Revealing context-specific conditioned fear memories with full immersion virtual reality

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.

Keywords: contextual fear; fear conditioning; hippocampus; memory retention; virtual reality.

Figure 1

Schematic of the control room and Duke’s immersive virtual environment (DiVE) with a human participant viewing a virtual scene.

Figure 2

Time line of fear conditioning and retention testing. Participants were seated in the DiVE during habituation/acquisition and extinction sessions on two consecutive days. Conditioned Stimuli (CS+) and (CS−) indicate the phasic reinforced and non-reinforced snake and spider images. The unconditioned stimulus (US), mild wrist shock, was paired with the CS+ on 40% of acquisition trials. Participants were tested in either the same or a different VR context (bottom panel) on the following day during extinction trials to measure fear retention.

Figure 3

Fear acquisition results. Data depict mean values (±SEM) across the three dependent measures all normalized to the maximum response on Day 1 when the differential fear contingency is initially learned. In early acquisition, differential fear is reflected in US Expectancy ratings (Top Panel) and Context Fear (mean skin conductance level during the interstimulus interval; Middle panel). Differential Cued Fear (skin conductance response to the CS+ relative to the CS−) emerges in late acquisition (Bottom Panel). *P < 0.01. SCR = skin conductance response.

Figure 4

Fear retention results. Data depict mean values (±SEM) across Contextually cued, Cued, and Context Fear measurements on Day 2 during retention testing trials. Data are normalized to the maximum response on Day 2. Fear was specified to the CS+ (relative to the CS−) in the Same Context group only, indicating significant contextually cued fear retention, *P < 0.001. These group differences were not due to differences in baseline Context Fear expressed during the interstimulus interval. SCR = skin conductance response.