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Persistence of Hippocampal and Striatal Multivoxel Patterns during Awake Rest after Motor Sequence Learning

Publication date: 2022-05-03

Author:

King, Bradley
Gann, Mareike ; Mantini, Dante ; Doyon, Julien ; Albouy, Geneviève

Abstract:

Memory consolidation is thought to be mediated by the offline reactivation of brain regions recruited during initial learning. Evidence for hippocampal reactivation in humans comes from studies showing that hippocampal response patterns elicited during learning can persist into subsequent rest intervals. Such investigations have largely been limited to declarative memory, which is surprising given the critical role of the hippocampus in motor memory processes. The primary goal of this study was therefore to investigate whether motor learning induces persistence of hippocampal patterns into subsequent rest. Based on their critical roles in motor learning and memory consolidation processes, we also assessed persistence in the striatum and primary motor cortex (M1). Functional magnetic resonance imaging (fMRI) data were recorded during motor learning as well as pre- and post-learning resting periods from 55 young healthy adults (males and females). Patterns of brain responses were assessed with intra- and inter-regional multivoxel correlation structure (MVCS). Intra-regional multivoxel patterns during motor sequence learning within the hippocampus and the striatum – but not within M1 – were more similar to post-learning as compared to pre-learning resting epochs, indicating persistence of task-related patterns thought to reflect reactivation processes. Interestingly, the multivoxel pattern of hippocampal connectivity with the striatum (i.e., inter-regional MVCS) was strongly dissimilar between post-learning rest and task practice. Altogether, these results provide evidence for the persistence of learning-related response patterns within the hippocampus and striatum into rest following motor learning. They also suggest that striatal-hippocampal connectivity patterns elicited by task practice are reorganized in post-learning waking rest.

Significance statement

Memory consolidation, the process by which newly encoded and fragile memories become more robust, is thought to be supported by the reactivation of brain regions - including the hippocampus - during post-learning rest. While hippocampal reactivations have been demonstrated in humans in the declarative memory domain, it remains unknown whether such a process takes place after motor learning. Using functional MRI, we show that patterns of brain activity within both the hippocampus and striatum elicited during motor learning indeed persist into post-learning rest. In contrast, connectivity patterns between the striatum and the hippocampus do not persist but instead are reorganized during post-learning waking rest. These results thus provide novel insights into the reactivation of brain activity after motor sequence learning.