Post-Learning Sleep Transiently Boosts Context Specific Operant Extinction Memory.

Margarita Borquez,Ennio Vivaldi,María P Contreras,Jan Born,Marion Inostroza

doi:10.3389/fnbeh.2017.00074

Abstract

Operant extinction is learning to supress a previously rewarded behavior. It is known to be strongly associated with the specific context in which it was acquired, which limits the therapeutic use of operant extinction in behavioral treatments, e.g., of addiction. We examined whether sleep influences contextual memory of operant extinction over time, using two different recall tests (Recent and Remote). Rats were trained in an operant conditioning task (lever press) in context A, then underwent extinction training in context B, followed by a 3-h retention period that contained either spontaneous morning sleep, morning sleep deprivation, or spontaneous evening wakefulness. A recall test was performed either immediately after the 3-h experimental retention period (Recent recall) or after 48 h (Remote), in the extinction context B and in a novel context C. The two main findings were: (i) at the Recent recall test, sleep in comparison with sleep deprivation and spontaneous wakefulness enhanced extinction memory but, only in the extinction context B; (ii) at the Remote recall, extinction performance after sleep was enhanced in both contexts B and C to an extent comparable to levels at Recent recall in context B. Interestingly, extinction performance at Remote recall was also improved in the sleep deprivation groups in both contexts, with no difference to performance in the sleep group. Our results suggest that 3 h of post-learning sleep transiently facilitate the context specificity of operant extinction at a Recent recall. However, the improvement and contextual generalization of operant extinction memory observed in the long-term, i.e., after 48 h, does not require immediate post-learning sleep.

Highlights

Sleep has been identified as a state that optimizes the consolidation of newly acquired memory (Born et al, 2006; Ribeiro, 2012)
We examined the effects of post-learning sleep on memory for the extinction of an operant behavior and on the context specificity of this extinction memory in rats using a Recent and a Remote recall test
The two main findings were: (i) At the Recent recall test, sleep compared with wakefulness enhanced the extinction memory but only if recall was tested in the same context as during extinction learning, indicating that 3 h of post-learning sleep enhances a context specific extinction memory; (ii) At the Remote recall test (48 h later), the Sleep group showed—in comparison with Recent recall testing— improved recall of the extinction memory when tested in the novel context, with this improvement reaching a level only slightly lower than that for testing in the extinction context B

Summary

Introduction

Sleep has been identified as a state that optimizes the consolidation of newly acquired memory (Born et al, 2006; Ribeiro, 2012). According to the active systems consolidation view, sleep supports the formation of long-term memories through the repeated reactivation of newly encoded representations occurring during sleep (Dudai, 2004; Diekelmann and Born, 2010). Such reactivations mediate the gradual redistribution of the representation from networks serving as initial store to networks serving as long-term store. Extinction refers to the fact that the operant behavior diminishes when the consequences do not occur on repeated occasions (Skinner, 1953). Context specificity of extinction is the most important limiting factor in the clinical application of extinction-based therapies, e.g., in drug addiction, with frequent relapses once the patient leaves the therapeutic setting

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