Brain polarization enhances the formation and retention of motor memories

Abstract

One of the first steps in the acquisition of a new motor skill is the formation of motor memories. Here we tested the capacity of transcranial DC stimulation (tDCS) applied over the motor cortex during motor practice to increase motor memory formation and retention. Nine healthy individuals underwent a crossover transcranial magnetic stimulation (TMS) study designed to test motor memory formation resulting from training. Anodal tDCS elicited an increase in the magnitude and duration of motor memories in a polarity-specific manner, as reflected by changes in the kinematic characteristics of TMS-evoked movements after anodal, but not cathodal or sham stimulation. This effect was present only when training and stimulation were associated and mediated by a differential modulation of corticomotor excitability of the involved muscles. These results indicate that anodal brain polarization can enhance the initial formation and retention of a new motor memory resulting from training. These processes may be the underlying mechanisms by which tDCS enhances motor learning.

FIG. 1.

Schematic representation of the main experiment setup. A: pre. Transcranial magnetic stimulation (TMS)–evoked movement directions were derived from the first-peak acceleration in the 2 major axes of the movement (extension/flexion and abduction/adduction) measured by an accelerometer mounted on the proximal phalanx of the thumb. Black arrows indicate the direction of individual TMS-evoked thumb movements (in this case extension and abduction). B: motor training. Pre was followed in 2 separate sessions randomly ordered by 30 min of motor training with either sham or anodal transcranial DC stimulation (tDCS) being applied over the left primary motor cortex (M1). Voluntary thumb movements were performed in a direction opposite to the baseline TMS-evoked movement direction (in this case: flexion and adduction). C: post 1 (p1). The direction of TMS-evoked thumb movements was determined as previously measured in pre. D: post 2 (p2). The subjects rested for 10 min and the direction of TMS-evoked thumb movements was again determined.

FIG. 2.

Intervention-dependent changes in TMS-evoked thumb movement directions in a representative subject. Each line represents the first-peak acceleration direction vector of a single thumb movement. The pre block is characterized by predominantly extension/adduction movement directions in both sessions. A: after motor training with anodal tDCS the direction of TMS-evoked thumb movements (p1) changed to a direction similar to training (flexion/abduction). This was partially maintained in p2. B: after training with sham tDCS the direction of TMS-evoked thumb movements within p1 did not have such a dramatic change with only a small proportion of movements moving in a direction similar to motor training. For p2 all movements were in a direction similar to the pre block.

FIG. 3.

Percentage of movements falling in the training target zone (pTTZ). A: with anodal tDCS applied during training there was a significant increase in movements falling within the TTZ during p1 and p2. Asterisks denote P ≤ 0.02. B: 50 min after the cessation of anodal tDCS (p3) TMS-evoked movement directions returned to premotor training values (n = 3). C: TMS-evoked movement directions were similar between sham and cathodal sessions at p1 and p2 times (n = 3). D: application of anodal tDCS for 30 min without motor training did not elicit changes in pTTZ. Data are means ± SE.

FIG. 4.

Angular distance and compound acceleration of TMS-evoked movements. A: angular distance of TMS-evoked movements relative to training during pre, p1, and p2. In comparison to sham, anodal tDCS led to a greater reduction in the angular distance between training movements and those evoked by TMS at p1 and p2 times. Please note that at pre, both sessions have similar angular difference from the trained direction. B: average compound acceleration during pre, p1, and p2. Anodal tDCS led to a greater change in direction of compound acceleration during p1 and p2 relative to sham. Asterisks, P ≤ 0.03. Data are means ± SE.

FIG. 5.

Corticomotor excitability, measured by the motor-evoked potential (MEP) amplitude for the agonist and antagonist muscles involved in motor training. A: changes in the MEP amplitude recorded from the training antagonist (closed squares) and agonist (open diamonds) muscles. MEP amplitudes increased with both sham and anodal tDCS. B: MEP amplitude ratio (post/pre) significantly increased in the MEPagonist muscle compared with the MEPantagonist during p1 for both sham and anodal tDCS. For anodal tDCS this difference was maintained during p2. For both p1 and p2, anodal tDCS resulted in a greater increase in the MEPagonist ratio. Asterisks, P ≤ 0.05. Data are means ± SE.