Variations in the retention of taste aversions: Evidence for retrieval competition

In six experiments, we examined taste and compound taste/taste aversions at different retention intervals. In Experiment 1, saccharin aversions were significantly weaker 1 day after conditioning than 21 days after conditioning. This effect was determined not to be caused by the aftereffects of illness or differential hydration. With the use of a saccharin/denatonium compound, Experiment 2 demonstrated overshadowing of a denatonium aversion at 21- and 1-day retention intervals, Experiment 4 showed a potentiated saccharin aversion only at the 21-day retention interval, and both Experiments 2 and 4 revealed that the aversion of the taste-only controls was stronger at the later retention interval. Experiments 3 and 5 demonstrated that the differences at the two retention intervals were not caused by unconditioned changes in taste preference. Finally, Experiment 6 showed that extinction of the conditioning environment prior to testing results in stronger saccharin aversions than occur in nonextinguished controls. Collectively, these experiments suggest that testing within a 24-h period after conditioning will result in significantly weaker taste aversions. Also, these results support a retrieval-competition explanation that may account for the weakened aversions at the 1-day testing interval of both groups conditioned to single elements and those conditioned to compounds.     

Impact of brief or extended extinction of a taste aversion on inhibitory associations: Evidence from summation,retardation, and preference tests

In five conditioned taste aversion experiments with rats, summation, retardation, and preference tests were used to assess the effects of extinguishing a conditioned saccharin aversion for three or nine trials. In Experiment 1, a summation test showed that saccharin aversion extinguished over nine trials reduced the aversion to a merely conditioned flavor (vinegar), whereas three saccharin extinction trials did not subsequently influence the vinegar aversion. Experiment 2 clarified that result, with unpaired controls equated on flavor exposure prior to testing; the results with those controls suggested that the flavor extinguished for nine trials produced generalization decrement during testing. In Experiment 3, the saccharin aversion reconditioned slowly after nine extinction trials, but not after three. Those results suggested the development of latent inhibition after more than three extinction trials. Preference tests comparing saccharin consumption with a concurrently available fluid (water in Experiment 4, saline in Experiment 5) showed that the preference for saccharin was greater after nine extinction trials than after three. However, saccharin preference after nine extinction trials was not greater, as compared with that for either latent inhibition controls (Experiments 4 and 5) or a control given equated exposures to saccharin and trained to drink saline at a high rate prior to testing (Experiment 5). Concerns about whether conditioned inhibition has been demonstrated in any flavor aversion procedure are discussed. Our findings help explain both successes and failures in demonstrating postextinction conditioned response recovery effects reported in the conditioned taste aversion literature, and they can be explained using a memory interference account.     

Long-term retention of a conditioned taste aversion in preweanling and adult rats

The retention and extinction of a conditioned taste aversion after either short (6-day) or long (60-day) intervals was investigated in preweanling (18-day-old) and adult rats. Taste-only and illness-only control conditions were employed, as were variations in the concentration of the US (holding LiCl amount constant). Results indicated that after the short retention interval, retention of the taste aversion was equivalent for both ages. After the long interval, however, the 18-day-old rats exhibited significantly weaker taste aversion than their adult counterparts— infantile amnesia. Manipulation of US concentration had no effect on the magnitude of the taste aversions for either age or retention interval. The results are discussed in terms of their implications for infantile amnesia and general laws of learning.     

Cross-modality transfer effects in conditioning-enhanced neophobia in chicks (Gallus domesticus): Evidence for the separability of novelty from specific stimulus characteristics

In this study, we investigated the separability of novelty from specific stimulus characteristics (e.g., color or taste quality) in the transfer of aversion effects. Ninety-six chicks (Gallus domesticus) received a novel visual (red water) or taste (3.0% vinegar) CS paired with an injection of lithium chloride or saline. The chicks were then tested for aversion to the CS or for conditioning-enhanced neophobia in response to a different novel visual cue (green water) or taste cue (1.0% saline). Aversions to the CSs were reliable and similar to each other. Reliable evidence of conditioning-enhanced neophobia occurred with respect to each test stimulus, irrespective of the type of CS, but conditioning with the vinegar CS produced reliably greater enhancement of neophobia than did conditioning with red water. For each CS, postconditioning neophobia was more persistent in testing with saline than with green water. The results for postconditioning neophobia suggested that novelty is a general stimulus property that is separable from specific stimulus characteristics.     

