Flavor-illness aversions: potentiation of odor by taste is disrupted by application of novocaine into amygdala

Taste and odor have different properties in toxiphobic conditioning. When each is used alone, taste becomes aversive when followed by immediate or delayed poison, while odor becomes aversive only if followed by immediate poison. However, if odor and taste are presented as a compound and followed by delayed poison, then odor does become aversive when tested alone. It is as if taste has potentiated the odor signal. Several experiments assessed the role of the amygdala in this potentiation effect by anesthetizing the amygdala with 10% novocaine. Novocaine applied 30 min before presentation (Pre-CS) of an odor-taste compound disrupted the potentiated odor aversion but not the taste aversion. In contrast, novocaine applied 1 min after the compound odor-taste or 1 min prior to LiCl poison did not dissociate odor and taste aversions; both odor and taste aversions were facilitated. Novocaine applied 30 min before an odor alone also disrupted an odor aversion induced by immediate LiCl. But identical treatment did not disrupt odor avoidance conditioned by immediate foot-shock, suggesting that amygdala anesthesia does not simply produce anosmia. Pre-CS novocaine treatment also disrupted flavor neophobia prior to conditioning. The results suggest that novocaine applied to the amygdala disrupts the integration of odor with taste and illness during toxiphobic conditioning.     

Developmental flavor experience affects utilization of odor, not taste in toxiphobic conditioning

Feeding experiences were varied in developing rats and the effects upon flavor neophobia and lithium chloride-induced flavor aversions were observed. In Experiment 1, nursing experience of neonate rats was reduced by artificial feeding via intragastric cannula; the rats then were tested with apple juice paired with lithium chloride injection at weaning or maturity. Conditioned aversions were not affected, but neophobia to novel apple juice was attenuated in artificially-reared rats tested at maturity. In Experiment 2, rats received enriched feeding experience after weaning, which consisted of (a) obtaining many complex flavors, a few of which were paired with poisoning, effortlessly in the home cage, or (b) foraging for various foods on an elevated maze. No dramatic effects on neophobia or conditioned taste aversion for saccharin water were apparent. In Experiment 3, rats were given experience after weaning with vanilla-scented water either paired or unpaired with quinine water, and then tested with the odor of almond or that odor compounded with saccharin water for neophobia and lithium-induced aversions. Flavor-experienced rats exhibited more pronounced odor conditioning and more resistance to extinction of the odor aversion after both simple and compound conditioning. In contrast, saccharin taste aversions were relatively unchanged. Apparently, enriched feeding and drinking experience facilitates the utilization of odor more than taste cues.     

Simultaneous odor-taste and taste-taste compounds in poison-avoidance learning

In six experiments, rats received an odor or a taste alone or in simultaneous compound with another taste prior to lithium chloride-induced illness. Aversions to the target odor and the target taste were then assessed. In Experiments 1–3, the presence of the taste in compound with the target during conditioning attenuated the strength of the aversions to both the target odor and the target taste. Although these results were consistent with the familiar principles of compound conditioning, they contradicted previous reports of potentiation, rather than attenuation, of odor conditioning by taste. In Experiment 4, taste again attenuated the conditioning of odor when a second odor was presented during the CS-US interval. In Experiment 5, we looked for odor potentiation with a within-subject design, and in Experiment 6, we examined an alternative method of presenting odor. In neither case did we find odor potentiation by taste. Over the range of conditions investigated here, a taste often attenuates, and never potentiates, the conditioning of aversions to both odors and tastes.     

