Extinction interferes with the retrieval of visuomotor memories through a mechanism involving the sensorimotor cortex

Abstract

Savings is a fundamental property of learning. In motor adaptation, it refers to the improvement in learning observed when adaptation to a perturbation A (A1) is followed by re-adaptation to the same perturbation (A2). A common procedure to equate the initial level of error across sessions consists of restoring native sensorimotor coordinates by inserting null--unperturbed--trials (N) just before re-adaptation (washout). Here, we hypothesized that the washout is not innocuous but interferes with the expression of the new memory at recall. To assess this possibility, we measured savings following the A1NA2 protocol, where A was a 40° visual rotation. In Experiment 1, we increased the time window between N and A2 from 1 min to 24 h. This manipulation increased the amount of savings during middle to late phases of adaptation, suggesting that N interfered with the retrieval of A. In Experiment 2, we used repetitive TMS to evaluate if this interference was partly mediated by the sensorimotor cortex (SM). We conclude that the washout does not just restore the unperturbed sensorimotor coordinates, but inhibits the expression of the recently acquired visuomotor map through a mechanism involving SM. Our results resemble the phenomenon of extinction in classical conditioning.

Keywords: adaptation; anterograde interference; motor learning; null trials; sensorimotor cortex; transcranial magnetic stimulation.

Figure 1.

Experimental design. Shown is the experimental design for Experiment 1 (A,B) and Experiment 2 (C). Each plot indicates the presence (1) or absence (0) of the perturbation as a function of the number of trials. (A) On day 1, control subjects of Experiment 1 (A₁NA₂) were exposed to 2 blocks of null trials (baseline) followed by 6 blocks of a 40° clockwise rotation. On day 2, they were exposed to 2 blocks of null trials (washout), followed by 6 blocks of the same clockwise rotation (re-adaptation). (B) Like control subjects, experimental subjects (A₁NA₂-24 h) were washed out on day 2 but re-adapted 24 h later, on day 3. (C) Sham and experimental subjects of Experiment 2 followed the same protocol as A₁NA₂, but before the washout were exposed to 15 min of rTMS over the sensorimotor cortex (A₁NA₂-M1) or the vertex (A₁NA₂-Sham). After the washout, there was a 15-min period to prevent the spread of rTMS effects into re-adaptation. Error-free trials are indicated by 2 parallel segments (||).

Figure 2.

Learning curves for Experiment 1. Mean visuomotor error ± SE are shown as a function of cycle (one cycle = average of 8 trials) for the adaptation and re-adaptation sessions. (A) A₁NA₂, (B) A₁NA₂-24 h. The curves resulting from fitting the data with a double exponential function are displayed for the adaptation and re-adaptation sessions.

Figure 3.

Initial level of error reduction. Shown is the mean ± SE percent reduction in the initial visuomotor error (first cycle) across learning sessions for Experiment 1 (A) and Experiment 2 (B). Only the experimental group of Experiment 1 (A₁NA₂-24 h) showed a significant increment in the initial level of error reduction as indicated by an asterisk (*P < 0.01).

Figure 4.

Progression of savings as a function of cycle for Experiment 1. (A) Savings (S) was computed as the cumulative percent increment in learning from adaptation, according to equation 2. Shown are the mean ± SE of S for each cycle of the experimental (A₁NA₂-24 h) and the control (A₁NA₂) group. Note that A₁NA₂-24 h starts from zero because the first cycle was removed by the correction.

Figure 5.

Time course of EF₂ and the end of the washout for A₁NA₂-24 h. Shown is the time course of the mean ± SE of the visuomotor error for the last 16 trials of the washout (WO) and the 16 trials of the second set of error-free trials (EF₂).

Figure 6.

Learning curves for Experiment 2. Mean visuomotor error ± SE are shown as a function of cycle (1 cycle = average of 8 trials) for the adaptation and re-adaptation sessions. (A) A₁NA₂-sham, (B) A₁NA₂-M1. The curves resulting from fitting the data with a double exponential function are displayed for the adaptation and re-adaptation sessions.

Figure 7.

Progression of Savings as a function of cycle for Experiment 2. (A) Savings (S) was computed as the cumulative percent increment in learning from adaptation, according to equation 2. Shown are the mean ± SE of S for each cycle of the experimental (A₁NA₂-M₁) and the control (A₁NA₂-Sham) group.