CS–US interval determines the transition from overshadowing to potentiation with flavor compounds

The present series of five flavor aversion experiments with rat subjects examined compound conditioning at varying CS-US intervals. Using a taste-taste design, Experiments 1A and 1B demonstrated overshadowing at a 0-min CS-US interval and potentiation at a 120-min CS-US interval, and these effects occurred with both tastes of the compound. Experiment 2 showed that the aversion to a single element is reduced when the CS-US interval is increased to 120 min, but the aversion for a compound taste is not. Experiments 3A and 3B explored odor + taste compound conditioning; the results demonstrated odor potentiation across the trace interval and a transition from taste overshadowing to taste potentiation. Collectively, the data show that the change from overshadowing to potentiation was not due to changes in the aversions produced by compound conditioning but, instead, was due to a more rapid loss of conditionability across a trace interval prior to the US in single-element conditioning. These experiments suggest that following compound conditioning, the aversion to each element represents generalization decrement from the configured compound, but the designation of overshadowing or potentiation actually depends on the status of conditioning in the single-element control.     

Effects of postconditioning inflation on odor + taste compound conditioning

The within-compound association approach has been proposed as an account of synergistic conditioning in flavor aversion learning. One prediction from the within-compound association approach is that following taste + odor compound conditioning, postconditioning inflation of one element of the compound should increase responding to the second element. In four experiments with rats, the AX+/A+ design was used to determine whether postconditioning inflation of A would increase responding to X. In Experiments 1 and 3, responding to X was significantly stronger after AX+/A+ conditioning, as compared with AX+ conditioning. In Experiments 2 and 4, the specificity of the inflation effect was demonstrated, because AX+/A+ conditioning produced a stronger aversion to X than did AX+/B+ conditioning. Furthermore, it appears that the taste + odor association is symmetrical because inflation of the taste aversion increased responding to the odor (Experiments 1 and 2) and inflation of the odor aversion increased responding to the taste (Experiments 3 and 4).     

Latent inhibition of conditioned disgust reactions in rats

The present experiments, using the latent inhibition (LI) paradigm, evaluated the effect of nonreinforced exposure to saccharin on the acquisition of an LiCl-induced saccharin aversion as measured by conditioned disgust reactions in the taste reactivity test and conditioned taste avoidance in a consumption test. When rats were preexposed to saccharin by bottle exposure (Experiments 1 and 3), LI was evidenced only by conditioned taste avoidance (bottle testing), but not by conditioned disgust reactions (intraoral [IO] testing). On the other hand, when rats were preexposed to saccharin by IO infusion (Experiments 2 and 3), LI was evidenced only by conditioned disgust reactions, but not by conditioned taste avoidance. Experiment 4 showed that LI of conditioned disgust reactions does not appear to be affected by a context shift from preexposure to testing phases. These results show that the expression of LI of both conditioned taste avoidance and conditioned disgust reactions depends critically on a common method of flavor exposure during preexposure and testing.     

Lack of effect of specific sodium hunger on learned aversions to sodium and sucrose

Frumkin (1975) reported that sodium-deficient rats fail to learn taste aversions to NaCl. However, those rats were sodium-deficient at the time of testing as well as at the time of training; any learned aversion could have been masked by a strong sodium hunger. Rats were made temporarily sodium-hungry by injections of Formalin or aldosterone. They were then poisoned after drinking both an NaCl and a sucrose solution. Several days later they were tested for learned aversions. Rats trained under the influence of aldosterone did not differ from controls. Rats trained under the influence of Formalin acquired slightly weaker aversions to both NaCl and sucrose. Thus there is no evidence that sodium deficiency alters the associability of NaCl with poison.     

