Elevated Sleep Spindle Density after Learning or after Retrieval in Rats

Abstract

Non-rapid eye movement sleep has been strongly implicated in consolidation of both declarative and procedural memory in humans. Elevated sleep-spindle density in slow-wave sleep after learning has been shown recently in humans. It has been proposed that sleep spindles, 12-15 Hz oscillations superimposed on slow waves (Ͻ1 Hz), in concert with high-frequency hippocampal sharp waves/ripples, promote neural plasticity underlying remote memory formation. The present study reports the first indication of learning-associated increase in spindle density in the rat, providing an animal model to study the role of brain oscillations in memory consolidation during sleep. An odor-reward association task, analogous in many respects to human paired-associate learning, is rapidly learned and leads to robust memory in rats. Rats learned the task over 10 massed trials within a single session, and EEG was monitored for 3 h after learning. Learning-induced increase in spindle density is reliably reproduced in rats in two different learning situations, differing primarily in the behavioral component of the task. This increase in spindle density is also present after reactivation of remote memory and in situations when memory update is required; it is not observed after noncontingent exposure to reward and training context. The latter results substantially extend findings in humans. The magnitude of increase (ϳ25%) and the time window of maximal effect (ϳ1 h after sleep onset) were remarkably similar to human data, making this a valid rodent model to study network interactions through the use of simultaneous unit recordings and local field potentials during postlearning sleep.

Sleep spindles are locally modulated by training on a brain–computer interface

“…Increasingly, sleep spindles, one of the most prominent features of NREM, have been implicated in these plastic processes (5,7,8,17,29). It has been postulated that spindles facilitate synaptic plasticity in cortical cells via calcium-dependent mechanisms (11), and it has been shown that cortical stimulation at the spindle frequency increases synaptic plasticity (30).…”

“…This dissociation could provide a window for uninterrupted replay of recently instantiated memories and thus support sleep-dependent memory consolidation. There is now a large body of evidence linking sleep spindles to learning and memory in both humans and animals (5)(6)(7). For example, increases in spindle density have been correlated with learning a declarative memory task (5), with retention of verbal memories (6), and with relevant recall of a remote memory (7).…”

“…There is now a large body of evidence linking sleep spindles to learning and memory in both humans and animals (5)(6)(7). For example, increases in spindle density have been correlated with learning a declarative memory task (5), with retention of verbal memories (6), and with relevant recall of a remote memory (7). Additionally, spindles are correlated with sharp-wave complexes in the hippocampus (8,9) and are associated with storedtrace reactivation in the neocortex (10).…”

Integrated Brain Circuits: Neuron-Astrocyte Interaction in Sleep-Related Rhythmogenesis

“…Given that these hippocampal events include replayed place cell sequential offline firing, and that their activity coincides with cortical UP states, it is thought that they may play an important role in the coordination of corticohippocampal activity necessary for memory consolidation[21]. Additionally, UP states appear to coordinate SWR-spindle events, which occur at an increased incidence after learning, further supporting a role of this rhythm in memory consolidation[64,65]. …”

“…This imposes an inhibitory rhythmic synaptic drive onto thalamocortical cells, which ultimately results in entrainment of the cortex to that rhythm[67]. Work by Sara’s lab has shown that spindle density rises in the cortex as a function of learning, suggesting that this rhythm might be important for off-line memory processing[68]. Interestingly, while slow oscillations and delta oscillations are low-frequency rhythms that are classically thought to promote synaptic depression, a number of experiments support a role for spindle oscillations in the induction of cortical long-term potentiation[69].…”