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.     

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.     

Slow reacquisition of a conditioned taste aversion

Rats were used to examine the extent to which extinction of an acquired conditioned taste aversion retards subsequent reacquisition. A saccharin-flavored solution (sac) was paired with LiCl and then followed by CS-alone extinction trials with this flavor. A control group received a different flavor, decaffeinated-coffee (coff), during initial conditioning and extinction. Sac was then paired with LiCl for all rats during a second conditioning phase. Reacquisition of the aversion to sac was retarded relative to the acquisition of an aversion to sac by the control group. A similar experiment with fewer extinction trials, but still with complete loss of the initial aversion, did not obtain slow reacquisition. The results are discussed with respect to an interference view of extinction and the slow-reacquisition effect.     

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.     

Habituation to illness: Effects of prior experience with the US on the formation of learned taste aversions in rats

Experiment 1 investigated the effects of US habituation on the acquisition and extinction of learned taste aversions in rats. Subjects receiving five noncontingent LiCl intubations prior to conditioning failed to develop a conditioned taste aversion, while control subjects experiencing a single saccharin/LiCl pairing displayed a pronounced taste aversion which weakened during subsequent poisonings. Experiment 2 examined whether habituation, defined as a waning of responses to repeated presentation of an illness stimulus, was a possible mechanism for explaining the results of Experiment 1. Subjects showed a decrease in motor activity following an initial LiCl intubation, but less attenuation of activity with successive intubations.     

The interaction of conditioned taste aversions and schedule-induced polydipsia: Effects of repeated conditioning trials

In Experiment 1, rats poisoned following schedule-induced saccharin consumption showed a moderate reduction in the schedule-induced consumption of saccharin. With repeated poisoning, schedule-induced saccharin polydipsia was markedly reduced. Acquisition of conditioned aversion under the schedule-induced procedure was significantly slower than acquisition under water deprivation. In addition, recovery of consumption of the previously poisoned solution during extinction was more rapid under schedule-induced polydipsia. Experiment 2 revealed that schedule-induced polydipsia was less sensitive to suppression by conditioned aversions than a prandial drinking condition in which subjects were equally food deprived but were given a mass feeding instead of spaced pellet deliveries, suggesting that the relative insensitivity of schedule-induced polydipsia to conditioned taste aversions is not simply a function of different levels of food deprivation. This relative insensitivity is offered as a partial basis for the occurrence and maintenance of schedule-induced alcohol polydipsia.     

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.     

Reinstatement-induced recovery of a taste-LiCl association following extinction

Water-deprived rats were given a single exposure to saccharin and LiCl, either paired or unpaired. Half the subjects then received three saccharin-only exposures (extinction) in the training enclosure, followed by a single LiCl-only presentation (unconditioned stimulus reinstatement) 8 days after conditioning. The remaining subjects received six saccharin-only exposures, followed by LiCl reinstatement 13 days after conditioning. In both cases LiCl reinstatement occurred outside the training/test context. Appreciable recovery from extinction was observed after the partial loss of taste aversion obtained with three extinction sessions and the 8-day conditioning-reinstatement interval, but not after the asymptotic loss of taste aversion obtained with six extinction sessions and the 13-day conditioning-reinstatement interval. Conditioned taste aversions appear to be similar to more traditional associations with respect to both extinction and reinstatement-induced recovery from extinction. The results are discussed with reference to the event-memory, contextual-conditioning, and facilitated-retrieval hypotheses of postextinction reinstatement effects.     

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.     

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.     

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.     

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.     

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.     

Conditioned taste aversion in Philippine rice rats (R. r. mindanensis): Comparisons among drugs,dosages, modes of administration,and sexes

The effects of select drugs, dosages, and modes of administration upon learned taste aversions were compared among groups of wild-caught male and female Philippine rice rats (R. r. mindanensis). Experiment 1 compared two-choice saccharin aversions for 28 days among groups intubated with copper sulfate, cyclophosphamide, lithium chloride, red squill, sodium chloride (control), or deionized water (control). Main results were that 375 mg/kg lithium chloride produced the greatest sustained aversions, whereas 198 mg/kg cyclophosphamide and 210 mg/kg red squill produced moderate aversions, with males showing more resistance to extinction than females. Experiment 2 compared saccharin aversion among matched groups of male and female rats that received low (36 mg/kg), moderate (105 mg/kg), or high (368 mg/kg) dosages of lithium by gavage, ip injection, or ingestion. Sex differences in rates of extinction were found for the ingestion and injection-dosed rats, but no sex difference was again found for rats dosed by gavage. A significant mode × day interaction indicated that extinction progressed more rapidly for rats dosed by gavage. For all modes of administration, high dosages yielded intense 28-day aversion, moderate dosages produced intermediate 3–5 day aversion, and low dosages caused no aversion.     

