Working memory and fear conditioning

Abstract

Previous studies of associative learning implicate higher-level cognitive processes in some forms of classical conditioning. An ongoing debate is concerned with the extent to which attention and awareness are necessary for trace but not delay eye-blink conditioning [Clark, R. E. & Squire, L. R. (1998) Science 280, 77-81; Lovibond, P. F. & Shanks, D. (2002) J. Exp. Psychol. Anim. Behav. Processes 28, 38-42]. In trace conditioning, a short interval is interposed between the termination of the conditioned stimulus (CS) and the onset of the unconditioned stimulus (US). In delay conditioning, the CS and US overlap. We here investigate the extent to which human classical fear conditioning depends on working memory. Subjects had to carry out an n-back task, requiring tracking an item 1 or 2 back in a sequentially presented list of numbers, while simultaneously being tested for their ability to associate auditory cues with shocks under a variety of conditions (single-cue versus differential; delay versus trace; no task versus 0-, 1-, and 2-back). Differential delay conditioning proved to be more resilient than differential trace conditioning but does show a reduction due to task interference similar in slope to that found in trace conditioning. Explicit knowledge of the stimulus contingency facilitates but does not guarantee trace conditioning. Only the single-cue delay protocol shows conditioning during the more difficult working memory task. Our findings suggest that the larger the cognitive demands on the system, the less likely conditioning occurs. A postexperimental questionnaire showed a positive correlation between conditioning and awareness for differential trace conditioning extinction.

Figure 1

(A) Delay conditioning consisted of a 0.25-sec-long electric shock that overlapped and coterminated with the 1-sec-long CS⁺ (tone or noise). In trace conditioning, the CS⁺ was followed 3 sec later by the US. (B) The conditioning protocol consisted of three phases: habituation, acquisition, and extinction. (C) Distraction tasks and conditioning procedures were performed concurrently. During a 0-back task, the subject pressed a key (marked by an X) whenever a predetermined number appeared (4 in this case). During a 1- or 2-back task, the subject pressed a key whenever the number matched the one before it or the one before the previous one, respectively.

Figure 2

Mean range-corrected SCRs to CS presentations for each trial. Thirty-six subjects (six per group) participated in either the differential delay (A, C, or E) or trace (B, D, or F) learning procedure without any task or while being distracted by a 1- or a 2-back task. Mean range-corrected SCRs to CS⁺ are shown in solid lines with cross markers. Mean range-corrected SCRs to CS⁻ are indicated by dashed lines with circles. Significant conditioning exists during the delay procedure with no concurrent task and while performing the 1-back task. Only under the no-task condition did we find significant trace conditioning. The vertical line marks the last test trial during the acquisition phase.

Figure 3

Scatter plot of mean range-corrected differences between CS⁺ and CS⁻ and the subject's awareness index. During differential trace extinction (Fig. 2 B, D, and F; trials 5–16), subjects show a linearly increasing relationship between average amplitude of response difference and postexperimental questionnaire score (adjusted r² = 0.334, Pearson coefficient = 0.611, P < 0.01, n = 18). Subjects show no significant correlation between conditioning (average range-corrected CS⁺ to CS⁻) and awareness index during differential trace acquisition, differential delay acquisition, or differential delay extinction.

Figure 4

Mean range-corrected SCRs to CS presentations for each trial. Sixteen subjects (four per group) participated in either single-cue delay (A or C) or trace (B or D) conditioning without any distraction or while carrying out a 2-back task. Mean range-corrected SCRs to CS⁺ are shown in solid lines with cross markers. Mean range-corrected SCRs to marked phantom CS⁻ time points are indicated by dashed lines with circles. Significant conditioning exists for delay conditioning with no concurrent task and while performing the 2-back task. Significant trace conditioning is present only while no task is performed. The vertical line marks the last test trial presented during acquisition.

Figure 5

Mean range-corrected SCRs to CS presentations for each trial. Sixteen subjects (four per group) participated in either informed or uninformed single-cue trace conditioning without being distracted (no task) or while carrying out a 0- or a 2-back task. Mean range-corrected SCRs to CS⁺ are shown in solid lines with cross markers. Mean range-corrected SCRs to marked phantom CS⁻ time points are indicated by dashed lines with circles. Significant conditioning is present for informed trace conditioning while subjects performed no task or a 0-back task. Significant uninformed trace conditioning is present only without a concurrent task (Fig. 2B). The vertical line marks the last test trial presented during acquisition.

Figure 6

Summary of our data plotted in a 3D space capturing the contingencies of our protocol. The vertical axis marks the group average for each subject's average range-corrected and normalized CS⁺/CS⁻ difference. The horizontal axis marks the task difficulty. The axis into the plane of the paper marks the group as trace or delay using the difference in CS/US onset (stimulus onset asynchrony, SOA) in seconds. In addition, the line for trace is hatched, whereas the line for the delay group is solid. **, significant conditioning at P < 0.01. Areas of the lines that are not filled in are meant to assist the stability of the figure, not to imply any prediction about the magnitude of conditioning in that area. (A) Mean group differences for differential subjects. (B) Mean group differences for uninformed single-cue subjects. (C) Mean group differences for single-cue informed subjects. Our results indicate the higher the cognitive load, the smaller the CS⁺/CS⁻ difference.