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Comparative Study
. 2006 Dec 13;26(50):12914-20.
doi: 10.1523/JNEUROSCI.3175-06.2006.

Elevated sleep spindle density after learning or after retrieval in rats

Oxana Eschenko  1 , Matthias Mölle, Jan Born, Susan J Sara
Affiliations
Comparative Study

Elevated sleep spindle density after learning or after retrieval in rats

Oxana Eschenko et al. J Neurosci. .

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 (<1 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 (approximately 25%) and the time window of maximal effect (approximately 1 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.

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Figures

Figure 1.
Figure 1.
Spindle density across 2 h of recording before and after learning of a digging (top) or nose-poke (bottom) odor–reward association task. The time from SWS onset is indicated. Bars represent an average spindle density for consecutive 30 min time intervals. Open bars, Baseline recording; hatched bars, postlearning recording. *p < 0.05, **p < 0.01 for between-condition orthogonal comparisons (Newman–Keuls test).
Figure 2.
Figure 2.
Spindle density (mean ± SEM) as a function of the type of memory manipulation (experiment 2, new vs old memory). Bars represent average spindle density during the first hour after SWS onset. Open bars, Baseline (nonmanipulated) sleep recording for all groups; hatched bars, repeated sleep recording. Control, Baseline (nonlearning) recordings on 2 successive days; Learning, baseline (open bar), then sleep after exposure to a new learning situation for the first time; Retrieval, baseline (open bar), then sleep after a new exposure to the learning situation several days after the initial learning. *p < 0.05, **p < 0.01 for within-group comparisons; ##p < 0.01 comparison with the control group.
Figure 3.
Figure 3.
Spindle density (mean ± SEM) after multiple exposure to different learning situations (experiment 3, content of memory manipulation). Top, Bars represent average spindle density during the first hour after SWS onset during four test situations presented in a daily sequence, as follows: Baseline; Learning, sleep after exposure to a new learning situation for the first time; Retrieval, sleep after repeated exposure to the identical learning situation; Extinction, sleep after exposure to the learning context with no reward. *p < 0.05, **p < 0.01 for comparison with the baseline. Bottom, Dots represent the percentage of baseline increases for each individual observation. Note that spindle numbers after retrieval and extinction did not differ from those after learning (p > 0.05).
Figure 4.
Figure 4.
Average spindle density during the first hour after SWS onset during baseline (nonmanipulated; open bar) sleep recording and after a 10 min exploration of a novel environment with freely distributed reward (hatched bars) on a following day. Note that there was no elevated spindle density observed after a simple exploration of a novel situation not requiring odor–reward association. Bars represent mean ± SEM.
Figure 5.
Figure 5.
Individual variability of learning-induced elevated spindle density in rats (top; data from experiment 1) and humans (bottom) after a paired-association task. Bars represent the percentage of baseline change for each individual rat or human subject. Human data are modified from Gais et al. (2002).
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