Taste preconditioning augments odor-aversion learning

On the basis of previous work that has shown a taste can potentiate odor-aversion conditioning in AX+ conditioning, 6 experiments used rats to examine the effects of pairing a preconditioned taste (A) with a novel odor cue (X) in an A+/AX+ aversion conditioning design. Experiments 1A and 1B demonstrated that a preconditioned taste produced a robust odor aversion that was significantly stronger than a potentiated odor aversion. The results of Experiment 2 showed that the robust odor aversion produced by A+/AX+ conditioning was not the result of the potentiated odor aversion summating with generalization from the taste aversion. The augmented odor aversion was produced only when the taste and odor stimuli were presented simultaneously (Experiment 3) and the preconditioned taste aversion was intact at compound conditioning (Experiment 4). Pairing a novel odor with a preconditioned taste was not sufficient to condition an aversion to odor (Experiment 5), although other results implicated a role for an association between odor and taste in the odor augmentation effect (Experiment 6). The present results have implications for current models of taste + odor interactions in flavor-aversion conditioning.     

Potentiation of a conditioned taste aversion in preweanling and adult rats

Preweanling (18 days old) and adult rats were made ill with LiCl either 2 min or 1 hr after tasting controlled amounts of either one of two single flavors (saccharin or NaCl) or a compound mixture of the two. Conditioning was assessed with a single test 4 days later relative to explicitly unpaired control conditions. Generally, potentiation of the aversions to either flavor occurred for animals conditioned to the compound. The potentiation effect was decreased or eliminated by nonreinforced exposure to the alternative flavor of the compound. These effects tended to be stronger for the younger rats. Specifically, adult animals did not express potentiation of the saccharin aversion whereas preweanlings expressed potentiated salt aversions. Nonreinforced exposure to the alternative element eliminated the potentiation effect. Conditions conducive to potentiation are discussed in light of investigators who have not observed this effect in similar studies with compound stimuli.     

Characteristics of taste-mediated environmental potentiation in rats

When rats drink a novel flavor in a distinctive environment and are injected with lithium, potentiated aversions are established to the environment as evidenced by the animals' unwillingness to consume a familiar, nonaversive flavor in this environment. Experiment 1 demonstrates that this potentiation is due to the presence of both the distinctive taste and the environmental cues on the conditioning trials, not simply aversive conditioning to each element or to generalization between the two elements. This potentiation phenomenon was shown to be sensitive to the novelty of the potentiating flavor in Experiment 2. Experiment 3 demonstrated that second-order conditioning is difficult to establish using these procedures, although Experiment 4 revealed that postconditioning extinction of the aversive flavor interfered substantially with environmental potentiation. These outcomes are discussed in terms of their implications for adaptive adjustments in feeding behavior as well as for more general conceptions of associative learning.     

Effects of preexposure flavor concentration on conditioned aversion and neophobia

In Experiment 1, 128 experimentally naive, water-deprived rats (Rattus norvegicus) received pretraining access to either 0.25 or 1.5% saccharin, distilled water, or 2.0% saline, followed either by a pairing of 0.25 or 1.5% saccharin with an intraperitoneal injection of 0.15 M lithium chloride (LiCl) or by a pairing of distilled water with LiCl. Preexposure to either saccharin concentration reliably reduced conditioned aversion effects to 0.25% saccharin, relative to that for preexposure to distilled water or saline. But only preexposure to 1.5% saccharin reduced aversion effects to that concentration. In Experiment 2, 48 naive, water-deprived rats received preexposure procedures as in Experiment 1. Afterwards, the rats were tested for neophobia to 0.25 or 1.5% saccharin. Neophobia was reliably greater to the 1.5% concentration. However, preexposure to either saccharin concentration obliterated evidence for neophobia to saccharin, relative to that following preexposure to distilled water or saline.     

