Slow-Wave Sleep-Imposed Replay Modulates Both Strength and Precision of Memory

Abstract

Odor perception is hypothesized to be an experience-dependent process involving the encoding of odor objects by distributed olfactory cortical ensembles. Olfactory cortical neurons coactivated by a specific pattern of odorant evoked input become linked through association fiber synaptic plasticity, creating a template of the familiar odor. In this way, experience and memory play an important role in odor perception and discrimination. In other systems, memory consolidation occurs partially via slow-wave sleep (SWS)-dependent replay of activity patterns originally evoked during waking. SWS is ideal for replay given hyporesponsive sensory systems, and thus reduced interference. Here, using artificial patterns of olfactory bulb stimulation in a fear conditioning procedure in the rat, we tested the effects of imposed post-training replay during SWS and waking on strength and precision of pattern memory. The results show that imposed replay during post-training SWS enhanced the subsequent strength of memory, whereas the identical replay during waking induced extinction. The magnitude of this enhancement was dependent on the timing of imposed replay relative to cortical sharp-waves. Imposed SWS replay of stimuli, which differed from the conditioned stimulus, did not affect conditioned stimulus memory strength but induced generalization of the fear memory to novel artificial patterns. Finally, post-training disruption of piriform cortex intracortical association fiber synapses, hypothesized to be critical for experience-dependent odor coding, also impaired subsequent memory precision but not strength. These results suggest that SWS replay in the olfactory cortex enhances memory consolidation, and that memory precision is dependent on the fidelity of that replay.

Slow Oscillations during Sleep Coordinate Interregional Communication in Cortical Networks

“…The existence of two types of spindles, fast and slow, with different spatial topographies has been demonstrated repeatedly (Zeitlhofer et al, 1997;Andrillon et al, 2011). Interestingly, slow and fast spindles express distinct temporal relations with SOs .…”

“…Intriguingly, SO modulations have been related to prior daytime learning Mölle et al, 2004Mölle et al, , 2009Mölle et al, , 2011, and SOs are causally involved in the offline reprocessing and stabilization of memories (Marshall et al, 2006;Antonenko et al, 2013;Ngo et al, 2013). Such sleep-related memory stabilization is widely held to involve the reactivation of memory traces in hippocampo-neocortical networks, leading to the formation of hippocampus-independent links between cortically distributed memory representations (Marr, 1971;Frankland and Bontempi, 2005).…”

Olfactory Aversive Conditioning during Sleep Reduces Cigarette-Smoking Behavior

“…In addition, extinction of olfactory contextual fear conditioning was greater when reexposure to the odorant context occurred during sleep compared with wakefulness (Hauner et al, 2013). Moreover, consolidation of emotional memories, though not neutral memories, is more enhanced during sleep than during wakefulness (Hu et al, 2006;Wagner et al, 2006;Payne et al, 2008;Baran et al, 2012). Finally, memory reactivation during sleep both strengthened and linked categorically related memories together, while equivalent wake reactivation only strengthened individual memories (Oudiette et al, 2013).…”

The Consolidation and Transformation of Memory

“…Also, reactivating conditioned fear memories during SWS in humans by presenting the conditioned stimulus alone, in the absence of the aversive unconditioned stimulus, induced an extinction-like effect (He et al, 2015;Hauner et al, 2013). However, two rodent studies that cued fear memories during SWS by repeatedly presenting the conditioned stimulus, found the opposite, i.e., strengthening of the originally learnt fear memory (Rolls et al, 2013;Barnes and Wilson, 2014). All in all, whether memory consolidation during sleep represents unsupervised learning (Margoliash and Schmidt, 2010) or a process whose efficacy critically depends on evaluative feedback mechanism, remains an open question.…”