Role of exteroceptive background context in taste-aversion conditioning and extinction

In two experiments, saccharin (CS) and lithium chloride (US) were paired in a context consisting of specific visual, auditory, tactual, and olfactory cues. The saccharin aversion was then extinguished in a context free from conditioning-context cues. Later, saccharin preference tests were given in the presence and absence of these cues. The results indicated that the background cues of the conditioning trial controlled the amount of saccharin drunk on extinction trials, and, furthermore, that extinction of the taste aversion was context specific; i.e., groups given extinction trials in a different (from conditioning) context retained their saccharin aversion in the conditioning context only. The results indicate an important role played by the exteroceptive context in taste-aversion conditioning.     

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.     

Facilitation and impairment of conditioning in the preweanling rat after prior exposure to the conditioned stimulus

Olfactory aversion conditioning of preweanling rats, 10 or 18 days postnatal, was tested after some had been given nonreinforced experience with the to-be-conditioned odor stimulus. In three experiments, it was established that the amount of prior exposure to the CS determined the effectiveness of conditioning. For both ages, odor-shock conditioning was more likely impaired with longer durations of preexposure. This effect was more apparent in the older animals. Low to moderate degrees of prior exposure to the CS under some conditions facilitated, rather than impaired, olfactory conditioning in the 10-day-old rat. This result is in agreement with one previous study in which facilitation in learning was reported for this age after short-term preexposure to the CS. The present study adds to previous data on differential effects of CS preexposure on conditioning. Although the conditions under which facilitation rather than impairment occurs are not yet clear, age-related differences in the effects of CS preexposure were apparent in the present experiments.     

Overshadowing not potentiation of illness-based contextual conditioning by a novel taste

In four experiments using rat subjects, we investigated the effects of presenting a novel flavor cue at the time of pairing an environmental context with illness. In each experiment, the subjects were allowed to spend time in a distinctive cage before receiving an injection of LiCl. For some, plain water was made available on these conditioning trials; for others, a novel taste (HCl) was presented. We measured the strength of the context aversion by assessing the ability of the contextual cues to block the acquisition of an aversion to sucrose in a further phase of training. We found that initial training with HCl present made the context less effective as a blocking cue and concluded that the HCl had overshadowed learning about the context. We suggest that this blocking procedure provides a more accurate assessment of contextual aversion than does the consumption test that has more usually been used and that taste-context overshadowing may be a more robust phenomenon than has thus far been thought.     

Context specificity of conditioning in flavor-aversion learning: Extinction and blocking tests

In three experiments using rats as subjects, we investigated the degree to which a conditioned flavor aversion transfers from one context to another. Experiment 1, using a one-trial conditioning procedure, found no effect of a change of context on a conditioned aversion. Experiment 2 employed a multitrial procedure and demonstrated that a conditioned aversion was extinguished more rapidly after a change of context. Experiment 3 showed that context change decreased the effectiveness with which a conditioned flavor could block acquisition of an aversion by a second flavor. It is argued that these data cannot be explained in associative terms, and that they constitute evidence of conditionality in a simple aversive conditioning procedure.     

Conditioned aversion is promoted by memory of CS−

Five experiments tested the effects of experience with a white compartment not paired with footshock (CS?) on conditioning of an aversion to a black compartment paired with footshock. As previously found with odors as CSs, a single pairing of the CS+ with footshock yielded significant conditioning only if the animal was also exposed to CS?, with greater conditioning when the CS? exposure preceded the CS+ than when the CS+ preceded the CS?. If, however, the CS? preceded CS+ by a 24-h interval, it was ineffective and no CS+ conditioning occurred. For adult rats, the effectiveness of the CS?/CS+ “integration” progressively decreased with increasing length of the interval separating their occurrence, although it was still significant (i.e., some CS+ conditioning occurred) with a 12-h CS? to CS+ delay. For preweanlings (16 days postnatal), no conditioning to CS+ occurred if the interval between CS? and CS+ was 1 h or longer, although significant conditioning to CS+ did occur with a CS? to CS+ interval as long as 40 min. It was as if active memory for the CS? at the time of CS+ exposure was necessary for CS+ conditioning, and forgetting of the CS? memory proceeded more rapidly for preweanling than for adult rats. Collectively, these experiments extend results previously indicating that (1) the CS+ contiguous to the US may or may not be “selected” for conditioning, depending on the rat’s exposure to, or memory for, a CS?, and (2) this stimulus selection might differ for immature and mature rats.     

