Novel experience induces persistent sleep-dependent plasticity in the cortex but not in the hippocampus

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.

Schema-conformant memories are preferentially consolidated during REM sleep

“…The association of REM sleep, rather than SWS, with rapidly-consolidated schema-conformant memories found in our data, suggests that the mPFC intracortical strengthening may occur during REM sleep rather than SWS. Support for this idea comes from research on immediate early genes in which the zif268 gene has been found to be associated with learning during and subsequent upregulation at night specifically during REM sleep, and outside of the MTL (Ribeiro, 1999;Ribeiro et al, 2002Ribeiro et al, , 2007. In a follow-up to their original schema study, Tse et al (2011) found that zif268 was upregulated in the mPFC, and most strongly for rats which had learned new flavour-location pairs and integrated them rapidly into an existing schema.…”

Slow synaptic dynamics in a network: From exponential to power-law forgetting

“…There has been a great deal of research into the idea that sleep consolidates shortterm memories into long-term ones [56][57][58]; experiments on rats suggest that this transformation occurs via a hippocampus-cortical memory transfer [59]. In the context of our model, this would suggest that competitive mechanisms predominate in the cortex rather than the hippocampus; this idea provides a testable prediction for experiments in vivo.…”

Use of Telemetric EEG in Brain Injury

“…Buzsáki, (1991) elaborated a model of memory trace formation based on neocortical-hippocampal interactions, proposing that during exploratory behavior, information is transmitted from neocortex to hippocampus through fast-firing granule cells projections to a specific population of CA3 pyramidal neurons. In fact, during the acquisition of memories (spatial and episodic), the hippocampus is initially engaged, but later the memory traces are migrated to the neocortex (Ribeiro et al, 2007). Indeed, the immediate early genes expression is upregulated during REM sleep in cortical areas but not in the hippocampus (Ribeiro et al, 2007).…”