Contributions of the motor cortex to adaptive control of reaching depend on the perturbation schedule

Abstract

During adaptation, motor commands tend to repeat as performance plateaus. It has been hypothesized that this repetition produces plasticity in the motor cortex (M1). Here, we considered a force field reaching paradigm, varied the perturbation schedule to potentially alter the amount of repetition, and quantified the interaction between disruption of M1 using transcranial magnetic stimulation (TMS) and the schedule of perturbations. In the abrupt condition (introduction of the perturbation on a single trial followed by constant perturbation), motor output adapted rapidly and was then followed by significant repetition as performance plateaued. TMS of M1 had no effect on the rapid adaptation phase but reduced adaptation at the plateau. In the intermediate condition (introduction of the perturbation over 45 trials), disruption of M1 had no effect on the phase in which motor output changed but again impaired adaptation when performance had plateaued. Finally, when the perturbation was imposed gradually (over 240 trials), the motor commands continuously changed during adaptation and never repeated, and disruption of M1 had no effect on performance. Therefore, TMS of M1 appeared to reduce adaptation of motor commands during a specific phase of learning: when motor commands tended to repeat.

Figure 1.

(A) Experimental setup. Subjects were seated in front of a robotic arm and were asked to hold the handle and shoot through a 10 cm distant target. The two targets that we used are plotted here. (B) TMS was delivered when the hand crossed the target during the force-field trials. (C) Subjects participated in one of the three experiments: abrupt, intermediate, or gradual. In the first 90 trials, the robot did not produce any forces. In the subsequent 290 trials, a curl force field was introduced, perturbing the hand perpendicular to its direction of motion. It was introduced either over 1 trial (abrupt condition), over 45 trials (intermediate condition), or over 240 trials (gradual condition). The gray bars represent error-clamp trials (see Methods).

Figure 2.

Force output in the abrupt, intermediate, and gradual protocols. (A) Performance of the abrupt group. Top row: perturbation schedule. Middle row: peak force in error-clamp trials over the course of the training. The solid curves represent the running average over a window of 10 trials, which are interrupted during set breaks. Error bars are standard error of the mean. Bottom row: output of the ANCOVA on peak force in error-clamp trials during the early and late periods of training (factor: group and covariate: peak velocity). Error bars are CI. (B) Performance of the intermediate group. (C) Performance of the gradual group. (D) Running standard deviation of the peak force for the control groups (blue curves of middle row) is presented on the left panel. In the normalized version of this plot (right panel), the standard deviation of the force is divided by its magnitude.

Figure 3.

Site specificity of the TMS effect. TMS impaired peak force when it was delivered over the primary motor cortex (red curve, same as Figure 2A) but not when delivered over the occipital cortex (green curve). Figure structure is similar to Figure 2.

Figure 4.

Force output during the end of training period and throughout the posttraining period. (A) Peak force over the course of last 25 error-clamp trials during the training period and the 80 ensuing ones. Trial bins consisted of 5 trials each. Error bars are standard error of the mean. (B) Bootstrap estimate population of the decay parameter b(10 000 resamplings). Top horizontal bars represent CI. Top row: abrupt condition, middle row: intermediate condition, and bottom row: gradual condition.

Figure 5.

Kinematics of the reach in the abrupt, intermediate, and gradual protocols. (A) Performance of the abrupt group. Top row: perturbation schedule. Middle row: endpoint error over the course of the training. The solid curves represent the running average over a window of 14 trials, which are interrupted during set breaks. Error bars are standard error of the mean (SEM). Bottom row: average trajectory profiles during baseline (trials 41–90), early (trials 136–185), and late periods (trials 331–380). Trials were rotated such that the target is represented 10 cm away in the North direction. Areas around the curves represent SEM. (B) Kinematics of the intermediate group. (C) Kinematics of the gradual group.

Figure 6.

Effect of TMS on early and late components of movement trajectories. (A) Schematic representation of how the trajectories were spatially divided into 2 phases (early phase: parallel position <5 cm and late phase: parallel position >5 cm). (B), (C), (D), and (E): intersubject relationship between the average perpendicular velocity and endpoint error for the CTRL and TMS groups (B and C and D and E, respectively) during the late training period. The average perpendicular velocity was computed either during the early (B and D) or late (C and E) phase of the movements. (E) Bootstrap estimate population of the Δc parameter (10 000 resamplings). This parameter represents the difference between the standardized coefficients of the multiple regression. In this regression, endpoint error is the dependent measure, and average perpendicular velocities of the early and late phases of the movement are the 2 factors. For this analysis, CTRL (CTRL_INT, CTRL_ABR, and TMS_OC) and TMS (TMS_INT and TMS_ABR) groups across the intermediate and abrupt conditions were collapsed together.