Analysis of memory modulation by conditioned stimuli

Abstract

Conditioned stimuli (CS) have multiple psychological functions that can potentially contribute to their effect on memory formation. It is generally believed that CS-induced memory modulation is primarily due to conditioned emotional responses, however, well-learned CSs not only generate the appropriate behavioral and physiological reactions required to best respond to an upcoming unconditioned stimulus (US), but they also serve as signals that the US is about to occur. Therefore, it is possible that CSs can impact memory consolidation even when their ability to elicit conditioned emotional arousal is significantly reduced. To test this, male Sprague-Dawley rats trained on a signaled active avoidance task were divided into "Avoider" and "Non-Avoider" subgroups on the basis of percentage avoidance after 6 d of training. Subgroup differences in responding to the CS complex were maintained during a test carried out in the absence of the US. Moreover, the subgroups displayed significant differences in stress-induced analgesia (hot-plate test) immediately after this test, suggesting significant subgroup differences in conditioned emotionality. Importantly, using the spontaneous object recognition task, it was found that immediate post-sample exposure to the avoidance CS complex had a similar enhancing effect on object memory in the two subgroups. Therefore, to our knowledge, this is the first study to demonstrate that a significant conditioned emotional response is not necessary for the action of a predictive CS on modulation of memory consolidation.

Figure 1.

Experimental design used in Experiments 1 and 2.

Figure 2.

(A–D) Mean (±SEM) percentages shocks avoided across 7 d of avoidance training in Non-Avoider and Avoider subgroups trained with 0, 0.2, 0.4, and 0.8 mA shock. The asterisk denotes a significant difference compared with the Non-Avoider subgroup. (E–H) Mean (±SEM) hot-plate latencies assessed immediately after avoidance training. The asterisk denotes a significant difference between the Non-Avoider and Avoider subgroups.

Figure 3.

(A) Mean (±SEM) percentage avoidance during the Shock-OFF avoidance test in Non-Avoider and Avoider subgroups trained with 0-, 0.2-, 0.4-, and 0.8-mA shock. The asterisk denotes a significant difference between the Non-Avoider and Avoider subgroups. (B) Mean (±SEM) hot-plate latencies assessed immediately after the Shock-OFF avoidance test.

Figure 4.

(A) Mean (±SEM) percentage shocks avoided across 7 d of avoidance training in animals trained with 0- and 0.8-mA shock. Only animals trained with 0.8-mA shock were divided into Non-Avoider and Avoider subgroups. (B) Mean (±SEM) hot-plate latencies assessed immediately after avoidance training. The asterisk denotes a significant difference compared with the 0.8-mA Non-Avoider subgroup. The number sign denotes a significant difference compared with the 0-mA group. The “at” sign denotes a significant difference compared with training day 1.

Figure 5.

(A) Mean (±SEM) percentage avoidance during the Shock-OFF avoidance test in animals trained with 0- and 0.8-mA shock. Only animals trained with 0.8-mA shock were divided into Non-Avoider and Avoider subgroups. (B) Mean (±SEM) hot-plate latencies assessed immediately after the Shock-OFF avoidance test. The asterisk denotes a significant difference compared with the 0.8-mA Non-Avoider subgroup. The number sign denotes a significant difference compared with the 0-mA group.

Figure 6.

The mean (±SEM) discrimination ratio produced during the sample and choice phase of object recognition following exposure to the avoidance context and CS postsample. The asterisk denotes a significant difference compared with sample phase discrimination ratio. The number sign denotes a significant difference compared with the 0-mA choice phase discrimination ratio.