Impairment of retention but not acquisition of a visuomotor skill through time-dependent disruption of primary motor cortex

Abstract

Learning a visuomotor skill involves a distributed network which includes the primary motor cortex (M1). Despite multiple lines of evidence supporting the role of M1 in motor learning and memory, it is unclear whether M1 plays distinct roles in different aspects of learning such as acquisition and retention. Here, we investigated the nature and chronometry of that processing through a temporally specific disruption of M1 activity using single-pulse transcranial magnetic stimulation (TMS). We applied single-pulse TMS to M1 or dorsal premotor cortex (PMd) during adaptation of rapid arm movements (approximately 150 ms duration) to a visuomotor rotation. When M1 was stimulated either immediately after the end of each trial or with a 700 ms delay, subjects exhibited normal adaptation. However, whereas the memory of the subjects who received delayed-TMS showed normal rates of forgetting during deadaptation, the memory of those who received immediate TMS was more fragile: in the deadaptation period, they showed a faster rate of forgetting. Stimulation of PMd with adjusted (reduced) intensity to rule out the possibility of coactivation of this structure caused by the current spread from M1 stimulation did not affect adaptation or retention. The data suggest that, during the short time window after detection of movement errors, neural processing in M1 plays a crucial role in formation of motor memories. This processing in M1 may represent a slow component of motor memory which plays a significant role in retention.

Figure 1.

Experimental design. Thick lines represent visual rotation magnitude. Arrows indicate the blocks with TMS.

Figure 2.

TMS of M1 immediately after trial end impaired performance during deadaptation but not adaptation. A, Angular endpoint errors (mean ± SEM of three-trial bins) during preadaptation, adaptation, and deadaptation periods of experiment 1. Positive values indicate counter-clockwise deviation. Inset, Expansion of box showing trial-by-trial errors (mean ± SEM) during the early part of the deadaptation period. B, Cursor trajectories (mean ± SD) for first three and last three trials of each adaptation block, and for first six trials and last three trials of deadaptation period. Trajectory labels correspond to trial numbers.

Figure 3.

TMS of M1 immediately after trial end during null blocks did not affect subsequent adaptation to abrupt counter-clockwise 30° visual rotation. Angular endpoint errors (mean ± SEM of three-trial bins) during preadaptation, null with TMS, adaptation, and deadaptation periods of experiment 2 are shown.