Taste-potentiated color aversions in pigeons: Examination of CS preexposure and subsequent effects on postconditioning extinction of the taste aversion

In the present study, we investigated the mechanisms of potentiation using pigeons as subjects. Half the groups were given unreinforced preexposures to the CS on 2 consecutive days before aversion training. After training, the taste aversion was extinguished in some of the groups conditioned with a colored, tasty compound. Postconditioning extinction of the taste aversion was found to attenuate potentiated color aversions. This was the case for the subjects that both were and were not preexposed to the CS. These results lend support to the summation theory of potentiation (Durlach & Rescorla, 1980) and weaken the claim that CS preexposures are necessary for obtaining such support. Alternative accounts of the data are discussed.     

Changes in the retrievability of associations to elements of the compound CS determine the expression of overshadowing

In two experiments, rats were presented with a taste conditioned stimulus (CS) alone, an odor CS alone, or an odor-taste compound followed by lithium chloride injection. When tested 1 day following conditioning, there was evidence that the odor cue overshadowed conditioning to the taste; however, there was no indication of overshadowing following a longer (21-day) retention interval, despite undiminished strength of the aversion in animals conditioned with only the single element (taste). The overshadowing observed at the 1-day retention interval was not reciprocal. Rats conditioned with the odor CS alone or with the compound CS expressed odor aversions of comparable strength—that is, no overshadowing. However, in contrast to the taste aversion, overshadowing of conditioning to the odor by taste was evident following a 21-day retention interval. Rather than reflecting a failure of the overshadowed stimulus to acquire associative strength, these data suggest that overshadowing may be expressed, or not expressed, as a result of changes in the relative retrievability of learned associations over time.     

Lack of reinstatement of an extinguished taste aversion

Three experiments with rat subjects were designed to investigate the possibility that an extinguished saccharin aversion might be reinstated if the animals are made ill with lithium chloride (in the absence of saccharin) following extinction. Although reinstatement can be obtained when the unconditioned stimulus is presented following the extinction of other kinds of conditioned behaviors, the present experiments provided no evidence that an extinguished taste aversion can be reinstated. No reinstatement was observed, even when the aversion had been only partially extinguished and when multiple injections of lithium chloride were administered in an attempt to reinstate the aversion.     

The effect of drug habituation before and after taste aversion learning in rats

In Experiment I, rats received eight habituation injections of either lithium chloride (LiCl) or sodium chloride (NaCl), then two aversion training trials in which access to saccharin solution was followed by LiCl injections, and finally eight extinction trials with saccharin but no injections. The rats habituated to LiCl showed less aversion to saccharin during training and extinction. In Experiment II, rats received two aversion training trials, then eight habituation trials to either LiCl or NaCl, then eight extinction trials, four more aversion training trials, and eight more extinction trials. The rats habituated to LiCl did not differ during the first extinction period from those habituated to NaCl, but showed less aversion to saccharin during the second training and extinction periods. Consequently, habituation to LiCl reduces the learning of an aversion to saccharin but does not reduce the performance of a previously learned aversion.     

A mixed design reveals that glucose moieties facilitate extinction of a conditioned taste aversion in rats

Separate groups of water-deprived rats had four trials with 15-min access to 0.0073 M saccharin, 0.3 M alanine, 0.3 M glucose, 0.1 M maltose, 0.3 M fructose, 0.06 M sucrose, or 0.03 M Polycose. Trials 1–3 were followed by injections of either 0.15 M LiCl (1.33 ml/100 g b.w., i.p.) or saline; Trial 4 (Test) was CS only. Extinction included either 48-h access to water alone or to the appropriate CS, both followed by a 24-h, two-bottle choice of CS and water. This 3-day cycle was repeated five to six times. All rats acquired comparable conditioned taste aversions (CTAs), but extinction rates varied with the test and the taste CS. No CTA extinguished during the two-bottle choices following 2 water days. During one-bottle CS exposure, all CTAs extinguished, but the aversion continued longer in the probe two-bottle tests. Intake of glucose moieties recovered rapidly, often in two cycles; the other CSs took four to six cycles. Thus, CTA extinction varies with the nature of the taste CS.     

Extinction of the overshadowing CS after overshadowing in conditioned taste aversion

Using a conditioned taste aversion preparation overshadowing of flavor-illness association was produced through the presentation of a second flavor during the interval between the first flavor and illness. The modulatory effects of extinguishing the association between the second (over-shadowing) flavor and illness on conditioned responding to the target flavor was investigated. In Experiment 1, we found that, following one-trial overshadowing, extinction of the overshadowing flavor had no effect on conditioned responding to the target flavor. In Experiment 2, we found a similar absence of an effect of extinction of the overshadowing stimulus in a multitrial over-shadowing paradigm. Experiment 3 confirmed the results of Experiments 1 and 2 using conditioning parameters that were designed to weaken the association between the overshadowed flavor and illness. In Experiments 4 and 5, we used simultaneous presentation of the flavors during conditioning and obtained a weakened aversion to the overshadowed flavor when the overshadowing CS was extinguished. These findings are inconsistent with previous observations in conditioned fear preparations that suggest that extinction of the association between the overshadowing stimulus and the unconditioned stimulus attenuates overshadowing. Possible reasons for the discrepant results are discussed.