Contextual control of operant behavior: evidence for hierarchical associations in instrumental learning

Recent research has suggested that operant responses can be weakened when they are tested in new contexts. The present experiment was therefore designed to test whether animals can learn a context–(R–O) relation. Rats were given training sessions in context A, in which one response (R1; lever pressing or chain pulling) produced one outcome (O1) and another response (R2; chain pulling or lever pressing) produced another outcome (O2) on variable interval reinforcement schedules. These sessions were intermixed with training in context B, where R1 now produced O2 and R2 produced O1. Given the arrangement, it was possible for the animal to learn two distinct R–O associations in each specific context. To test for them, rats were then given aversion conditioning with O2 by pairing its presentation with lithium-chloride-induced illness. Following the aversion conditioning, the rats were given an extinction test with both R1 and R2 available in each context. During testing, rats showed a selective suppression in each context of the response that had been paired with the reinforcer subsequently associated with illness. Rats could not have performed this way without knowledge of the R–O associations in effect in each specific context, lending support to the hypothesis that rats learn context–(R–O) associations. However, despite a complete aversion to O2, responding was not completely suppressed, leaving the possibility open that rats form context–R associations in addition to context–(R–O) associations.     

Toxiphobia conditioning with exteroceptive cues

The types of conditioned properties acquired by novel (i.e., nonpreexposed) or familiar (i.e., preexposed) exteroceptive cues that were paired with toxicosis, in the absence of a flavor CS, were evaluated in four experiments. In Experiment 1, the conditioned properties of novel exteroceptive cues served to block the acquisition of an aversion to a flavor CS during flavor conditioning and to suppress the ingestion response during flavor testing; animals failed to suppress their ingestion of either the flavor CS or a neutral flavor when tested in the absence of the exteroceptive CS, but suppressed their ingestion of both the flavor CS and the neutral flavor when tested in the presence of the exteroceptive CS. In Experiment 2, preexposed exteroceptive cues that had been paired with toxicosis failed to provide evidence of such conditioned properties. Experiment 3 demonstrated that preexposed contextual cues that were reinforced in compound with novel exteroceptive cues failed to acquire the conditioned properties acquired by nonpreexposed contextual cues under the same conditions of reinforcement. Finally, in Experiment 4, the conditioned properties of the novel exteroceptive cues served to evoke a conditioned gastrointestinal response that gradually extinguished as a function of repeated nonreinforced exposures to the exteroceptive cues, and, in the absence of such extinction, the conditioned properties served to block the acquisition of a flavor aversion.     

Effects of pretraining on conditioning-enhanced neophobia: Evidence for separable mechanisms of neophobia and aversion conditioning

In two experiments, rats (n = 228) received pretraining access to a distinctive novel flavor (saline) followed by aversion conditioning to a different novel conditioned stimulus (CS) (saccharin). Then the rats were tested for aversion to the CS (saccharin) or for conditioning-enhanced neophobia to a third novel flavor (casein hydrolysate). Pretraining access to a distinctive novel flavor that differed from the CS reliably reduced the magnitude of conditioning-enhanced neophobia to casein, but did not reliably affect conditioned aversion effects to the CS. Pretraining access to the CS reduced aversion effects to the CS and reduced postconditioning neophobia to casein to the performance level shown by ingestion-toxin controls. Results were consistent with the view (Braveman & Jarvis, 1978) that conditioned aversion and neophobia may be independent phenomena with separable underlying mechanisms.     

Context sensitivity of conditioned suppression following preexposure to the conditioned stimulus

Conditioned suppression in rats is often unaffected when the context (or set of background stimuli) is changed following conditioning. This suggests that responding to the conditioned stimulus (CS) can be relatively insensitive to the context in which the CS is presented. In two experiments, we examined whether sensitivity to contextual stimuli is affected by preexposure to the CS. In Experiment 1, when the CS was novel at the outset of conditioning, conditioned suppression was not affected when the context was changed following conditioning. However, when the CS had been preexposed, responding was weaker when extinction occurred outside of the conditioning context. In Experiment 2, responding was again sensitive to the test context, regardless of whether preexposure occurred in the conditioning context or in an alternate context. These results suggest that the extent to which responding is sensitive to context can depend on the conditioning history of the CS.     

