Abstract
Much remains to be discovered about the fate of recent memories in the human brain. Several studies have reported the reactivation of learning-related cerebral activity during post-training sleep, suggesting that sleep plays a role in the offline processing and consolidation of memory. However, little is known about how new information is maintained and processed during post-training wakefulness before sleep, while the brain is actively engaged in other cognitive activities. We show, using functional magnetic resonance imaging, that brain activity elicited during a new learning episode modulates brain responses to an unrelated cognitive task, during the waking period following the end of training. This post-training activity evolves in learning-related cerebral structures, in which functional connections with other brain regions are gradually established or reinforced. It also correlates with behavioral performance. These processes follow a different time course for hippocampus-dependent and hippocampus-independent memories. Our experimental approach allowed the characterization of the offline evolution of the cerebral correlates of recent memories, without the confounding effect of concurrent practice of the learned material. Results indicate that the human brain has already extensively processed recent memories during the first hours of post-training wakefulness, even when simultaneously coping with unrelated cognitive demands.
Highlights
Human [1,2,3,4] and animal [5,6,7,8,9] studies have revealed experience-dependent reactivations of regional cerebral activity during post-training sleep, in brain areas previously engaged in learning during wakefulness
One cannot rule out the possibility that the five tests performed at the end of the learning session provided participants with feedback that partially contributed to the limited improvement in performance after the 1h interval
We show that post-learning persistence and early reorganization of neuronal activity during wakefulness is a common feature both for hippocampus-independent and hippocampus-dependent memories, but with different time courses
Summary
Human [1,2,3,4] and animal [5,6,7,8,9] studies have revealed experience-dependent reactivations of regional cerebral activity during post-training sleep, in brain areas previously engaged in learning during wakefulness. Using this within-subject strategy, post-training changes in regional brain activity related to the spatial memory task could be controlled for post-training activity modifications related to the motor procedural task, and vice-versa This unique experimental design allowed the characterization during active wakefulness of (a) the offline modulation of regional brain responses to the probe task by recent learning in the human brain, (b) the specificity of this modulation to the type of prior learning (i.e. spatial versus procedural), and (c) the evolution of these learning-related modulations at two different post-training time intervals, immediately and 45 min after training had ended.
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