Date Published: January 17, 2019
Publisher: Public Library of Science
Author(s): Ella Gabitov, Arnaud Boutin, Basile Pinsard, Nitzan Censor, Stuart M. Fogel, Geneviève Albouy, Bradley R. King, Julie Carrier, Leonardo G. Cohen, Avi Karni, Julien Doyon, Dhakshin Ramanathan.
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.
The traditional consolidation hypothesis posits that new memories are initially labile and susceptible to interference, but become stable in the long term through a protein-synthesis-dependent process known as “consolidation” [1–3]. In the late 1960s, this view, however, was challenged due to evidence that, in rats, electroconvulsive shock induced loss of previously consolidated memory, but only if animals were exposed to a “reminder cue” . Over the last two decades, similar loss of consolidated memory has been repeatedly demonstrated using, initially, pharmacological and, lately, behavioral interference in close temporal proximity to memory retrieval [5–15], but see . Thus upon retrieval, consolidated memories are reactivated and may return to a labile state becoming, once again, susceptible to interference. Crucially, interference procedures after memory retrieval have been shown to be effective only if they were administered within a limited time-window, that is when memories were still “active”. These findings were interpreted as support to the reconsolidation hypothesis, which postulates that memory retrieval can lead to memory destabilization, thereby necessitating another consolidation-like period of protein-synthesis-dependent stabilization, called “reconsolidation” . Extending the reconsolidation explanation to memory enhancement, it has been proposed that the post-retrieval restabilization time-window constitutes a unique opportunity for potential adaptive memory modification . Importantly, the underlying mechanisms of memory strength modification implied by reconsolidation are separate from those of memory acquisition and consolidation [19,20].
The main goal of our study was to examine the necessity of memory retrieval to induce a deficit in a pre-established procedural (“how to”) motor memory in humans . To this end, we used a 3-day motor sequence learning paradigm which consisted of an initial training on Day 1, an interference training on Day 2, preceded or not by the actual task-based retrieval of the initially trained sequence, and a final test session on Day 3. Our results suggest that susceptibility of consolidated motor memory to behavioral interference is independent of its active task-based retrieval. Since active task-based retrieval is the most adequate mechanism to reactivate memories , the impairment of the pre-established motor skill in the absence of its retrieval challenges the reconsolidation view that considers memory reactivation as a necessary condition for susceptibility of consolidated memory to changes [5,6,9,19].