Flavour-odour compound conditioning: Odour-potentiation and flavour-attenuation

Five experiments employed a toxiphobia conditioning paradigm to examine the strengths of odour and flavour aversions when conditioned separately and in compound. When conditioned in compound, odour aversions were stronger than when conditioned separately, i.e., the flavour potentiated the odour (Experiment Ia), but flavour aversions were weaker than when conditioned separately, i.e., the odour attenuated the flavour (Experiment Ib). The duration of exposure to the reinforced compound governed the nature of the interaction between the components: at a brief exposure, the flavour overshadowed the odour; at a long exposure, the flavour potentiated the odour (Experiment II). The remaining experiments examined the mechanism subserving the potentiation effect. Experiment III demonstrated that extinction of the flavour associate of the odour attenuated the odour aversion but further conditioning of the flavour did not strengthen the odour aversion. Experiment IV confirmed this effect of extinction but also found a comparable attenuation of the odour aversion from extinction of a separately conditioned flavour. Experiment V examined the previous failure to influence the strength of the odour aversion by strengthening the flavour aversion. In this experiment, conditioning the flavour associate or a separately conditioned flavour with a more potent US augmented the strength of the odour aversion. The results did not provide support for the idea that the potentiation phenomenon reflects the formation of within-compound associations but did indicate that a potentiated odour aversion could be modulated by manipulations designed to alter the US representation.     

Potentiation of latent inhibition

Rats were given exposure either to an odor (almond) or a compound of odor plus taste (almond plus saline), prior to training in which the odor served as the conditioned stimulus. It was found, for both appetitive and aversive procedures, that conditioning was retarded by preexposure (a latent inhibition effect), and the extent of the retardation was greater in rats preexposed to the compound (i.e., latent inhibition to the odor was potentiated by the presence of the taste). In contrast, the presence of the taste during conditioning itself overshadowed learning about the odor. We argue that the presence of the salient taste in compound with the odor enhances the rate of associative learning, producing a rapid loss in the associability of the odor. This loss of associability will generate both overshadowing and the potentiation of latent inhibition that is observed after preexposure to the compound.     

Associative interference with taste aversions after contextual discrimination learning

In two experiments, rats were first given discriminative training with two distinctive contexts, such that a flavor was paired with lithium chloride (LiCl) in one context, alternating with presentations of the flavor alone in another context. Contextual control of the fluid ingestion was observed in that rats reduced the fluid intake in the LiCl-paired context but drank the solution in the context never paired with lithium. Having learned this discrimination, the rats were now given a second flavor in their home cage before being injected with LiCl and transferred to the previously lithium-paired context. In Experiment 1, the acquisition of an aversion to the novel flavor was blocked when this flavor and the contextual cues are conditioned as a compound. In Experiment 2, the blocking effect and the conditional control over fluid consumption were abolished when the associative strength of the LiCl-paired context had been extinguished by exposing the animals to water in the contexts after discriminative training. These results are interpreted as evidence that context dependency of conditioned taste aversions is mediated by a summative effect of the context–LiCl and flavor–LiCl associations.     

Augmentation, not blocking, in an A+/AX+ flavor-conditioning procedure

An A+/AX+ Pavlovian conditioning design typically produces weakened or blocked conditioning to stimulus X. Two experiments were conducted in which rats first received an odor (A+) paired with an emetic US, and then received odor and taste (AX+) paired with the US. In both experiments, the preconditioned odorfacilitated conditioning to the taste. In Experiment 1, a group that received two odor-illness pairings in A+ conditioning had a stronger taste aversion than a group that only had a single odor-illness pairing. Experiment 2 demonstrated that the strengthened taste aversion in the A+/AX+ condition was not due to stimulus generalization. The results represent a unique outcome in the flavor-aversion literature that is similar to potentiation. We propose that this facilitated conditioning to X in the A+/AX+ design be termedaugmentation.     

Role of telereceptive and interoceptive (taste) cues in ingestional neophobia in chicks (Gallus domesticus)

Experiment 1 investigated the influence of telereceptive (visual) and interoceptive (taste) cues on neophobia by measuring the intakes of clear water and novel solutions of red-colored water, clear 4.0% vinegar, or red-colored 4.0% vinegar in chicks (Gallus domesticus) on 5 test days. Neophobia was reliably greater the more numerous the novel stimuli in testing (i.e., red-colored vinegar) but was similar in magnitude for novel visual and novel taste cues alone. In Experiment 2 chicks received zero, one, or five preexposures to red-colored water or to clear 4.0% vinegar and were tested for neophobia to red-colored 4.0% vinegar. Intake of red vinegar reliably increased with the number of preexposures. However, preexposure to red-colored water facilitated intake of red vinegar more than preexposure to clear 4.0% vinegar did. These results suggest that the familiarity of telereceptive (visual) stimuli attenuates the demonstration of taste neophobia.     

