Abstract

Recent work reveals that the extinction of conditioned fear depends upon the interval between conditioning and extinction. Extinction training that takes place within minutes to hours after fear conditioning fails to produce a long-term extinction memory, a phenomenon known as the immediate extinction deficit (IED). Neurobiological evidence suggests that the IED results from stress-induced dysregulation of prefrontal cortical circuits involved in extinction learning. However, a recent study in humans suggests that an “event boundary” between fear conditioning and extinction protects the conditioning memory from interference by the extinction memory, resulting in high levels of fear during a retrieval test. Here, we contrast these hypotheses in rats by arranging extinction trials to follow conditioning trials with or without an event boundary; in both cases, extinction trials are delivered in proximity to shock-elicited stress. After fear conditioning, rats either received extinction trials 60-sec after the last conditioning trial (continuous, no event boundary) or 15-minutes after conditioning (segmented, a standard “immediate” extinction procedure associated with an event boundary). Both groups of animals showed decreases in conditional freezing to the auditory conditioned stimulus (CS) during extinction and exhibited an equivalent IED relative to non-extinguished controls when tested 48 hours later. Thus, eliminating the event boundary between conditioning and extinction with the continuous extinction procedure did not prevent the IED. These data suggest that the IED is the result of shock-induced stress, rather than boundary-induced reductions in memory interference.

Highlights

  • Traumatic events often result in long-lasting emotional memories that persist for years

  • We have recently shown that fear conditioning is associated with a reduction in the spontaneous firing of infralimbic (IL) cortical neurons involved in extinction learning; systemic propranolol administration eliminates this effect and rescues the IED6

  • To determine if the immediate extinction deficit (IED) is a result of event segmentation we devised an experiment (Fig. 2A) in which extinction sessions were presented continuously with fear conditioning, after a 15 min break, or animals were not extinguished at all immediately following fear conditioning (NO-EXT)

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Summary

Introduction

Traumatic events often result in long-lasting emotional memories that persist for years. Processing, and retrieval, and information that crosses event boundaries is often remembered less well[8,12] To test this hypothesis, Dunsmoor and colleagues[7] examined episodic recall of a fear conditioning episode in healthy humans that underwent an extinction procedure in which there was either no event boundary (a normal 10 second inter-trial interval occurred) or an explicit event boundary (subjects were verbally informed of a 10 second break) separating conditioning and extinction. In contrast with this hypothesis, the results revealed that eliminating the event boundary between conditioning and extinction did not rescue the IED Both the continuous and segmented extinction procedures yielded poor long-term extinction, which was manifest as high levels of conditioned freezing to the auditory conditioned stimulus (CS) that did not differ from non-extinguished controls. The most parsimonious interpretation of these results is that the arousal associated with fear conditioning impedes extinction procedures that occur within hours after conditioning

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