Hippocampus and striatum: Dynamics and interaction during acquisition and sleep‐related motor sequence memory consolidation

Abstract

While several models of memory consolidation have previously associated hippocampal activity with declarative memory, there is now increasing evidence that the hippocampus also plays a crucial role in procedural memory. Here, we review recent human functional neuroimaging studies demonstrating that the hippocampus is involved in the acquisition and sleep-related consolidation of procedural memories, and motor sequence-based skills in particular. More specifically, we present evidence that hippocampal activity and its functional interactions with other brain structures, particularly competition with the striatum, contribute to initial learning of sequential motor behavior. Interestingly, these early cerebral representations in the hippocampus and striatum, which may interact through the prefrontal cortex, can even predict subsequent sleep-related memory consolidation processes. We propose that sleep can reorganize the activity within, as well as the functional interactions between, these structures, ultimately favoring overnight performance enhancement. Finally, we conclude by offering insights into the respective roles of these structures in procedural memory consolidation processes. We argue that, in the context of motor sequence memory consolidation, the hippocampal system triggers subsequent sleep-dependent performance enhancement whereas the striatal system is involved in the maintenance of the motor behavior over time. V C 2013 Wiley Periodicals, Inc.

Taking the brakes off the learning curve

“…These results are in line with our previous work showing an antagonistic pattern of activation between hippocampo-and striato-cortical networks in which the hippocampus is recruited early on during training, whereas activity in the striatum increases as a function of practice (see Albouy et al 2013a for a review). This suggests that complex plastic phenomena occur within the first 14 blocks of acquisition of an explicit motor task that may condition the way in which the task is subsequently internalized and consolidated.…”

“…Our results show that the hippocampus is significantly recruited already in the first 3 blocks (corresponding on average to the first 2 minutes of task performance, just before an abrupt slowing of the performance), which suggests that it might be responsible for the monitoring and labeling of a repeated movement sequence as a potentially meaningful program to be transferred to other structures for storage later on (Gheysen et al 2010;Albouy et al 2013a;Lohse et al 2014;Davachi and DuBrow 2015). It was also proposed that the hippocampus might be in competition with the striatum (Albouy et al 2008(Albouy et al , 2015Lungu et al 2014) and that both the early recruitment of this structure, as well as the strength of its competitive interaction with the striatum influence subsequent motor memory consolidation (Albouy et al 2008;2013a;Steele and Penhune, 2010). Indeed, significant BOLD signal associated with the error-free repetition of the same motor sequence moved to the cerebello-cortical and striato-cortical circuits towards the end of the practice period, in the third phase.…”

Choose to move: The motivational impact of autonomy support on motor learning

“…A 1-day delay (or more) is typically used in motor learning research to allow for the dissipation of possible temporary and spurious effects of the independent variables on performance (Schmidt & Lee, 2011). Further, this delay may provide an opportunity for memory consolidation through sleep and wakefulness processes and other influences that strengthen motor memory (Albouy, King, Maquet, & Doyon, 2013;Robertson, 2009). Thus, the present findings indicate that providing choices during, or before, practice can have lasting effects on the retention of motor skills.…”

Levels of Interference in Long and Short-Term Memory Differentially Modulate Non-REM and REM Sleep

“…[6][7][8][9][10] Some interpreted these results as the positive evidence of a selective function of sleep in memory consolidation. [11][12][13] Sleep has also been hypothesized to promote forgetting, and in particular adaptive forgetting of undesirable memories, by decreasing synaptic strength created during wakefulness. [14][15][16][17] Forgetting of irrelevant information could thus occur during sleep to promote a more efficient and selective recall of more important information.…”