Effects of sleep on memory for conditioned fear and fear extinction

Abstract

Learning and memory for extinction of conditioned fear is a basic mammalian mechanism for regulating negative emotion. Sleep promotes both the consolidation of memory and the regulation of emotion. Sleep can influence consolidation and modification of memories associated with both fear and its extinction. After brief overviews of the behavior and neural circuitry associated with fear conditioning, extinction learning, and extinction memory in the rodent and human, interactions of sleep with these processes will be examined. Animal and human studies suggest that sleep can serve to consolidate both fear and extinction memory. In humans, sleep also promotes generalization of extinction memory. Time-of-day effects on extinction learning and generalization are also seen. Rapid eye movement (REM) may be a sleep stage of particular importance for the consolidation of both fear and extinction memory as evidenced by selective REM deprivation experiments. REM sleep is accompanied by selective activation of the same limbic structures implicated in the learning and memory of fear and extinction. Preliminary evidence also suggests extinction learning can take place during slow wave sleep. Study of low-level processes such as conditioning, extinction, and habituation may allow sleep effects on emotional memory to be identified and inform study of sleep's effects on more complex, emotionally salient declarative memories. Anxiety disorders are marked by impairments of both sleep and extinction memory. Improving sleep quality may ameliorate anxiety disorders by strengthening naturally acquired extinction. Strategically timed sleep may be used to enhance treatment of anxiety by strengthening therapeutic extinction learned via exposure therapy. (PsycINFO Database Record

(c) 2015 APA, all rights reserved).

Figures

Figure 1

Neural circuits associated with expression of conditioned fear and fear extinction memory overlap with limbic areas that reactivate during REM sleep from quiescence state in NREM sleep. (A) fear expression network (B) fear extinction network. (C) anterior paralimbic REM activation area. Hipp, hippocampus; vmPFC, ventromedial prefrontal cortex; dACC, dorsal anterior cingulate cortex; a, amygdala.

Figure 2

Intervening sleep promoted generalization of extinction of conditioned fear in comparison of two groups: Wake (trained in the morning and tested in the evening, upper panels) and Sleep (trained in the evening and tested in the morning, lower panels). A. Average trial by trial SCR during Fear Conditioning and Extinction Learning. There were no differences between the Sleep and Wake group. B. Schematic of the acquisition of conditioned fear (upper panel) and extinction learning (lower panel). Note that although acquisition of fear is schematically depicted as an ascending curve, actual SCR responses in humans tend to decrease across conditioning trials. C. Average trial by trial SCR to the extinguished (CS+E) and un-extinguished (CS+U) CS+ in the two groups during each trial of the Extinction Recall phase occurring 12 hours after Fear Conditioning and Extinction Learning phases. D. Schematic interpretation of results in C., i.e., because groups did not initially differ (A.), sleep promoted generalization of extinction learning. μS1/2, square-root transformed SCR in micro-Siemens,** p

Figure 3

Fear conditioning did not differ between morning and evening (A) whereas extinction was significantly better learned in the morning (B). Extinction Recall in the morning showed generalization of extinction memory (C) whereas recall in the evening preserved the differentiation of the extinguished and unextinguished CS+ and favored expression of a greater overall degree of conditioned fear (D). Significance indicated for the Morning vs. Evening and CS+E vs. CS+U main effect (large asterisks) and trial-by-trial differences (small asterisks). SCR½d: differential SCR, * p

Figure 4

Superior retention and generalization of extinction memory across sleep versus wakefulness during simulated exposure therapy for spider phobia. A. Experimental design showing putative learning and memory processes taking place between phases. B. Summed Disgust, Fear and Unpleasantness ratings. C. SCR in response to spider video. Note that extinction generalization in the Sleep group prevented sensitization to a novel spider video. Control groups tested following wakefulness entirely in the morning or evening (right panel of each graph) show no differences in extinction retention and generalization; a finding inconsistent with a circadian explanation of the sleep-wake differences. Bars are the standard error of the mean for groups computed by mixed ANOVA. † p 1/2 square-root transformed SCR in micro-Siemens.