Abstract
Episodic and spatial memories engage the hippocampus during acquisition but migrate to the cerebral cortex over time. We have recently proposed that the interplay between slow-wave (SWS) and rapid eye movement (REM) sleep propagates recent synaptic changes from the hippocampus to the cortex. To test this theory, we jointly assessed extracellular neuronal activity, local field potentials (LFP), and expression levels of plasticity-related immediate-early genes (IEG) arc and zif-268 in rats exposed to novel spatio-tactile experience. Post-experience firing rate increases were strongest in SWS and lasted much longer in the cortex (hours) than in the hippocampus (minutes). During REM sleep, firing rates showed strong temporal dependence across brain areas: cortical activation during experience predicted hippocampal activity in the first post-experience hour, while hippocampal activation during experience predicted cortical activity in the third post-experience hour. Four hours after experience, IEG expression was specifically upregulated during REM sleep in the cortex, but not in the hippocampus. Arc gene expression in the cortex was proportional to LFP amplitude in the spindle-range (10–14 Hz) but not to firing rates, as expected from signals more related to dendritic input than to somatic output. The results indicate that hippocampo-cortical activation during waking is followed by multiple waves of cortical plasticity as full sleep cycles recur. The absence of equivalent changes in the hippocampus may explain its mnemonic disengagement over time.
Highlights
Memory consolidation requires two consecutive and distinct steps: neural reactivation for short-term recall and synaptic remodeling for long-term storage (Hebb, 1949)
Based on the fact that long-term potentiation induction in the hippocampus during waking (WK) leads to zif-268 gene upregulation in the cortex during subsequent rapid eye movement (REM) sleep (Ribeiro et al, 2002), that such upregulation requires concomitant hippocampal activity (Ribeiro et al, 2002), and that it progresses over time in an anterograde manner across specific cortical areas (Ribeiro et al, 2002), we proposed that REM sleep is a privileged window for the propagation of memory traces from the hippocampus to the cerebral cortex (Pavlides and Ribeiro, 2003; Ribeiro and Nicolelis, 2004; Ribeiro et al, 2002)
To the extent that principal neurons with excitatory function tend to fire less than inhibitory interneurons (Swadlow, 2003), and since our electrode implants were aimed at pyramidal layers in the hippocampus (CA1 field) and cerebral cortex, the results suggest that most of the recorded units were principal neurons
Summary
Memory consolidation requires two consecutive and distinct steps: neural reactivation for short-term recall and synaptic remodeling for long-term storage (Hebb, 1949). Hippocampo-cortical reactivation during slow-wave sleep (SWS) (Pavlides and Winson, 1989; Peigneux et al, 2004; Ribeiro et al, 2004; Wilson and McNaughton, 1994) and upregulation during rapid eye movement (REM) sleep of calcium-dependent gene zif-268 (Ribeiro et al, 1999, 2002), a transcription factor (Wisden et al, 1990) with anterograde effects (Petersohn et al, 1995; Thiel et al, 1994) required for the consolidation of several kinds of memory (Bozon et al, 2003; Jones et al., 2001), suggest that the two major sleep states perform complementary mnemonic functions: neural reactivation during SWS and transcriptional storage during REM sleep (Ribeiro and Nicolelis, 2004; Ribeiro et al, 2004) In support of this view, it has recently been shown (Ulloor and Datta, 2005) that post-training REM sleep is associated with increased levels of the activity-regulated cytoskeleton-associated protein (Arc), a calcium-dependent immediate early gene (IEG) directly involved in synaptic remodeling (Guzowski et al, 2000; Lyford et al, 1995). The mechanisms relating neural activity and IEG expression during sleep remain uncharted, and the model does not take into account the short intermediate sleep (IS) between SWS and REM sleep, a distinct state (Gottesmann, 1996)
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