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

Abstract

Background: A 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.

Methods: We 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.

Results: Repetitive 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.

Conclusions: These 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.

Figure 1

(a) Two degree-of-freedom optical goniometer fixed to the dorsum of the wrist to measure deflection produced by TMS-induced twitch in the sagittal and coronal plane; (b) An example of goniometer trace as seen in the signal output for sagittal plane.

Figure 2

Schematic summary of the experimental design.

Figure 3

Mean group data for change in twitch direction of the wrist, showing a significant effect post intervention at time-point 1, with ~70% of subjects having a reversed direction from the original twitch. This effect was not sustained at time-point 2-5, and showed a trend to return to baseline across subjects by 10 minutes post.

Figure 4

Group MEP amplitude data (n = 20) recorded at rest before and immediately after training (t1). MEP amplitude in the antagonist muscle (to the trained muscle) was significantly reduced post training relative to pre, while the agonist (trained) muscle MEP amplitude was non-significantly elevated following the same training period.

Figure 5

Averaged MEP waveforms of one subject collected from the antagonist muscle at rest; (a) pre training and (b) immediately post training (t1), showing decreased amplitude following 5 minutes of training, associated with wrist movement, in direction opposite to that of original TMS-induced twitch.