitability seems to occur in the antagonists of a TMS‐targeted muscle (Giacobbe et al . ).…”

“…The plateauing of inspiratory rTMS GG Amp jointly with the reductions inV I, max and V I suggest that the balance towards constriction is greater during inspiration in comparison to expiration. Moreover, if a balance towards UA constriction contributes to the effects observed with rTMS, this would explain a plateauing in MEP GG Amp , because a reduction of excitability seems to occur in the antagonists of a TMS-targeted muscle (Giacobbe et al 2011).…”