Lack of reacquisition in learned taste aversions

Following ingestion of either water (Experiment 1) or saccharin (Experiment 2), experimental groups of rats were poisoned with lithium chloride and acquired an aversion to the ingested fluid. This aversion gradually extinguished and, in both experiments, was not reacquired when fluid intake was again followed by poisoning. These results are in marked contrast to usual findings of very rapid relearning following extinction with conditioning preparations other than taste-aversion learning.     

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.     

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.     

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.     

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.     

Increase in retention of a taste aversion by weanling rats after a long interval

Weanling rats were tested for retention of an aversion to a novel flavor (chocolate milk) that had been conditioned as a single-element conditioned stimulus (CS) or in compound with a novel ambient odor (banana). The presence of the ambient odor during conditioning had no effect on flavor aversion shortly thereafter, confirming previous results. The flavor aversion observed 21 days after conditioning, however, was significantly stronger for pups conditioned with the single-element CS than for those given the flavor-odor compound as the CS. This retention effect was due to a surprisingincrease in the conditioned aversion observed 21 days after conditioning with the single-element CS. A second experiment confirmed this paradoxical increase in retention of the aversion to chocolate milk. This experiment also verified that no such increase occurred in retention of the conditioned aversion to a different flavor (saccharin), whether the initial aversion was strong or weak. The results may be explained in terms of generalized latent inhibition from consumption of mother’s milk.     

Preweanling and adult rats treat conditioned light-tone combinations differently

Ontogenetic differences in processing light-tone compounds were discovered in preweanling (17-day-old) and adult (60–80-day-old) rats. Suppression of general activity was used as an index of the magnitude of conditioned fear following a single training session in which a CS+ was paired with mild footshock. In Experiment 1, rats were trained on discriminations in which the CS? consisted of a light and the CS+ was either a tone alone (simple discrimination) or a light-tone compound (simultaneous feature-positive discrimination). Adults and preweanlings given each type of discrimination were then tested for fear of the CS? and a target stimulus (tone alone or light-tone compound). Adults in all groups displayed greater fear of the target than of the CS?. Preweanlings, however, discriminated the CS? from the target only when the target was the same as the original CS+. Experiment 2 revealed that age-related differences in conventional stimulus generalization is not a likely explanation for the pattern of results found in Experiment 1. Experiment 3 revealed age-related differences in expressed fear of a serial feature-positive discrimination; adults, but not preweanlings, showed greater fear of the compound than of the CS?. Alternative interpretations of the results from these experiments are discussed, and the general conclusion is that adults appear more inclined to process elements of a compound stimulus selectively, whereas preweanlings seem more likely to process the compound unselectively, with roughly equivalent processing of each element.     

The influence of the information value provided by prior-cuing treatment on the reactivation of memory in preweanling rats

In two experiments, the influence of exposure to a CS? on the acquisition and retention of a conditioned odor aversion was examined. Preweanling rats were given exposure to the CS? either prior to (CS?/CS+) or following (CS + /CS?) the pairing of a second odor (the CS+) with footshock. The results of Experiment 1 indicated that subjects in both of the treatment conditions acquired aversions of comparable strength to the odor paired with footshock and that retention of the odor aversion was not affected by order of stimulus presentation during conditioning. Experiment 2 indicated, however, that the effectiveness of pretest exposure to various elements of the conditioning episode in reactivation of the memory for conditioningwas dependent on the order of stimulus presentation during conditioning. This differential effectiveness of the various reactivation treatments is discussed in terms of their relationship to the associative “status” of the stimuli present during conditioning and in terms of the information provided to the animal by the reactivation treatment.     

Novelty of contextual cues in taste aversion learning

The purpose of this experiment was to test the theory of Lubow, Rifkin, and Alek (1976) concerning the effects of stimulus preexposure on later learning. This hypothesis predicts that conditioning will occur faster when either the stimulus or the testing environment is novel relative to the other than when the stimulus and the environment are equally novel or equally familiar. The theory was tested in a taste aversion conditioning paradigm in which groups of rats were presented with either the familiar (preexposed) solution or the novel nonpreexposed solution, in either the familiar or the novel environment. Conditioning was affected by the novelty of both the stimulus and the environment, with novel stimuli enhancing learning and novel environments retarding it. However, no interaction between stimulus and environmental novelty was evident, and thus Lubow’s hypothesis was not confirmed.     

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.