Sleep transforms the cerebral trace of declarative memories

Abstract

After encoding, memory traces are initially fragile and have to be reinforced to become permanent. The initial steps of this process occur at a cellular level within minutes or hours. Besides this rapid synaptic consolidation, systems consolidation occurs within a time frame of days to years. For declarative memory, the latter is presumed to rely on an interaction between different brain regions, in particular the hippocampus and the medial prefrontal cortex (mPFC). Specifically, sleep has been proposed to provide a setting that supports such systems consolidation processes, leading to a transfer and perhaps transformation of memories. Using functional MRI, we show that postlearning sleep enhances hippocampal responses during recall of word pairs 48 h after learning, indicating intrahippocampal memory processing during sleep. At the same time, sleep induces a memory-related functional connectivity between the hippocampus and the mPFC. Six months after learning, memories activated the mPFC more strongly when they were encoded before sleep, showing that sleep leads to longlasting changes in the representation of memories on a systems level.fMRI ͉ hippocampus ͉ medial prefrontal cortex ͉ memory N ew memories must undergo a period of consolidation to become stable and immune to interference (1). Consolidation occurs in the form of molecular processes at individual synapses (2) but also in the form of systems consolidation, which is a reorganization of the memory trace within different brain systems (3)(4)(5). This is most obvious for declarative memory, where recall initially depends on the hippocampus, but after some time becomes hippocampus-independent (6-8). Instead, neocortical areas, especially the medial prefrontal cortex (mPFC), are assumed to take over its function (9,10). In a recent functional imaging study, Takashima et al. (11) showed that both regions display opposite activity over the course of 3 months; whereas the hippocampal contribution to memory recall decreases with time, the prefrontal one rises.During the last few years, an important contribution of sleep to memory consolidation has been revealed (12, 13). Sleep prevents forgetting and makes memories resistant to interference, especially when it closely follows learning (14, 15). In particular, animal research has shown that sleep provides the conditions for a hippocampal-neocortical dialogue and information transfer (16,17). Low levels of cholinergic neuromodulation disinhibit hippocampal-neocortical feedback synapses (18), and hippocampus and neocortex show synchronous activity during sleep (19). Together, these findings support the idea that sleep modifies the trace of a recently stored memory. In the present experiment, we tested this hypothesis using functional MRI (fMRI) to characterize brain activity related to free recall immediately, 48 h, and 6 months after learning a declarative memory task. The contribution of sleep to systems memory consolidation was tested by allowing subjects to sleep or by sleep depriving them during the first ...

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