Taste avoidance and taste aversion: Evidence for two different processes

The terms conditioned taste avoidance and conditioned taste aversion are often used interchangeably in the literature; however, considerable evidence indicates that they may represent different processes. Conditioned taste avoidance is measured by the amount that a rat consumes in a consumption test that includes both appetitive phases and consummatory phases of responding. However, conditioned taste aversion is more directly assessed with the taste reactivity test, which includes only the consummatory phase of responding. Rats display a conditioned taste aversion as conditioned rejection reactions (gapes, chin rubs, and paw treads) during an intraoral infusion of a nausea-paired flavored solution. Treatments that produce nausea are not necessary for the establishment of taste avoidance, but they are necessary for the establishment of taste aversion. Furthermore, treatments that alleviate nausea modulate neither the establishment nor the expression of taste avoidance, but they interfere with both the establishment and the expression of taste aversion. Considerable evidence exists indicating that these two measures are independent of one another. Taste avoidance may be motivated by conditioned fear rather than conditioned nausea, but taste aversion (as reflected by rejection reactions) may be motivated by conditioned nausea.     

Extinction of a saccharin—lithium association: Assessment by consumption and taste reactivity

Extinction of a conditioned palatability shift preceded extinction of conditioned taste avoidance whether rats were tested using a within-subjects design or a between-subjects design. In each of two experiments, consumption of 0.1% saccharin was paired with either 20 ml/kg of 0.15 M LiCl or equivolume physiological saline on a single trial. In Experiment 1, on each of 10 extinction trials, rats were given a taste reactivity test immediately prior to a consumption test. In Experiment 2, half of the rats were extinguished by taste reactivity testing and half of the rats were extinguished by a consumption test on each of 10 extinction trials. In both experiments, the aversive reactions of gaping and passive dripping were extinguished in a single trial and the suppression of ingestive reactions was extinguished in 2 trials; however, extinction of taste avoidance required 4–5 trials. These results suggest that rats continue to avoid a lithium-paired flavor even when they do not have an aversion to the taste.     

A history of morphine-induced taste aversion learning fails to affect morphine-induced place preference conditioning in rats

Drugs of abuse have both rewarding and aversive effects, as indexed by the fact that they support place preferences and taste aversions, respectively. In the present study, we explored whether having a history with the aversive effects of morphine (via taste aversion conditioning) impacted the subsequent rewarding effects of morphine, as measured in the place preference design. In Experiment 1, rats were exposed to a taste aversion procedure in which saccharin was followed by morphine. Place preference conditioning was then initiated in which animals were injected with morphine and placed on one side of a two-chambered apparatus. Animals with a taste aversion history acquired place preferences to the same degree as controls without such a history, suggesting that morphine’s affective properties condition multiple effects, dependent on the specific stimuli present during conditioning. To determine whether these results were a reflection of processes operating in traditional associative conditioning, in a modified blocking procedure, place preference conditioning was attempted in the presence of a taste previously associated with morphine (Exp. 2). Under these conditions, animals still acquired morphine-induced place preferences comparable to those of animals without a morphine or conditioning history. These results are consistent with the position that drugs of abuse have multiple stimulus effects (positive and negative) that are differentially associated with specific stimuli (environmental and taste) that drive different behavioral responses (approach and avoidance).     

An extinction cue reduces spontaneous recovery of a conditioned taste aversion

The effect of an auditory cue presented during extinction on spontaneous recovery of a conditioned taste aversion was investigated in three experiments. Experiment 1 demonstrated that the presence of the cue during extinction did not influence saccharin consumption during that phase, and that an aversion to saccharin in the absence of the cue was stronger at 18 days than at 1 day after extinction, representing spontaneous recovery rather than a renewal effect. Experiment 2 showed that a cue presented during extinction and testing reduced spontaneous recovery. Experiment 3 replicated that effect and showed that it depended on the cue’s correlation with extinction and not on an unconditioned effect; cues that had been presented during or prior to conditioning did not reduce spontaneous recovery when presented during testing. The cue’s potential to reduce spontaneous recovery through conditioned inhibition or configural cue learning is discussed, as is the possibility that the cue retrieves a saccharin extinction memory in a manner consistent with Bouton’s (1993) account of spontaneous recovery.     

