Retrograde enhancement of episodic learning by a postlearning stimulus

Abstract

Evidence suggests encoding of recent episodic experiences may be enhanced by a subsequent salient event. We tested this hypothesis by giving rats a 3-min unsupervised experience with four odors and measuring retention after different delays. Animals recognized that a novel element had been introduced to the odor set at 24 but not 48 h. However, when odor sampling was followed within 5 min by salient light flashes or bedding odor, the memory lasted a full 2 d. These results describe a retroactive influence of salience to promote storage of episodic information and introduce a unique model for studying underlying plasticity mechanisms.

Figure 1.

A novel environmental event retroactively enhances unsupervised encoding of olfactory cues. (A) Rats were exposed (session 1) to four odors (A–D) for 3 min and tested (session 2) 24 or 48 h later with one of the cues replaced with a novel odor (E, orange). A 15-sec strobe light was flashed on the arena immediately after session 1 in one group. (B, left) Rats did not have preferences for the different odors used in the initial exposure period. (Right) On average, ∼50% of the time spent investigating the cues occurred in the first minute of session 1. (C) During the 24-h retention test, rats preferably sampled novel odor “E” (n = 12, [*] P = 0.019, within group comparison for seconds sampling E vs. mean time sampling cues A–C). (D) When tested 48 h after session 1, control (no strobe) rats did not distinguish between novel and familiar odors (n = 10, P > 0.05), whereas rats given the strobe flashes did preferentially explore novel odor E (n = 15, [*] P = 0.018, within group comparison for sampling times; [*] P = 0.017, between group comparison for percent time sampling the novel cue). The sampling time for cue E recorded for the 24-h control (no strobe) group was statistically greater than for the 48-h control group ([*] P = 0.020, not shown in figure).

Figure 2.

The strobe light did not disrupt exploration or produce anxiogenic effects. (A) Rats maintained a consistent level of exploration while sampling odors during session 1: There was no evidence for freezing during the strobe flashes or during the following 15 sec (no strobe N = 7, strobe = 7; P > 0.05 at 15-sec strobe mark). (B) Rats performed equivalently on an elevated plus maze whether they received strobe light or not. Both groups remained within the closed arm for the majority of the trial and for nearly identical amounts of time (control/no strobe = 6, [*] P = 0.021; strobe n = 7, [**] P = 0.008).

Figure 3.

Retroactive enhancement is delay dependent and not specific to visual cues. (A) Rats that were exposed to a strobe light 1–3 min after the initial 3-min session with four odors spent a greater percent time (seconds) sampling novel odor E than the mean for the three previously sampled cues (A–C) during a delayed (48 h) retention trial (n = 14, [*] P = 0.016, paired t-test for time with novel vs. familiar cues). (B) Preference for novel odor E was not significant when the delay between the initial odor exposure session and the strobe was increased to 5–10 min (n = 13, P = 0.112). However, when comparing the 1–3 min and 5–10 min groups, the amount of time spent with novel odor E was not significantly different (n = 14,13; t₂₄ = 1.078; P = 0.291). (C) Rats exposed to female rat bedding (instead of a strobe light) after odor cue sampling in session 1, had excellent retention scores 48 h later (time/seconds investigating the novel vs. the previously sampled odors: n = 14, [**] P = 0.003, within group t-test). Rats exposed to control bedding after session one did not prefer the novel cue E in the delayed retention trial (n = 20, P = 0.407, paired t-test for sampling times). The percent time spent with novel odor E was greater for the female bedding group than the control bedding group ([**] P = 0.006, unpaired test).