Demonstrations of neophobia and enhanced neophobia in the albino rat.

The conditions under which neophobia and enhanced neophobia occur in the albino rat were studied. Neophobia to a .1% saccharin solution was demonstrated in a 10-min single-bottle test. This neophobia was enhanced by pairing water ingestion with a radiation exposure of 100 r. or an injection of lithium chloride 24 hr prior to the saccharin test. In addition, it was found that the differences in consumption of saccharin in a 10-min single-bottle test due to neophobia and enhanced neophobia were produced by consistent differences in drinking rates which appeared early in the 10-min period. The disappearance of neophobia and enhanced neophobia in a 1-hr single-bottle test suggested that the effects of neophobia and enhanced neophobia are short-lived and are best measured in a brief single-bottle test. Finally, enhanced neophobia was not found when 2 days of water drinking were interposed between LiCl poisoning and saccharin testing.     

Taste Aversion Learning Based on Swimming and Lithium Chloride Injection in Rats: Implications From Cross-familiarization Tests and Stimulus Selectivity1

In rats, swimming causes avoidance of the taste solution consumed immediately before the swimming. Several lines of research have shown that this taste avoidance reflects Pavlovian conditioned aversion based on correlations between the taste and swimming-induced nausea. The present research compared swimming-based taste aversion learning (TAL) with conventional TAL based on nausea-inducing lithium chloride (LiCl). By exploiting cross-familiarization techniques, Experiments 1A and 1B suggested that different physiological states are induced by swimming and LiCl. This claim was supported by Experiment 2, which reports stimulus selectivity in saccharin and sucrose aversions based on swimming and LiCl.     

Potentiation by a novel flavour of conditioned place aversions based on both toxicosis and shock

Three experiments examined how a flavour modified the development of aversions to the place in which it was presented and paired with a reinforcer. Experiment 1 confirmed the cue-to-consequence effect: rats made sick after exposure to a flavour in a novel place (Skinner boxes) displayed stronger aversions than shocked animals when they were presented with the flavour in a second, familiar place; rats shocked after exposure to water acquired stronger place aversions than animals made sick. Experiment 2 confirmed the potentiation effect: rats made sick after exposure to the flavour developed stronger place aversions than those made sick after ingestion of water. This experiment also revealed that rats shocked after exposure to the flavour likewise acquired stronger place aversions than the animals shocked after ingestion of water. Experiment 3 replicated this flavour potentiation of place aversions based on shock. The results are not consistent with Garcia, Lasiter, Bermudez-Rottoni, & Deems' (1985) account of how a flavour interacts with an aversive reinforcer to modify what is learned about its associates in a compound.     

Potentiation and blocking of conditioned flavour and context aversions

Experiments 1, 2, and 3 demonstrated that the place in which rats had been made sick subsequently blocked the development of an aversion to a novel flavour that was presented in that place and paired with illness. These experiments also showed that a poisoned flavour subsequently potentiated the acquisition of an aversion to a novel place in which it was presented and paired with illness. Experiments 4 and 5 examined the hypothesis that the potentiation effect was mediated by the association between the place and the averted flavour rather than by the association between the place and the illness. However, there was no evidence that the place acquired aversive control over ingestive behaviours simply as a consequence of it having contained the averted flavour. Further, reinforcement of the aversive flavour outside the place-flavour compound increased flavour aversions but decreased, rather than increased, place aversions. These failures to detect evidence for an association between the place and the poisoned flavour led to a consideration of whether the animals were sensitive to the relation between the place and the poisoned flavour. Experiment 6 demonstrated that the potentiation effect was in fact contingent upon the relation between the place and the poisoned flavour, as was required by the view that the poisoned flavour had facilitated the association between the place and the illness.     