Nonreinforced flavor exposure attenuates the effects of conditioned taste aversion on both flavor consumption and cue palatability

Nonreinforced exposure to a cue tends to attenuate subsequent conditioning with that cue—an effect referred to as latent inhibition (LI). In the two experiments reported here, we examined LI effects in the context of conditioned taste aversion by examining both the amount of consumption and the microstructure of the consummatory behavior (in terms of the mean size of lick clusters). The latter measure can be taken to reflect affective responses to, or the palatability of, the solution being consumed. In both experiments, exposure to a to-be-conditioned flavor prior to pairing the flavor with nausea produced by lithium chloride attenuated both the reduction in consumption and the reduction in lick cluster sizes typically produced by taste aversion learning. In addition, we observed a tendency (especially in the lick cluster measure) for nonreinforced exposure to reduce neophobic responses to the test flavors. Taken together, these results reinforce the suggestion from previous experiments using taste reactivity methods that LI attenuates the effects of taste aversion on both consumption and cue palatability. The present results also support the suggestion that the failure in previous studies to see concurrent LI effects on consumption and palatability was due to a context specificity produced by the oral taste infusion methods required for taste reactivity analyses. Finally, the fact that the pattern of extinction of conditioned changes in consumption and in lick cluster sizes was not affected by preexposure to the cue flavors suggests that LI influenced the quantity but not the quality of conditioned taste aversion.     

One bottle too many? Method of testing determines the detection of overshadowing and retention of taste aversions

A two-bottle testing method generally is regarded as a more sensitive measure of taste aversions than a one-bottle test. The current research compared the sensitivity of one-bottle and two-bottle tests in the detection of taste aversions. Specifically, the experiments were designed to detect both overshadowing (single- vs. compound-element conditioning) and retention interval (5 days vs. 1 day) effects. The groups tested with the one-bottle method evidenced both significant overshadowing and stronger aversions at 5-day retention intervals. On the other hand, the differences on these measures were not significant with the two-bottle tests. It is suggested that the efficacy of the two-bottle test be re-evaluated since it may obscure between-group differences in aversion strength.     

The effect of nonreinforced stimulus exposure on the strength of a conditioned taste aversion as a function of retention interval: Do latent inhibition and extinction involve a shared process?

Two experiments examined the effects of nonreinforced flavor exposure on the strength of a conditioned taste aversion. Rats were conditioned by pairing maple flavor with LiC1. Prior to or subsequent to this pairing, some animals received nonreinforced exposure to either maple or saccharin. In separate subjects, preference for maple was tested 1 or 21 days after the last training episode. In the first experiment, the nonreinforced stimulus exposure occurred before conditioning (latent inhibition, or LI, procedure); in the second experiment, the nonreinforced exposure occurred after conditioning (extinction, or EXT, training). In both experiments, nonreinforced exposure to maple or saccharin reduced the magnitude of a conditioned maple aversion when testing occurred soon after conditioning. When testing was delayed, however, the attenuation due to nonreinforced saccharin exposure dissipated, both with the LI procedure and with EXT. In contrast, the nonreinforced exposure to maple was found to attenuate conditioned reactions at both short and long retention intervals. The release from generalized LI and spontaneous recovery following generalized EXT training are discussed in terms of retrieval processing. The possibility that the same mechanism may underlie LI and EXT is considered.     

Taste aversion learning and schedule-induced polydipsia in rats

Experiment 1 sought to determine whether schedule-induced drinking could be abolished by means of a taste aversion. Polydipsic rats were given access to a .4% saccharin solution while they were exposed to an intermittent food schedule. Immediately after the session, they received an intraperitoneal injection of either lithium chloride or sodium chloride. Following a recovery day with water in the experimental chamber, the animals were again exposed to the saccharin solution. The poisoned animals (lithium chloride) drank very little saccharin compared to the control animals (sodium chloride), indicating that they had learned a taste aversion in only one conditioning trial. Experiment 2 established that polydipsic rats can learn a taste aversion despite a long delay between schedule-induced saccharin consumption and poisoning, and that the delay gradient displayed by polydipsic rats is similar to that observed in thirst-motivated rats.     

