Rapid, labile, and protein synthesis-independent short-term memory in conditioned taste aversion

Abstract

Short-term memory is a rapid, labile, and protein-synthesis-independent phase of memory. The existence of short-term memory in conditioned taste aversion (CTA) learning has not been demonstrated formally. To determine the earliest time at which a CTA is expressed, we measured intraoral intake of sucrose at 15 min, 1 hr, 6 hr, or 48 h after contingent pairing of an intraoral infusion of 5% sucrose (6.6 ml over 6 min) and toxic lithium chloride injection (76 mg/kg). Rats were implanted with intraoral catheters to allow presentation of taste solutions at arbitrary times. Intraoral intake was measured under conditions of long-delay, single-trial learning typical of CTA. Rats decreased intraoral intake of sucrose at 15 min after contingent pairing of sucrose and LiCl, but not after noncontingent LiCl or sucrose. Thus CTA learning can be expressed rapidly. To determine if short-term CTA memory is labile and decays in the absence of long-term memory, we measured intraoral intake of sucrose after pairing sucrose with low doses of LiCl. Rats received an intraoral infusion of 5% sucrose (6 ml/6 min); 30 min later LiCl was injected at three different doses (19, 38, or 76 mg/kg). A second intraoral infusion of sucrose was administered 15 min, 1 hr, 3 hr, 4.5 hr, 6 hr, or 48 hr later. The formation of long-term CTA memory was dependent on the dose of LiCl paired with sucrose during acquisition. Low doses of LiCl induced a CTA that decayed within 6 hr after pairing. Central administration of the protein synthesis inhibitor cycloheximide prior to LiCl injection blocked long-term CTA expression at 6 and 48 hr, but not short-term CTA expression at 1 hr. Thus, short-term memory for CTA learning exists that is acquired rapidly and independent of protein synthesis, but labile in the absence of long-term memory formation.

Figure 1

Rapid expression of a CTA. Intraoral intake of 5% sucrose was measured as weight gain during the intraoral infusion. Individual rats were tested only once at one time point (n = 4–9). Arrows indicate the times of LiCl injection (76 mg/12 ml/kg, i.p.). (A) Intraoral intake of 5% sucrose after contingent pairing of an intraoral infusion of 5% sucrose (6.6 ml over 6 min) and LiCl. Rats significantly decreased their intraoral intake of sucrose at 15 min after pairing. (*) P < 0.005 compared to noncontingent lithium or noncontingent sucrose. (B) Intraoral intake of 5% sucrose after noncontingent injection of LiCl. Rats received an intraoral infusion of 5% sucrose (6.6 ml over 6 min) 24 hr prior to the LiCl injection. Intraoral intake was not significantly reduced after noncontingent LiCl. (C) Intraoral intake of 5% sucrose after a noncontingent intraoral infusion of 5% sucrose (6.6 ml over 6 min). Rats received an injection of LiCl 24 hr prior to the intraoral infusion of sucrose. Intraoral intake was not reduced significantly after noncontingent sucrose.

Figure 1

Rapid expression of a CTA. Intraoral intake of 5% sucrose was measured as weight gain during the intraoral infusion. Individual rats were tested only once at one time point (n = 4–9). Arrows indicate the times of LiCl injection (76 mg/12 ml/kg, i.p.). (A) Intraoral intake of 5% sucrose after contingent pairing of an intraoral infusion of 5% sucrose (6.6 ml over 6 min) and LiCl. Rats significantly decreased their intraoral intake of sucrose at 15 min after pairing. (*) P < 0.005 compared to noncontingent lithium or noncontingent sucrose. (B) Intraoral intake of 5% sucrose after noncontingent injection of LiCl. Rats received an intraoral infusion of 5% sucrose (6.6 ml over 6 min) 24 hr prior to the LiCl injection. Intraoral intake was not significantly reduced after noncontingent LiCl. (C) Intraoral intake of 5% sucrose after a noncontingent intraoral infusion of 5% sucrose (6.6 ml over 6 min). Rats received an injection of LiCl 24 hr prior to the intraoral infusion of sucrose. Intraoral intake was not reduced significantly after noncontingent sucrose.

Figure 1

Rapid expression of a CTA. Intraoral intake of 5% sucrose was measured as weight gain during the intraoral infusion. Individual rats were tested only once at one time point (n = 4–9). Arrows indicate the times of LiCl injection (76 mg/12 ml/kg, i.p.). (A) Intraoral intake of 5% sucrose after contingent pairing of an intraoral infusion of 5% sucrose (6.6 ml over 6 min) and LiCl. Rats significantly decreased their intraoral intake of sucrose at 15 min after pairing. (*) P < 0.005 compared to noncontingent lithium or noncontingent sucrose. (B) Intraoral intake of 5% sucrose after noncontingent injection of LiCl. Rats received an intraoral infusion of 5% sucrose (6.6 ml over 6 min) 24 hr prior to the LiCl injection. Intraoral intake was not significantly reduced after noncontingent LiCl. (C) Intraoral intake of 5% sucrose after a noncontingent intraoral infusion of 5% sucrose (6.6 ml over 6 min). Rats received an injection of LiCl 24 hr prior to the intraoral infusion of sucrose. Intraoral intake was not reduced significantly after noncontingent sucrose.

Figure 2

Dose-dependent expression of a labile short-term CTA. Intraoral intake of 5% sucrose after contingent pairing of an intraoral infusion of 5% sucrose (6.6 ml over 6 min) with different doses of LiCl [0 (○), 19 (□), 38 (▴), or 76 (●) mg/kg] or 0.15 m NaCl (12 ml/kg). Individual rats were tested only once at one time point (n = 4–9). Intakes from Fig. 1 for the time points at 15 min, 1 hr, 6 hr, and 48 hr after 76 mg/kg were included in the analysis and data shown here. After all doses of LiCl, rats significantly decreased intraoral intake of sucrose at 15 min to 3 hr doses compared to NaCl treatment. After 6 hr, however, intraoral intake of sucrose was only significantly decreased after pairing with the highest dose of LiCl. (*) P < 0.005 vs. intake after 76 mg/kg; ^†P < 0.05 vs. intake after 38 mg/kg.

Figure 3

Protein-synthesis-independent and -dependent expression of CTA. Rats received an intraoral infusion of 5% sucrose, followed 15 min later by an ICV injection of 0.15 m NaCl (10 μl; open bars) or cycloheximide (250 μg/10 μl; solid bars); 15 min after the ICV injection, all rats received LiCl (76 mg/kg, i.p.). Individual rats were tested only once at one time point (n = 5–8). After either ICV cycloheximide or NaCl, rats significantly decreased intraoral intake of sucrose at 1 hr compared to their initial sucrose intake. At 6 and 48 hr, however, intraoral intake of sucrose was significantly decreased only after ICV NaCl; cycloheximide-treated rats consumed significantly more sucrose than NaCl-treated rats, with no significant decrease compared to their initial sucrose intake. (*) P < 0.05 vs. NaCl-treated rats; (^†)P < 0.05 vs. sucrose intake during pairing.