Susceptibility of consolidated procedural memory to interference is independent of its active task-based retrieval

Abstract

Reconsolidation theory posits that upon retrieval, consolidated memories are destabilized and need to be restabilized in order to persist. It has been suggested that experience with a competitive task immediately after memory retrieval may interrupt these restabilization processes leading to memory loss. Indeed, using a motor sequence learning paradigm, we have recently shown that, in humans, interference training immediately after active task-based retrieval of the consolidated motor sequence knowledge may negatively affect its performance levels. Assessing changes in tapping pattern before and after interference training, we also demonstrated that this performance deficit more likely indicates a genuine memory loss rather than an initial failure of memory retrieval. Here, applying a similar approach, we tested the necessity of the hypothetical retrieval-induced destabilization of motor memory to allow its impairment. The impact of memory retrieval on performance of a new motor sequence knowledge acquired during the interference training was also evaluated. Similar to the immediate post-retrieval interference, interference training alone without the preceding active task-based memory retrieval was also associated with impairment of the pre-established motor sequence memory. Performance levels of the sequence trained during the interference training, on the other hand, were impaired only if this training was given immediately after memory retrieval. Noteworthy, an 8-hour interval between memory retrieval and interference allowed to express intact performance levels for both sequences. The current results suggest that susceptibility of the consolidated motor memory to behavioral interference is independent of its active task-based retrieval. Differential effects of memory retrieval on performance levels of the new motor sequence encoded during the interference training further suggests that memory retrieval may influence the way new information is stored by facilitating its integration within the retrieved memory trace. Thus, impairment of the pre-established motor memory may reflect interference from a competing memory trace rather than involve interruption of reconsolidation.

Fig 1. Study design.

(A) sequential finger tapping task. A sequence initially trained on the Day 1 (T-Seq, left panel) and a novel sequence used during the interference training on Day 2 (Int-Seq, right panel). The two sequences were matched for number of movements per digit and mirror-reversed in relation to each other (in terms of order). (B) Experimental groups. On Day 1 all groups underwent training on the T-Seq consisted of 14 performance blocks. On Day 2 the memory for the T-Seq was retrieved (or not) using one performance block and the interference training on the novel Int-Seq was conducted according to the experimental group (NoReInt, ReInt and Re8hInt). On Day 3 the performance levels for the T-Seq were tested in all groups using 7 performance blocks; the performance for the Int-Seq was subsequently tested as well. In all sessions performance blocks consisted of 60 key-presses, equivalent to 12 possible sequences, and were separated by 25-second periods of rest.

Fig 2. Performance rate.

Time (i.e., duration) to complete the last 30 key-presses for each performance block during the training (Day 1), retrieval (Day 2) and test (Day 3) of the trained sequence (T-Seq, filled markers) as well as during the training (Day 2) and test (Day 3) of the interference sequence (Int-Seq, empty markers) is plotted for the NoReInt, ReInt and Re8hInt group (blue, magenta and yellow markers, respectively). Last training blocks, the retrieval block and first test blocks are time-points of interest (End-T, Retrieval and Test respectively). Bars–standard error of the mean (s.e.m.).

Fig 3. Experience-driven changes in tapping patterns.

(A) Changes in tapping pattern, i.e., pattern of inter-key press intervals, from the first to the last block during the initial training on Day 1 and interference training on Day 2 (upper and lower plot respectively) are shown for one representative subject. Each point represents mean duration for each of 4 possible transitions between successive elements within a sequence (from 1st to 4th) plus an additional transition between the sequences (between) for each block. Thus, shape of each line depicts a tapping pattern for a single block. With practice, tapping pattern progressively became more similar to the tapping pattern generated during the last training block (red line). Note that changes in tapping pattern (i.e., line shape) do not directly reflect changes in performance rate. (B) Degree of similarity between tapping patterns was assessed based on normalized Pearson correlation coefficients using the Fisher’s z-transformation. Group average of individual normalized Pearson correlation coefficients between tapping patterns formed by the end of training (i.e., during the last training block) and each block during the training (training blocks 1–13) and test (test blocks 1–7) are shown for each sequence (T-Seq, upper plots; Int-Seq, lower plots). Bars–standard error of the mean (s.e.m.). *–significant results at .05 level, #–significant results at .01 level, n.s.–no significant differences.

Fig 4. The effect of memory retrieval on performance rate.

(A) Time to complete the last 30 key-presses during the last training block, the retrieval block and the first test block (End-T, Retrieval and Test respectively) is plotted for each group (NoReInt, ReInt and Re8hInt with blue, magenta and yellow markers respectively) and each sequence (T-Seq, filled markers upper plot; Int-Seq, empty markers lower plot). (B) Gains in performance, normalized to the last training block, that developed during the post-training interval for each sequence (i.e., between the end of training on Day 1 (T-Seq) or on Day 2 (Int-Seq) and the corresponding test session on Day 3; Post-T Gains) averaged across participants of each group (upper plot). Positive values correspond to faster performance by Day 3 than by the end of training. Individual Post-T Gains for the T-Seq (x axis) plotted against Post-T Gains for the Int-Seq (y axis) (lower plots). Bars–standard error of the mean (s.e.m.). *–significant results at .05 level, #–significant results at .01 level, n.s.–no significant differences. Note that in the ReInt group, regression analysis did not result in significant correlation even after excluding two participants with extremely negative values.

Fig 5. Changes in tapping patterns during test.

Degree of similarity between tapping patterns, i.e., patterns of inter-key press intervals, was assessed based on normalized Pearson correlation coefficients calculated for each individual using the Fisher’s z-transformation. Mean normalized Pearson correlation coefficients between tapping patterns for the first test block and during the subsequent repeated practice (i.e., test blocks 2–7) for each group and each sequence (T-Seq, upper plots; Int-Seq, lower plots). Bars–standard error of the mean (s.e.m.). #–significant results at .01 level.