Second-order conditioning detects unexpressed morphine-induced salt aversion

Morphine failed to condition a salt taste aversion at a dose (15 mg/kg) sufficient to produce a robust aversion to a saccharin taste. Indeed, three different concentrations of salt (1%, 1.5%, and 2%) paired with the same morphine dose yielded no direct evidence for conditioned aversion. Yet, when a novel saccharin taste was paired in compound with the previously conditioned salt conditioned stimulus, we found evidence for a conditioning to the saccharin cue alone in three separate experiments. Control groups eliminated alternative accounts such as neophobia and differential exposure to morphine. Combined, these findings indicate that morphine conditioned a salt aversion. Although this aversion was not directly expressed, a second-order conditioning procedure was able to provide a more sensitive index of conditioning.     

Amount of solution drunk is a factor in the establishment of taste aversion

Experiment I demonstrated that the strength of a rat’s aversion to saccharin is a direct function of the amount of saccharin it consumed prior to poisoning. Using Kalat and Rozin’s (1973) procedure, Experiment II showed that results consistent with a “learned-safety” theory of taste aversion appear to depend on whether rats drink most saccharin on their first or second exposure to the solution prior to poisoning. Experiment III demonstrated that when animals drank equal amounts of saccharin solution on each of two exposures prior to poisoning, evidence strongly confirming the “learned-safety” theory was obtained. These experiments together demonstrate the importance of amount of solution drunk in the determination of taste aversion.     

Expression of a taste aversion conditioned with an odor-taste compound: Overshadowing is relatively weak in weanlings and decreases over a retention interval in adults

Adult rats were injected with lithium chloride (LiCl) after consumption of a novel flavor (chocolate milk) that either was or was not presented together with a novel ambient odor (banana) as a compound conditioned stimulus (CS). In Experiment 1, the adults’ consumption of the flavor 24 h after conditioning was compared with that of weanling rats given the same conditioning treatment on Postnatal Day 21. The results confirmed previous indications that the reduction in aversion observed for adults conditioned with the compound CS (overshadowing) was weak or nonexistent in weanlings. After a longer retention interval (21 days), there was no evidence of overshadowing in adults despite maintained retention of the basic conditioned aversion. In Experiment 2 this decrease in overshadowing after a long retention interval was replicated with adult animals and extended to a different method of testing. The form of the effect was the same as in Experiment 1: The decrease in overshadowing occurred over the retention interval without loss in retention of the basic taste aversion; the decrease in overshadowing was a consequence of anincrease in the flavor aversion displayed by animals conditioned with the compound CS. The impaired flavor aversion (i.e., the overshadowing) observed shortly after conditioning apparently was due to factors associated with memory retrieval, rather than to reduced attentional or associative strength.     

Extended exposure to environmental cues,but not to sucrose,reduces sucrose cue reactivity in rats

In the present study, we examined the effects of extinction of sucrose-predictive contextual cues and/or sucrose satiation on the expression of sucrose cue reactivity in a rat model of relapse. Context extinction was imposed by housing rats in their home cage or in the operant conditioning chamber for 17 h prior to testing. For sucrose satiation, rats were allowed unlimited access to water or sucrose for 17 h prior to testing. Cue reactivity was assessed after either one (Day 1) or 30 (Day 30) days of forced abstinence from sucrose self-administration. An abstinence-dependent increase in sucrose cue reactivity was observed in all conditions (“incubation of craving”). Context extinction dramatically reduced lever responding on both Day 1 and Day 30. Sucrose satiation had no significant effect on cue reactivity in any condition. These results demonstrate that the context in which self-administration occurs maintains a powerful influence over cue reactivity, even after extended forced abstinence. In contrast, the primary reinforcer has little control over cue reactivity. These findings highlight the important role of conditioned contextual cues in driving relapse behavior.