Sustained increase in hippocampal sharp-wave ripple activity during slow-wave sleep after learning

Abstract

High-frequency oscillations, known as sharp-wave/ripple (SPW-R) complexes occurring in hippocampus during slow-wave sleep (SWS), have been proposed to promote synaptic plasticity necessary for memory consolidation. We recorded sleep for 3 h after rats were trained on an odor-reward association task. Learning resulted in an increased number SPW-Rs during the first hour of post-learning SWS. The magnitude of ripple events and their duration were also elevated for up to 2 h after the newly formed memory. Rats that did not learn the discrimination during the training session did not show any change in SPW-Rs. Successful retrieval from remote memory was likewise accompanied by an increase in SPW-R density and magnitude, relative to the previously recorded baseline, but the effects were much shorter lasting and did not include increases in ripple duration and amplitude. A short-lasting increase of ripple activity was also observed when rats were rewarded for performing a motor component of the task only. There were no increases in ripple activity after habituation to the experimental environment. These experiments show that the characteristics of hippocampal high-frequency oscillations during SWS are affected by prior behavioral experience. Associative learning induces robust and sustained (up to 2 h) changes in several SPW-R characteristics, while after retrieval from remote memory or performance of a well-trained procedural aspect of the task, only transient changes in ripple density were induced.Hippocampal neural activity during sleep has been hypothesized to play a critical role in memory consolidation (Buzsaki 1989(Buzsaki , 1996Pennartz et al. 2002;Born et al. 2006). Sharp-wave/ripple complexes (SPW-Rs), first described a quarter of a century ago (Buzsaki et al. 1983), are associated with a synchronous discharge of a large neuronal population in multiple hippocampal sites (Buzsaki et al. 1983;Suzuki and Smith 1985;Buzsaki 1986). Buzsaki (1989) suggested that the SPW-R bursts are initiated by neurons whose recurrent connectivity had been transiently potentiated during the preceding awake experience. The fact that only a small and select subpopulation of pyramidal cells fire during successive SPW-Rs indicates experience-specific modulation of neuronal connectivity during the SPW-R (Buzsaki 1996). SPW-Rs are present mainly during SWS but also occur during behaviors not associated with theta rhythm like eating, drinking, grooming, and drowsiness (Buzsaki et al. 1983;Suzuki and Smith 1985;Buzsaki 1986). This supports the notion that SPW-R activity provides a substrate for off-line memory consolidation during behavioral states not associated with new information processing. Slow-wave sleep (SWS) is of particular interest because learning-associated changes in cortical spindle activity during SWS are well documented both in humans (Meier-Koll et al. 1999;Fogel et al. 2002;Gais et al. 2002;Clemens et al. 2005) and recently in rats (Eschenko et al. 2006). Moreover, hippocampal ripples and cortical spindles tend to group...

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