Formation of a motor memory by action observation

Abstract

Mirror neurons discharge with both action observation and action execution. It has been proposed that the mirror neuron system is instrumental in motor learning. The human primary motor cortex (M1) displays mirror activity in response to movement observation, is capable of forming motor memories, and is involved in motor learning. However, it is not known whether movement observation can lead directly to the formation of motor memories in the M1, which is considered a likely physiological step in motor learning. Here, we used transcranial magnetic stimulation (TMS) to show that observation of another individual performing simple repetitive thumb movements gives rise to a kinematically specific memory trace of the observed motions in M1. An extended period of observation of thumb movements that were oriented oppositely to the previously determined habitual directional bias increased the probability of TMS-evoked thumb movements to fall within the observed direction. Furthermore, the acceleration of TMS-evoked thumb movements along the principal movement axis and the balance of excitability of muscle representations active in the observed movements were altered in favor of the observed movement direction. These findings support a role for the mirror neuron system in memory formation and possibly human motor learning.

Figure 1.

Experimental design. At the beginning of each session, the direction of TMS-evoked movements (“baseline before training”) was determined in each individual by assessing the first-peak accelerations along the extension/flexion and abduction/adduction axes (Classen et al., 1998). Subsequently, subjects participated in three different training sessions: physical training, which consisted of performance of voluntary thumb movements in a direction opposite the baseline direction and observation of thumb movements directed opposite the baseline direction and toward the baseline direction.

Figure 2.

Effect of different training interventions on TMS-evoked movement direction. A, Example of one subject. First-peak acceleration vectors of TMS-evoked thumb movements before (left) and after (right) each of the three interventions (PhysPract, ObsPract_opposite, and ObsPract_toward). For better comparability, all examples are aligned to the training direction indicated by the arrow. The TTZ is shown in gray. PhysPract and ObsPract_opposite, but not ObsPract_toward, led to substantial changes in the direction of TMS-evoked movements. B, Group data (n = 10) showing the P_TTZ before and after PhysPract, ObsPract_opposite, and ObsPract_toward. Before the training interventions, the percentage of TMS-evoked movements in TTZ was similar in PhysPract and ObsPract_opposite. PhysPract and ObsPract_opposite, but not ObsPract_toward, led to a significant increase in the percentage of TMS-evoked movements falling into TTZ. Data show means ± SEM. ^*p < 0.005. n.s., Not significant. C, Time course of changes of P_TTZ as a function of training intervention. To compare between conditions, ΔP_TTZ was computed as the baseline-normalized, intervention-dependent change in percentage of TMS-evoked thumb movements falling into the TTZ (see Materials and Methods). At the end of 30 min, the percentage change of TMS-evoked movements in TTZ was larger in PhysPract than in ObsPract_opposite or ObsPract_toward and with ObsPract_opposite than with ObsPract_toward. Rhombi, PhysPract; circles, ObsPract_opposite; triangles, ObsPract_toward. Filled symbols, Time points significantly different from baseline; two-tailed t tests; false discovery rate correction. ^*p < 0.05. D, Duration of changes of P_TTZ as a function of training intervention. Symbols as in C. Error bars represent SEM.

Figure 3.

Effect of different training interventions on compound acceleration vector. A, Group data (n = 10) showing the mean compound acceleration vector for the extension/flexion direction before and after training. Before training, the compound acceleration vector of each subject was aligned such that all vectors pointed into the extension direction. After PhysPract, the mean compound acceleration vector came to point into the flexion direction, corresponding to the practiced direction. ObsPract_opposite decreased the length of the mean compound acceleration vector, whereas ObsPract_toward did not change the mean compound acceleration vector. ^*p < 0.01. Open bars, Before training; filled bars, after training. B, Time course of changes of the mean compound acceleration vector as a function of training intervention. At the end of 30 min, the mean compound acceleration vector was smaller in PhysPract than in ObsPract_opposite or ObsPract_toward and with ObsPract_opposite than with ObsPract_toward. Error bars represent SEM. pre, Before training; B1, B2, and B3, results obtained after the first, second, and third training block, respectively.

Figure 4.

Effect of different training interventions on corticomuscular excitability. A, Changes in MEP amplitudes (relative to baseline) recorded from training agonist muscle (MEP_agonist; circles) and antagonist muscle (MEP_antagonist; triangles). PhysPract led to a significant increase in MEP_agonist compared with baseline. B, The ratio between the MEP_agonist and MEP_antagonist increased both after PhysPract and ObsPract_opposite but not after ObsPract_toward. Open bars, Before training; filled bars, after training. ^*p < 0.05. Error bars represent SEM.