Aversion conditioning and enhanced neophobia: role of test stimuli

In Experiment 1, 100 rats (Rattus norvegicus) received 10% sucrose or 5% casein hydrolysate followed, after 10 min, by a LiCl or saline injection or, after 12 h, by a LiCl injection. Subsequently, rats received aversion testing to the CS or neophobia testing to the opposite novel flavor. Aversion effects were reliably greater to casein than to sucrose. However, conditioning with sucrose yielded a reliably greater increase in neophobia to casein (relative to controls) than conditioning with casein yielded to sucrose. In Experiment 2, 60 rats received distilled water followed, after 10 min, by LiCl or saline injection or, after 12 h, by LiCl injection. Aversion effects occurred to distilled water. Neophobia testing to casein and sucrose showed that, relative to controls, neophobia increased reliably more to casein. The results of Experiments 1 and 2 were not attributable to differences in baseline intakes between casein and sucrose flavors. Together, these experiments indicated that the demonstration of conditioning-enhanced neophobia may depend more on the characteristics of the neophobia test flavor than on the strength of aversion established because of CS characteristics.     

Potentiation by a taste of toxicosis-based context conditioning: Effects of varying the test fluid

Rats that drank water in a distinctive environment and were then injected with lithium chloride (water-lithium condition) were compared with those given an added taste on those conditioning sessions (sucrose-lithium condition). In three experiments this taste potentiated a conditioned aversion to the context, as measured by suppression of intake of another solution: either a novel sour taste (Experiments 1 and 2) or a familiar saline solution (Experiment 3). In contrast, this potentiation effect was not detected when subjects were tested with water, whether a high or low dose of lithium was used (Experiment 2). Instead, in Experiments 1 and 2 water-lithium subjects drank less water than did the sucrose-lithium subjects on such tests i.e. an apparent overshadowing effect, which was the opposite outcome to that found previously using almost identical procedures. Intake on recovery sessions in another context suggested that, when water is used as the test fluid, potentiation can be masked by two factors: a context-dependent aversion to water in water-lithium subjects, and a conditioned inhibition effect of water in sucrose-lithium subjects. These may account for previous failures to detect potentiation of context conditioning.     

Augmentation of taste conditioning by a preconditioned odor.

Five experiments explored facilitated taste-aversion conditioning (odor-mediated taste augmentation), using rats that experienced odor (A) and taste (X) in an A+/AX+ design. Augmentation occurred when the stimuli were presented simultaneously during AX+ conditioning, and significantly weaker conditioning occurred after a sequential presentation (Experiment 1). Experiments 2 and 3 demonstrated that augmented conditioning decreased if the odor aversion was reduced through preexposure or extinction following A+ conditioning. A second-order conditioning explanation was not supported by the results of Experiment 4. Experiment 5 showed that extinction of the odor aversion after AX+ conditioning did not alter the strength of the augmented taste aversion. Odor-mediated taste augmentation is similar to potentiation, in which odor and taste cues operate in a synergistic, not competitive, manner.     

Taste potentiation of auditory aversions in rats (Rattus norvegicus): a case for spatial contiguity

An aversion for an auditory stimulus was established in laboratory rats when a tone was spatially and temporally contiguous with a novel taste in a food conditioned stimulus compound followed by toxicosis. The procedure involved varying the location of the tone relative to a novel tasting food. During toxicosis conditioning, one group ate sweet food with a speaker located in the food, two groups ate sweet food with the speaker displaced (near or far) from the food, and a fourth group was presented with a tone without food available. It was found that the potentiation of auditory aversions required both the presence of a novel taste and spatial contiguity between the taste and the tone.