Abstract

The extinction of conditioned fear is known to be context-specific and is often considered more contextually bound than the fear memory itself (Bouton, 2004). Yet, recent findings in rodents have challenged the notion that contextual fear retention is initially generalized. The context-specificity of a cued fear memory to the learning context has not been addressed in the human literature largely due to limitations in methodology. Here we adapt a novel technology to test the context-specificity of cued fear conditioning using full immersion 3-D virtual reality (VR). During acquisition training, healthy participants navigated through virtual environments containing dynamic snake and spider conditioned stimuli (CSs), one of which was paired with electrical wrist stimulation. During a 24-h delayed retention test, one group returned to the same context as acquisition training whereas another group experienced the CSs in a novel context. Unconditioned stimulus expectancy ratings were assayed on-line during fear acquisition as an index of contingency awareness. Skin conductance responses time-locked to CS onset were the dependent measure of cued fear, and skin conductance levels during the interstimulus interval were an index of context fear. Findings indicate that early in acquisition training, participants express contingency awareness as well as differential contextual fear, whereas differential cued fear emerged later in acquisition. During the retention test, differential cued fear retention was enhanced in the group who returned to the same context as acquisition training relative to the context shift group. The results extend recent rodent work to illustrate differences in cued and context fear acquisition and the contextual specificity of recent fear memories. Findings support the use of full immersion VR as a novel tool in cognitive neuroscience to bridge rodent models of contextual phenomena underlying human clinical disorders.

Highlights

  • In the emotional learning literature, it is well established that the extinction of conditioned fear to a discrete cue is context-specific

  • Winocur et al (2007) employed a comparative contextual fear and food preference conditioning paradigm by testing rats in a new context or the conditioning context at 1 and 8 days for food preference memory, or 1 and 28 days for fear memory. Responding to both the food and fear cue was context-specific at the short intervals but not at the long intervals. This decrease in the learned response outside of the original context is known as the context shift effect and suggests that both conditioned fear and food preference memory retention is initially context-specific due to the incorporation of background stimulus attributes into the memory (Perkins and Weyant, 1958; McAllister and McAllister, 1963; Feinberg and Riccio, 1990; Zhou and Riccio, 1996; Anderson and Riccio, 2005)

  • Analysis revealed a main effect of conditioned stimulus (CS) Type, F (1, 272) = 33.793, P < 0.001, indicating greater responding to the CS+ across variables, as expected

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Summary

Introduction

In the emotional learning literature, it is well established that the extinction of conditioned fear to a discrete cue is context-specific (for review, see Bouton et al, 2006). Winocur et al (2007) employed a comparative contextual fear and food preference conditioning paradigm by testing rats in a new context or the conditioning context at 1 and 8 days for food preference memory, or 1 and 28 days for fear memory. Responding to both the food and fear cue was context-specific at the short intervals but not at the long intervals. This decrease in the learned response outside of the original context is known as the context shift effect (reviewed in Riccio and Joynes, 2007) and suggests that both conditioned fear and food preference memory retention is initially context-specific due to the incorporation of background stimulus attributes into the memory (Perkins and Weyant, 1958; McAllister and McAllister, 1963; Feinberg and Riccio, 1990; Zhou and Riccio, 1996; Anderson and Riccio, 2005)

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